Psychological Bulletin

1984, Vol95, No. 1,3-28

Copyright I984t>y the

American Psychological Association, Inc.

Neuropsychological Studies of the Frontal Lobes

Donald T. Stuss
Schools of Medicine (Neurology) and Psychology
University of Ottawa and
Ottawa General Hospital, Ottawa,
Ontario, Canada

D. Frank Benson
Department of Neurology
University of California, Los Angeles,
School of Medicine

This review summarizes the current state of knowledge of prefrontal lobe functions
as derived from studies and observations of adult humans following frontal lobe
damage. Following an overview of the neuroanatomy and neuropathology, frontal
lobe activities are presented under the following headings: motor functions; sensory,
perception and construction functions; attention; abnormal awareness; flexibilityperseveration; language; memory; cognition; personality; localization; and hemispheric activity. Six specific prefrontal functions are suggested as the principal
disorders underlying many if not all of the described manifestations.
In 1928 the American neurologist Tilney
suggested that the entire period of human evolutionary existence could be considered the
"age of the frontal lobe." A great deal of indirect evidence supported such a claim. Specific knowledge of frontal lobe functions, however, has remained relatively limited and hypotheses concerning these functions remain
controversial, a state reflected in the wellknown description of activities of the frontal
lobes as a riddle (Teuber, 1964). Some authors
credited frontal association cortex with the
highest intellectual and moral functions (Halstead, 1947; Rylander, 1939), whereas others
were unable to confirm exclusive roles for this
cortical area (Hebb, 1945; Mettler, 1949; Teuber, 1959; Weinstein & Teuber, 1957).
Several reasons can be rioted for the continuing riddle, Many frontal lobe lesions produce no primary neurologic deficits; therefore,
possible subtypes of frontal lobe dysfunction
cannot be readily demarcated by neighborThis study was supported in part by Grant #NSO6209
from the National Institutes of Health to Boston University
School of Medicine,-the Research Service of the Veterans
Administration,' University of Ottawa Faculty of Social
Sciences Grant, the National Research Council of Canada,
the Ontario Mental Health Foundation, and the Augustus
S. Rose Endowment Fund. The library search assistance
of Francine Sarazin is gratefully acknowledged. Bonita
Porch is thanked for the preparation of the manuscript.
Requests for reprints should be sent to Donald T. Stuss,
Human Neurosciences Research Unit, RM 2166, University of Ottawa, 451 Smyth Road, Ottawa, Ontario K1H
8M5, Canada.

hood neurologic findings. Because these deficits cannot be subclassified, the term frontal
lobe syndrome is used to refer to an amorphous, varied group of deficits, resulting from
diverse etiologies, different locations, and varir
able extents of abnormalities. A second source
of confusion stems from inappropriate assessment procedures, lack of adequate control
groups, and interinvestigator variations in test
procedures. In addition, frontal lobe pathology
is often misinterpreted as a psychiatric problem. When the subtlety of deficits, the wide
variations of symptomatology, and lack of
clarification from neurologic, psychologic, and
psychiatric disciplines are considered together,
the reason the activity of the frontal lobes remains a riddle becomes clear.
This review will briefly view the current
state of knowledge of frontal lobe functions.
Somewhat arbitrarily the frontal lobe activities
will be presented as phenomenological units
with the major focus on behavioral changes
that occur in adult humans following acquired
frontal lobe damage. Reference to the animal
literature will be limited to corroborative evidence, except for the section on neuroanatomy, where nonhuman data is the basis.
Neuroanatomical Considerations
Anatomically the frontal lobes are the massive cerebral area anterior to the rolandic fissure and above the sylvian fissure. There are
two roughly symmetrical lobes, each of which
can be further divided into three main areas:

DONALD T. STUSS AND D. FRANK BENSON

dorsal-lateral, medial, and basilar-orbital. Actually, the frontal lobe may be divided in a
number of ways.
First, using Brodmann area numbers, three
major subdivisions are noted. Area 4, the precentral gyrus, is the primary motor area, with
Area 6 and the posterior part of Area 8 called
the premotor area. Areas 44 and 45, also
known as Broca's area, are considered part of
the premotor area (Jouandet & Gazzaniga,
1979). Area 8 represents the frontal eye fields.
The remainder of the frontal lobe, including
Areas 9, 10, 11, 12, 46, 47, 13, 14, and 15, is
called prefrontal cortex, and can be further
subdivided into basal-medial (9-13, 24, 32),
dorsal-lateral (9, 10, 11, 12, 46, 47), mesial
(9, 10, 11, 12), and orbital (10, 11, 12, 13, 14,
15, 47). Functional differences between these
sections are not clear, but some postulates will
be discussed.
As a second approach, three main cytoarchitectural divisions can be outlined in the
frontal cortex. Agranular cortex refers to the
motor area (Areas 4 and 6), in which the external pyramidal layer (III) and internal pyramidal layer (V) are so large that they become
one deep layer, with virtually no internal granular layer (IV). In the prefrontal cortex, on
the other hand, Layer IV, the inner granular
layer, reappears producing a distinct granular
cortex. Lying between the granular and agranular cortices is a third, transitional area called
the dysgranular cortexthe frontal eye field.
A third anatomical definition of the frontal
lobe concerns thalamic-cortical connections
(Akert, 1964; Goldman, 1979; Nauta, 1971).
The motor cortex receives projections from
the ventral lateral nucleus and the premotor
area from the medial ventral anterior nucleus.
The prefrontal cortex is directly connected to
the dorsal medial nucleus of the thalamus and
appears to be divisible into several distinct
regions. Important connections also exist between frontal and nonspecific thalamic nuclei
(Goldman, 1979; Scheibel & Scheibel, 1967).
Territories of vascular distribution provide
yet another means of subdividing the frontal
lobes. The dorsal-lateral convexities are primarily served by the middle cerebral artery,
the medial frontal areas by the anterior cerebral
artery. The lateral orbital surface is middle
cerebral territory, whereas the medial orbital
area is fed by the anterior cerebral.

The importance of the frontal lobes derives

from rich connections, both afferent and efferent, with almost all other parts of the central
nervous system. Frontal connections with cortical sensory areas, providing information from
the external milieu, occur either by direct cortical-cortical afferents or via the thalamus. The
occipital, parietal, and temporal sensory association cortices connect to both the anterior
temporal and the inferior parietal areas; in
turn, each of these has direct afferent connections to the frontal cortex. There is a difference, however. The inferior parietal-frontal
connection is distributed over a wide, primarily
dorsal-lateral area, while the temporal-frontal
connection projects both to dorsal-lateral and
orbital cortex (Nauta, 1971, 1972).
Knowledge of these connections is becoming
more specific. The dorsal bank of the sulcus
principalis on the dorsal-lateral convexity has
four primary ipsilateral connections (Goldman
& Nauta, 1977b). There are parallel contralateral projections, apparently allowing the two
hemispheres to converse. An ipsilateral-contralateral projection initiates as well from the
posterior-medial orbital frontal area.
The prefrontal cortex receives projections
from olfactory sensation; it is thus the only
cortical area interacting with all four sensory
modalities (Nauta, 1971,1972). Two olfactoryfrontal pathways have been described (Potter
& Nauta, 1979).
The frontal lobes also have well-developed
connections with limbic and subcortical areas
that provide monitoring of the internal milieu
(Nauta, 1971, 1972, 1973). Most of these
pathways proceed via the dorsal medial (DM)
nucleus of the thalamus and are transmitted
either to the orbital-frontal cortex (medial DM
cells) or to the convexity (lateral DM cells).
In addition, there are some primary efferent
limbic connections that traverse directly to the
cingulate gyrus. These cingulate-frontal connections are specific (Pandya, Van Hoesen, &
Mesulam, 1981).
The connections between the brain stem
and frontal lobes are partially discussed in
other sections, including frontal-limbic and
frontal-thalamic connections. Luria (1973)
indicates that the frontal lobes are involved
in the regulation of arousal and tone through
the activating input to the brainstem reticular
formation from the orbital and medial frontal

NEUROPSYCHOLOOICAL STUDIES OF THE FRONTAL LOBES

cortex. This reticular system is generally divided into two parts (Benson & Geschwind,
1975)the brainstem reticular formation,
which modulates and modifies arousal (Bremer, 1954; Moruzzi & Magoun, 1949; Rossi
& Zanchetti, 1957), and the interlocking but
essentially antagonistic system, the diffuse
thalamic projection system (DTPS), which
controls phasic activity. It has been suggested
that this frontal-brainstem reticular system
(including thalamus) is an apposed but complementary selective gating system, providing
control of the most complex forms of conscious activity (Scheibel, 1980).
Three main brainstem connections to dorsal-lateral prefrontal and cingulate cortex,
corresponding to known monoamine pathways, have been reported (Porrino & Goldman-Rakic, 1982). These connections are from
the ventral midbrain, the central superior nucleus and caudal portion of the dorsal raphe
nucleus, and from the locus coeruleus and
proximal medial parabrachial nucleus. Approximately similar projections to the orbital
prefrontal cortex were also noted. The prefrontal cortex is closely linked with the brainstem areas of sleep and arousal.
Frontal-tectal connections are derived not
only from frontal eye field zones (Astruc, 1971;
Kuypers & Laurence, 1967), but also from the
middle third of the dorsal bank of the principal
sulcus (Goldman & Nauta, 1976). In addition,
there are connecting pathways between the
principal sulcus and the nearby frontal eye
fields.
Knowledge of prefrontal-striatal pathways
indicates that the frontal cortex projects not
only to the head of the caudate (projections
are maximum here), but also to the entire
caudate (Goldman & Nauta, 1977a). It appears
that cortical zones that are connected with
each other also have projections, at least in
part, to the same area in the caudate (Yetarian
& Van Hoesen, 1978).
At best, this brief synopsis of the anatomy
of the frontal lobe and its connections suggests
a possible cognitive globe on which our
knowledge of frontal lobe functions may be
mapped. Although cytoarchitectural specificity
appears lacking, some degree of functional definition to the different frontal regions and the
related frontal systems may be inferred from
their anatomical connections.

Neuropathology
The wide variety of etiologies that can produce frontal lobe dysfunction constitutes a
major element in the riddle of the frontal lobes.
Only a brief synopsis of the many recognized
problems can be described here and these will
be subdivided, somewhat artificially, into the
following three groups for ease of discussion:
primary neurologic disorder, frontal brain
trauma, and frontal psychosurgery.
The first of these subgroupings is the most
difficult to discuss because it contains a myriad
of widely different disorders. Some of the disorders are widespread, affecting much of the
brain, but show some degree of predilection
for frontal structures (e.g., general paresis of
the insane); others involve subcortical structures primarily, affecting frontal function only
secondarily. Nonetheless, they are often listed
among frontal disorders (e.g., Huntington's
disease, multiple sclerosis). Cerebral vascular
disease is only rarely a purely frontal phenomenon. With the exception of the relatively
uncommon obstruction of the anterior cerebral artery, most strokes that involve the frontal lobe also cause damage to deep structures,
to more posterior structures, or both. Even
brain tumors, which can arise totally within
the frontal lobe, almost always produce distant
effects (pressure phenomena, vascular insufficiency) before being recognized as a frontal
disorder. Primary neuropathological involvement restricted to the frontal lobes is rare;
most consequent behavior is contaminated by
distant effects. Nonetheless, most of the accepted descriptions of frontal phenomenology
derive from such clinical sources. In particular,
much of the masterful work on the frontal
lobes produced by A. R. Luria over the years
(1965, 1966, 1969, 1973) was derived from
his evaluations of patients with frontal lobe
tumor and, despite the recognized limitations,
represents some of the best clinical-pathological observations currently available.
Trauma to the brain deserves separate consideration. Whereas closed head trauma tends
to have widespread cerebral consequences,
some open head injuries, particularly those
produced by high velocity missiles or shrapnel,
can produce relatively localized frontal damage. Because of the large size and comparatively great distance from essential, more cen-

DONALD T. STUSS AND D. FRANK BENSON

trally located brain structures, significant

frontal damage is often compatible with life,
leaving the person behaviorally disturbed but
otherwise relatively intact. The literature contains many excellent descriptions of such individuals (Faust, 1960; Feuchtwanger, 1923;
Kleist, 1934a) and a great deal of the knowledge of frontal lobe psychiatric symptomatology stems from this source (Lishman,
1966). It must be recognized, however, that
brain injury is never totally focal, and the wide
variety of both neighborhood and distant
symptomatology contaminating these studies
represents another source of confusion in the
clinical descriptions of frontal phenomenology.
Psychosurgery can be considered the third
major etiologic source of data on frontal function. In the late 1940s and early 1950s many
(probably over 100,000) prefrontal destructive
procedures were performed. Most were bilateral and, technically, were fairly exact. As such,
prefrontal leukotomy could be expected to
yield considerable information concerning behavior following focal frontal lobe damage; the
outcome, however, has been disappointing.
Several obvious factors can be cited as the
source of this problem. For one, most individuals who underwent prefrontal psychosurgery were behaviorally abnormal (schizophrenic, phobic, depressed, violent); presurgical evaluation was difficult (and rarely done),
and postoperative findings were often contaminated by the premorbid behavioral problems.
In addition, most of the diagnostic procedures
performed in those years were limited to psychiatric outcome; little attempt was made to
study alteration in any behavior except the
premorbid problem. The follow-up after psychosurgery was characteristically short (average
duration less than 6 weeks but often only overnight). The few psychologic studies of frontal
function in these subjects concentrated on intellectual competency and failed to demonstrate other aspects of frontal damage (Greenblatt & Solomon, 1958/1966; McKenzie &
Kaczanowski, 1964; Valenstein, 1977). Even
these studies were limited to short postoperative duration. Very few long-term studies of
frontal lobe function have been made in patients who had undergone psychosurgery, and
most of these have been limited both in terms
of the evaluation performed and in the number
of patients examined. Recently, however, a se-

ries of reports have been published of neurological, neuroradiological, and a comprehensive battery of neuropsychological tests administered to a small number of individuals
who had undergone prefrontal leukotomy 25
to 30 years earlier (Benson et al, 1981; Naeser,
Levine, Benson, Stuss, & Weir, 1981; Stuss,
Kaplan, Benson, Weir, Naeser, & Levine,
1981).
Motor Functions
Of all frontal lobe functions, the control of
motor responses is the most obvious. It has
long been recognized that the frontal portion
of the brain subsumed motor actions, in contrast to the sensory activities of the parietal,
temporal, and occipital lobes (Meynert, 1872).
Bianchi (1895) posited that the frontal lobe
not only initiated the "final common pathway"
for brain responses but served to integrate information from other parts of the brain and
thus to modulate the final response. The resulting frontal motor activities are complex
and must be subdivided for study. Two of the
most significant portions of the frontal lobe,
the pre-central and the pre-motor areas, have
been well studied. Their motor functions are
described in all neuroanatomy texts and need
not be detailed here. The remaining motor
activities, those stemming from prefrontal area
participation, are far more complex and, to
date, defy specific descriptions. It is from this
system that sophisticated motor responses to
a variety of high-level stimuli are coordinated.
In global terms, the description of motor
function after prefrontal damage from any
etiology has been crudely separated into two
types, reflecting Kleist's (1934a) localization
differences. The hypokinetic patient is slow
and apathetic, responds in an automatonlike
manner, and demonstrates little initiative or
spontaneity (Blumer & Benson, 1975; Goldstein, 1944; Kleist, 1934a; Lishman, 1978;
Walch, 1956). Lesion localization tends to be
maximal in the prefrontal convexity, but this
"apathetico-akinetico-abulic" syndrome is
most typical of massive frontal lobe damage
(Luria, 1973). The second type, with major
pathology involving the orbital area, shows
hyperkinesis, restlessness, and impulsivity
(Feuchtwanger, 1923; Kleist, 1934a). Such patients may explode into action, respond ap-

NEUROPSYCHOLOGICAL STUDIES OF THE FRONTAL LOBES

Another major disturbance, the participapropriately, and then relapse into a constant
multidirected restlessness. Although both'types tion of prefrontal areas in praxis abnormality,
have been described frequently, the pathology is also controversial. Some exclude the frontal
is seldom so well localized as to provide pure lobes from any involvement in ideomotor,
examples.
ideational, constructional, and dressing
Examination of patients using different apraxia (Hecaen, 1969; Hecaen & Assal,
motor tasks led Luria (1965,1973) to postulate 1970). Others state that constructional and
at least two major types of motor disorder dressing disturbances are not truly apractic
following frontal lobe pathology. The first, phenomena (Benson & Geschwind, 1971).
caused by lesions in pre-motor zones, results Glossokinetic (melokinetic) apraxia was
in a problem in the execution of dextrous thought to involve Areas 4 and/or 6 exclusively
movements such as rhythm tapping or drawing (Fulton, 1937; Kleist, 1934b; Nielsen, 1951)
a series of symbols requiring an alteration of and may be more of a motor deficit than a
design. If the lesion also extended deeper to true apraxia (Hecaen & Albert, 1978). As such,
involve the basal ganglia, compulsive repeti- glossokinetic apraxia may be better described!
tion of an initiated action resulted. Thus, if as Luria's premotor syndrome.
the patient is asked to copy a circle, the moveThe frontal lobes do participate in some
ment is completed correctly but cannot be practic functions, however. Bucco-linguo-facial
inhibited, and a series of repetitive circular apraxia has often been described with lesions
movements ensue. This response suggests in- involving the left frontal motor association
tact motor programs allowing the patient to (i.e., premotor) cortex, although supramarcarry out the specified action; damage to the ginal gyrus and unilateral right hemisphere
control aspect of motor behavior, however, re- lesions have also been reported (Geschwind,
sults in the inability to cease the behavior.
1965; Goldstein, 1909;Hartmann, 1907; Rose,
The second major type of frontal motor dis- 1908). Unilateral limb apraxia has been reorder is more frequently associated with mas- ported after frontal' lobe lesions, and two types
sive prefrontal pathology in which the motor can be differentiated. Sympathetic or ideoprogram itself is disturbed so that the scheme motor apraxia (Geschwind, 1967; Liepmann,
of action is replaced by an inert stereotype. 1905), usually associated with Broca aphasia,
Luria devised many tasks that demonstrated apparently results from a lesion destroying the
this latter type of frontal motor control defect. origin of motor fibers in the dominant hemiFor example, if such a patient is asked to draw sphere that cross the corpus callosum to the
a circle, the movement is completed correctly homologous nondominant motor area. Anwithout superfluous lines. If then requested to other type, unilateral, kinetic apraxia of the
draw a cross, the patient draws another circle. magnetic type (Denny-Brown, ,1958) is said
Similarly, when asked to do the opposite of to occur with pathology in superior or medial
the examiner or to perform a conflicting action frontal cortex of either hemisphere, with or
the patient echoes the examiner. For instance, without involvement of the corpus callosum.
if told to tap twice when the examiner taps
There is a need for much further research
once and vice versa, these patients soon do in the motor difficulties that follow frontal lobe
exactly what the examiner is doing, even damage. Drewe (1975), for example, suggested
though they can still correctly verbalize the that the go/no-go task is not unitary in nature
requirements of the task. Imitative action is and that lesions in different frontal lobe regions
not lost and, in fact, is so strong that it over- could subserve different aspects. Motor deficits
comes the well-understood verbal directions. of the kinds described above could not be elicIn contrast, patients with promoter pathology ited in patients with large prefrontal leukotomy
are more likely to tap perseveratively, failing lesions (Benson & Stuss, 1982). Future reeven to imitate correctly. A third variation is search will require precise localization of lea go/no-go task requiring the patient to re- sion, sophisticated motor testing, and attention
spond to one signal but not to a second signal. to compensatory capabilities.
Inability to inhibit responses to the no-go sigIn summary, the motor functions of the
nal is frequently seen following prefrontal pa- frontal lobe are manifold and current knowlthology.
edge of any except the most primary functions

DONALD T. STUSS AND D. FRANK BENSON

remains vague. There is reason to separate

frontal motor activities into categories with at
least some relation to the sophistication of the
action and to correlate this separation with
different areas of frontal lobe. At this juncture,
however, even the categorization of frontal
motor activity must remain suspect, and few
firm conclusions can be made.
Sensory, Perception, and
Construction Functions
Neurologically, the frontal lobes are generally considered to be motor areas, without
primary sensory functions. Accumulating evidence from clinical observations and psychological research, however, implicates the frontal
lobes in a number of sensory-perceptual functions. One clear example is the clinical observation that unilateral sensory neglect, characterized by an inability to attend to one
sensory field (hemi-inattention) can be demonstrated opposite the side of some frontal
lobe lesions (Damasio, Damasio, & Chui,
1980). This may vary in intensity from a fullblown hemisensory defect to a minimal sensory deficit elicited only as unilateral extinction
to double simultaneous stimulation testing.
There is also strong experimental evidence
that frontal lobes and/or their connections are
relevant to the unilateral inattention phenomenon. Experimental lesions placed in the frontal lobes of animals can produce similar sensory abnormalities (Bianchi, 1895; Kennard,
1939; Welch & Stuteville, 1958). Unilateral
ablation of Area 8, the frontal eye field, can
produce a temporary contralateral visual field
neglect (Doty, 1973) despite intact visual field
perimeters (Jenkner & Kutschera, 1965). A
series of studies and observations by Heilman
and colleagues (Heilman & Valenstein, 1972;
Watson & Heilman, 1979; Watson, Heilman,
Cauthen, & King, 1973; Watson, Heilman,
Miller, & King, 1974) suggests that the attention-arousal deficit can be caused by lesions
in any portion of a sizeable frontal-limbicreticular loop. Their studies suggest that sensory inattention may be caused by lesions in
many different but interrelated areas of the
central nervous system, including the frontal
cortex. Unilateral inattention will be discussed
further in a later section, but this work clearly

shows that frontal and/or frontal system pathology can produce an apparent sensory loss
on the contralateral side.
Supportive evidence for the involvement of
the frontal lobes in sensory-perceptual functions has also been developed from psychological research. For instance, deficits in visual
search are commonly observed after frontal
lobe damage (Luria, 1973). With bilateral
frontal damage, inertia of gaze is so great that
visual attention can be focused on only one
aspect of the visual field. With lesser degrees
of pathology the deficit is better described as
disorganized visual search and can be demonstrated by monitoring eye movements during a patient's examination of a thematic picture (Luria, Karpov, & Yarbuss, 1966). When
asked to tell the meaning of a thematic picture,
frontal damaged patients would give an answer
based on their first visual fixation with little
attempt to monitor additionally with a full
examination of the picture. Eye movement
measurements verified this observation, revealing that whereas the eye movements of
normal subjects were directed and organized,
those of frontal lobe patients were haphazard.
Teuber, Battersby, and Bender (1949) also
examined visual search in patients with focal
frontal lobe damage. They used a task with
an array of 48 patterns scattered randomly
over a screen with a duplicate of one of the
patterns projected in the center of the field.
The subject was requested to actively search
for the match. Frontal lobe patients had prolonged search times with greatest difficulty in
the visual field contralateral to the unilateral
lesion, independent of any gaze paresis. The
investigators suggested that this could result
from disinhibition of occipital fixation mechanisms following loss of the (inhibitory) action
of the frontal eye fields. Patients with lesions
invading the frontal eye fields were also impaired in inhibiting initial saccades at a potentially distracting stimulus (Guitton, Buchtel, & Douglas, 1982). Cogan (1966) stressed
the importance of the frontal lobes in Balint's
syndrome, citing frontal influence on voluntary occular movements (to verbal command)
as well as an inhibitory effect on occipital centers. A similar explanation has been suggested
in a recently published case of Balint's syndrome (paresis of gaze on volition, optic ataxia,

NEUROPSYCHOLOGICAL STUDIES OF THE FRONTAL LOBES

and decreased visual attention) with both bifrontal and bilateral occipital pathology
(Hausser, Robert, & Giard, 1980).
The importance of the frontal lobes in sensory-perceptual tasks was given considerable
impetus by the research of Teuber and colleagues (Teuber, 1964). Despite nonimpaired
performance on tests of general intelligence,
attention, and memory, specific frontal lobe
deficits were demonstrated on sensory-perceptual tasks. Thus, using variations of the
Aubert task (tilting chair test), Teuber and
Mishkin (1954) did four experiments that
clearly disassociated frontal from parietal patients. Patients with frontal lobe damage were
most impaired when their body was tilted
while they attempted to set a line straight.
Parietal-damaged patients were most impaired
when the line was tilted against a conflicting
visual background. In general, frontal patients
made more overcompensatory mistakes,
whereas posterior patients and normals had
less overcompensation, possibly because their
intact frontal lobes could monitor and correct
sensory-motor imbalances.
Using the Necker Cube Test as an extreme
case of reversible figures, Cohen (1959) and
Teuber (1964) independently demonstrated
that frontal lobe lesions in either hemisphere
caused a significant decrease in a number of
reversals achieved in comparison to other
brain-damaged groups and normal subjects.
Dissociation between subject groups was also
achieved on a perceptual orientation task.
Right frontal-damaged patients were more
vulnerable on personal orientation tasks but
parietal lobe patients were inferior at tasks
involving orientation in their surroundings
(extrapersonal space).
Other visual-perceptual tasks have been
shown to be sensitive to frontal lobe pathology.
Although all patient groups performed poorly
on the picture arrangement subtest of the
Wechsler Adult Intelligence Scale (WAIS),
frontal-damaged patients (especially right)
tended to leave all or many of the pictures in
the presented order, compensating with loosely
connected explanations (McFie & Thompson,
1972; Walsh, 1978). On a measure of visualized relative movement, Albert and Hecaen
(1971) demonstrated that although more deficits occurred in the right hemisphere damaged

patients, the greatest degree of error occurred

with frontal lesions, and these could involve
either hemisphere. The importance of the
frontal lobes for this visual sensory task was
impressive. The authors suggested that the
perception of position appears to be a right
hemisphere function but that the perception
of relative movement apparently demands
frontal lobe activity.
The role of the frontal lobes in constructional disturbances has been controversial.
Many authors have excluded the frontal lobes
as the cause of constructional apraxia (Hecaen,
1969; Hecaen & Assal, 1970). Benton (1967)
and Benson and Barton (1970), however, demonstrated that lesions in either hemisphere of
the frontal lobe could result in constructional
disturbance. Luria and Tsvetkova (1964) proposed that construction disturbances represent
a disorder in one of the specific frontal lobe
functions of intention, programming, regulation, or verification. Lhermitte, Derouesne,
and Signoret (1972) demonstrated this in a
block design and complex figure movement
experiment. If the frontal-damaged patients
were presented the model for the block design
with each block outlined, or if they were taught
to copy the complex figure in a structured,
sequential fashion, their performance improved, suggesting that the deficit was primarily one of planning.
This short outline of sensory-perceptualconstructive functions of the frontal lobe suggests disturbances on a continuum from more
basic to higher perceptual levels. As the task
involves greater degrees of direction, organization, monitoring, and correction, it is more
likely to suffer if there is frontal lobe damage.
Whether this is the entire explanation, however,
remains to be determined.
Attention
Disturbance of attention is a common observation after frontal lobe damage. "From the
first examination of the (frontal lobe) patient,
the disorder of attention is noticeable: it is
necessary to repeat questions and orders several times to obtain a response" (Hecaen &
Albert, 1975, p. 139). Development of this
observation evolves from research on animals
with frontal lobe pathology performing tasks
that require delayed responses. Deficits were

10

DONALD T. STUSS AND D. FRANK BENSON

first considered an impairment of short-term patient is alert and may be able to follow commemory (Jacobsen, 1935). Subsequent studies, mands, yet is bewildered, distractible, and ofhowever, implicated a basic impairment in di- ten poorly oriented. With continued decrease
rected attention; for example, placing monkeys of the level of consciousness, a state of stupor
in the dark to eliminate distracting stimuli or coma is reached in which the patient has
produced improved performance (Isaac & De no meaningful interaction with the environVito, 1958; Malmo, 1942). Several concepts ment.
The clinical state that most clearly reprehave been postulated to explain the attention
deficits: hyperactivity (Orbach & Fischer, 1959; sents a primary disorder of attention or arousal
Richter & Hines, 1938); hyper-reactivity (Buf- is akinetic mutism in which there is an intact
fery, 1967; Ruch & Shenkin, 1943); and a def- sleep-wake cycle but little measurable cogicit in habituation (Grueninger & Pribram, nitive function. In this state no gross alteration
1969; Kimble, Bagshaw, & Pribram, 1965). A of sensory-motor mechanisms exist, but the
variation proposed that hyperactivity was patient lies inert and speechless (Bricolo, Turreally a disorder of cortical inhibition (Ko- azzi, & Feriotti, 1980; Segarra, 1970). Two
varieties of akinetic mutism have been pronorski, 1967).
Many observations of attentional deficits posed, based on lesion location (Benson &
have been made in humans suffering frontal Geschwind, 1975; Plum & Posner, 1980). One
lobe damage. Frontal tumors classically result type has the appearance of somnolence; the
in confusion, disordered arousal and alertness, patient is immobile with eyes closed. The reand impairment of attention (along with other sponsible lesion is classically described in the
deficits) (Hecaen, 1964). Frontal trauma may low neuro axis, primarily in the mesenceproduce similar results (Goldstein, 1936, phalic-diencephalic area. In the second type,
1944), as can frontal lobectomy (Angelergues, coma vigil (Benson & Geschwind, 1975), the
Hecaen, & Ajuriaguerra, 1956; Rylander, patient is immobile but the eyes freely follow
1939). Most of these clinical observations have visual stimuli, suggesting some level of vigibeen based on deficient responses to testing lance. The lesion for coma vigil involves the
or demonstration of easy distractability. The posteromedial-inferior frontal areas and/or the
concept of attention as a higher order phe- hypothalamus. The pathology underlying
nomenon deserves consideration, also. Atten- coma vigil, although usually accepted as being
tion has been described as the adoption of most severe in the frontal area, almost certainly
specific cognitive strategies in response to involves other cortical areas, also (Plum &
stimulus demand (Moscovitch, 1979). By this Posner, 1980).
The disorders of attention produced by
extended definition, many of the frontal deficits described by Luria (1973) can be consid- pathological involvement of the brainstemfrontal system can be conceptualized as exered deficits in attention.
Some human attention disorders have been isting on three levels: the reticular activating
categorized as specific clinical entities. They system providing tonic levels of arousal and
are usually described on two levels: arousal alertness, the diffuse thalamic projection sysand attending. Arousal reflects two factors: tem correlated with phasic levels of alertness,
first, the ability to be awakened and to main- and the frontal-thalamic gating system retain wakefulness; second, the ability to follow sponsible for selected and directed attention.
stimuli or commands. Another level, attention, Based on neuroanatomical and clinical corsignifies the ability of an alert individual to relations, this tripartite division provides a
direct effort and concentration for specific pe- conceptual aid for understanding the function
riods of time to specific tasks. Brain disease called attention. The brainstem-frontal system
may lead to varying degrees of altered arousal can be viewed as a unified and integrated comand attention (Plum & Posner, 1980). One plex with pathology in the brainstem reticular
form is a clouding of consciousness with im- activating system influencing the tonic states
paired alertness as the major defect. Such a of alertness (Benson & Geschwind, 1975). Sepatient cannot think quickly and is easily dis- vere pathology results in coma or somnolent
tracted, even though oriented. Another state akinetic mutism. A lesser degree may show
has been called confusion. In this state, the "drifting attention" if phasic alertness is intact.

NEUROPSYCHOLOGICAL STUDIES OF THE FRONTAL LOBES

The patient will respond to a stimulus but

attention rapidly drifts back to "a somnolent
state. Such patients are described as obtunded
or stuporous (Plum & Posner, 1980).
A second type of attention disorder, wandering attention, is the converse of drifting.
The patient appears fully alert and cooperative,
indicating that the tonic alertness is intact, but
the phasic component is deficient in that the
patient is easily distracted by external stimuli.
The alert attention wanders. The latter problem can be conceived as a deficiency of the
diffuse thalamic projection system. Finally, in
the section on neuroanatomy, a thalamic gating system was described that enabled conscious, directed attentive behavior. This gating
system appears to be under the influence of
ascending fibers of the reticular activating system and descending impulses from the frontal
cortex, so that afferent and efferent information can be integrated, interpreted, and used
to control sensory pathways. Pathology in this
system would result in disorders of more complex behaviors requiring planning, selection of
behavior, and monitoring of performance.
Although the concepts above are useful for
understanding the neuroanatomical-behavioral correlates of attention, limitations should
be recognized. For example, little has been
said of the reticular activating system-limbic
combination that involves the dorsomedialorbital frontal areas. This interaction may have
considerable importance in vegetative and affective attentional interplay (Nauta, 1971).
In addition, negative results on measures of
attention following localized frontal brain
damage deserve notice. Both Feuchtwaiiger
(1923) and Teuber (1964), studying patients
with frontal gunshot wounds, could not find
specific attentional changes. In two more recent, studies, patients with massive bifrontal
pathology were not impaired in digit span performance (Benson, Gardner, & Meadows,
1976; Stuss, Alexander, Lieberman, & Levine,
1978). Negative findings have also been demonstrated following prefrontal leukotomy. In
a long-term follow-up of neuropsychological
function following prefrontal leukotomy
(Benson et al, 1981; Stuss, Benson, Kaplan,
Weir, & Delia Malva, 1981), three groups of
leukotomized schizophrenics, divided according to recovery status, were compared with a
nonleukotomized schizophrenic group and a

11

normal control group. A series of attention

tests was administered to probe sustained
mental activity, inhibition of interfering stimuli, and tracking (Digit Span, Digit Symbol,
Knox cube, Stroop test, Trail Making A and
B, and Serial Sevens). The only significant correlation obtained was with active psychosis.
Many subjects with large frontal lobe lesions
(as demonstrated by CT scan) performed as
well as or better than the normal control subjects.
Several reasons can be offered for the negative results, including questionable test validity and the effects of the rigidly structured
testing situation. Also, schizophrenia itself may
impair attention. The frontal leukotomy may
have created a double negative (decreasing the
schizophrenic effect of decreasing attention)
resulting in the intact performance. Regardless
of theoretical conjectures, the results of this
type of testing demonstrate that frontal lobe
lesions per se do not necessarily produce impaired attention and that sizeable bifrontal lesions may be present in a patient who performs
normally on a battery of standard attention
tests.
Syndromes of Abnormal Awareness
Among the most confusing problems in
neurology and psychiatry are abnormalities in
awareness, involving either the body or the
environment. The separate disorders of
awareness appear heterogeneous and include
such apparently diverse entities as confabulation, neglect, anosognosia, reduplicative
paramnesia, and the Capgras syndrome. These
symptoms remain mysterious and, predictably,
a psychogenic causation has been suggested
for each, often as an "unusual psychiatric syndrome" (Freedman & Kaplan, 1975). As with
so many mysterious entities, frontal lobe pathology has also been suggested in some of
these disorders, and in actuality, there is some
evidence to support this suggestion. On this
basis, a few disorders of awareness will be described and discussed.
One common disturbance of awareness is
apathy, or lack of concern. This has already
been discussed among the motor disturbances
but apathy is present to some degree in..all
syndromes of disturbed awareness and either
represents an important etiologic factor or

12

DONALD T. STUSS AND D. FRANK BENSON

stems from the same underlying disorder as

many of these syndromes.
Abnormal awareness df body appears to be
the most common of these disorders and is
also the most thoroughly discussed. Unfortunately, the discussion has not cleared the
mystery. Complex categorizations of disordered body awareness have been described
(e.g., Critchley, 1953, suggested nine, Benson
& Geschwind, 1975, outlined four). A relationship between these disturbances, at least
to some degree hierarchical, has been suggested
and implies a common disturbance. This is
an unsubstantiated assumption.
The basic disturbance of body awareness is
unilateral inattention, often called neglect.
This is a common neurologic finding best exemplified as a tendency not to report stimuli
to one side on double simultaneous stimulation, even though the patient accurately reports
all unilaterally presented stimuli. Frontal lobe
damage that produced unilateral neglect has
been clearly described (Bianchi, 1895; Damasio et al., 1980; Heilman & Valenstein,
1972; Kennard, 1939). Welch and Stuteville
(1958) demonstrated inattention to all sensory
stimuli on one side of the body following lesioning of the opposite arcuate sulcus of the
frontal lobe in monkeys. More recently, Heilman and associates (Heilman, 1979; Watson
etal., 1973; 1974) have demonstrated a similar
unilateral inattention with pathology in other
areas including the mesencephalic reticular
activating system and the cingulate cortex.
They posit a reticulo-limbic-frontal circuit
for attention and imply that pathology anywhere in this circuit decreases attention to the
opposite side.
Denny-Brown and Banker (1954) proposed
a different explanation of unilateral inattention
under the title of amorphosynthesis. They
posited a unilateral decrease in sensory input,
unbalancing a previously finely-tuned perceptual balance between the two hemispheres;
unilateral sensory system pathology would allow similar degrees of stimulation to be unequal in their cortical effect. Both the DennyBrown and the Heilman explanations appear
reasonable, and it appears plausible that either
or both may be correct in explaining a given
instance of unilateral neglect. Thus there may
be qualitatively different types of unilateral

inattention based on different areas of anatomical malfunction.

A further, more severe, step in the suggested
hierarchy of inattention is a state called unawareness. Most often this describes patients
who are unaware of their paralysis. They agree
if told that they cannot move a limb but continue to act as though the limb were intact.
Not only is there a unilateral neglect but such
patients appear unable to maintain the information that they have a problem. Patients with
this more advanced degree of unawareness almost always show a notable degree of apathy.
Closely associated with unawareness but
somewhat distinct and considerably more disabling is a state of unconcern. In this situation
the patient will also admit the evidence of disability but shows lack of interest to the level
of disdain. While not denying the disability,
the patient's actions and remarks suggest that
the problem is of no importance. Again, apathy is almost invariably a striking finding.
The ultimate stage in this hierarchy is the
total denial of an illness; this has been called
anosognosia and most commonly describes a
patient who totally denies the presence of an
obvious hemiplegia. Similar denial can be seen,
however, with blindness (Anton's syndrome),
amputation, or purely neurobehavioral phenomena such as amnesia, aphasia, and so on.
It has been suspected that active denial of an
obvious disability demands strong psychic activity (suppression of an unhappy fact) and,
on this basis, it is suggested that the denial of
illness is motivated (Weinstein & Kahn, 1955).
There is strong reason to doubt that anosognosia is entirely (or even partially) psychogenically based, however. All patients with this
disorder have evidence of significant organic
brain disorder, and the disorder almost always
appears in patients with bilaterally abnormal
electroencephalograms (EEGs; Weinstein &
Kahn, 1955).
There is some evidence to suggest that frontal lobe abnormality may play a role in the
syndromes of abnormal awareness of the body
described above. This is not firm, however,
and will be discussed after several additional
syndromes are presented.
A well-known syndrome that can be classed
with the abnormalities of awareness is confabulation. Confabulation is defined as the

NEUROPSYCHOLOGICAL STUDIES OF THE FRONTAL LOBES

presentation of incorrect, sometimes bizarre,

information to a standard question. Confabulation is most often noted in the presence of
memory disturbance (amnesia), but the bizarre
responses presented again suggest a psychogenie motivation. Although confabulation has
long been recognized, only recently have formal studies of confabulation been performed.
In one (Mercer, Wapner, Gardner, & Benson,
1977), a series of patients with amnesia were
carefully studied for confabulation, degree of
amnesia, suggestibility, and ability to self-correct. The degree of confabulation did not correlate with either the severity of the memory
disturbance or suggestibility but was closely
related to the lack of ability to self-correct.
This inability to self-correct suggested an abnormality of awareness. In another study of
confabulation, 5 patients with severe, fantastic,
and spontaneous confabulations were studied
both psychologically and anatomically (Stuss
et al., 1978). These patients differed from most
patients with confabulation by their wildly
fantastic responses and the fact that the confabulation was presented spontaneously rather
than in response to prompting from the examiner. The anatomical study in each case of
extraordinary confabulation demonstrated severe bifrontal structural pathology. These two
studies together suggest that the bifrontal disturbance present in the spontaneous confabulation syndrome may also be present in the
milder forms of confabulation where structural
pathology is not present. The association of
different degrees of confabulation with different levels of severity of impairment of the same
underlying disorder appears to have been confirmed (Kapur & Coughlan, 1980; Shapiro,
Alexander, Gardner, & Mercer, 1981). This
suggests that the decreased concern (self-correction) in both types of confabulation represents a disorder of awareness, a frontal malfunction.
Two disorders that may be related to confabulation, reduplicative paramnesia and the
Capgras syndrome, were also studied clinically.
Both disorders feature reduplication. Reduplicative paramnesia has traditionally referred
to reduplication of place; the patient knows
the name of the hospital but places it in a
distant locale (usually the patient's home
town). In the Capgras syndrome the redupli-

13

cation concerns persons, usually close relatives

such as wife, parents, or children. These individuals are said to be imposters who look,
talk and act like the real family members but
the patient is convinced that they are not the
true family members. In recently reported
studies on these two syndromes (Alexander,
Stuss, & Benson, 1979; Benson et al., 1976),
severe bifrontal structural pathology was present in each case. There was pathology in other
portions of the brain that was different in the
two syndromes but all patients showing this
tendency for reduplication had significant bifrontal pathology. Again, a disorder of awareness is the prominent feature.
From this short review of the clinical and
psychological features of abnormal awareness
it can be suggested that many syndromes, including confabulation, reduplicative paramnesia, the Capgras syndrome, and some of the
disorders of body awareness such as unawareness, unconcern, and anosognosia indicate
significant frontal lobe malfunction. Even the
mildest degree of unilateral inattention (neglect) may be indicative of frontal pathology.
Although there is a consistency of frontal involvement in the syndromes of disordered
awareness, the evidence supporting the role of
the frontal lobe remains circumstantial. Obviously, much more work must be performed
to understand these syndromes, and it is probable that the role of the frontal lobe abnormality will only represent part of the problem.
Nonetheless, the clinical studies strongly suggest that disturbances of awareness can indicate
frontal malfunction.
Flexibility-Perseveration
Perseveration, defined as an abnormal repetition of a specific behavior, is a common sign
of frontal lobe pathology (Halstead, 1947; Luria, 1973; Luria, Pribram, & Homskaya, 1964;
Nichols & Hunt, 1940). Perseverative behavior
has been reported in diverse tasks including
motor acts, verbalizations, sorting tests, drawings, writing, and tracking tests. So pervasive
is this phenomenon following frontal lobe
damage that Denny-Brown, in a review of Luria's works, considered that perseveration may
have been of sufficient severity to have been
responsible for much of the reported impairment (reported in Hecaen & Albert, 1978).

14

DONALD T. STUSS AND D. FRANK BENSON

Two facts are important. First, despite popular belief, perseveration and inflexibility cannot be considered exclusive hallmarks of the
frontal lobe (Critchley, 1953; Hecaen & Albert,
1975). These symptoms may reflect the size
of the lesion rather than the location (Goodglass & Kaplan, 1979). In addition, Luria
(1973) notes that elementary motor perseveration, the inability to inhibit a movement
once begun, occurs primarily in patients whose
premotor lesion extends sufficiently deep to
involve the basal ganglia, suggesting that at
least this one type of perseveration requires
specific frontal-subcortical damage.
Secondly, it appears that the term perseveration may be too global and that more specific analyses are required. The uninhibited
motor response of a patient with frontal-basal
ganglia involvement may be qualitatively different from the inability of another frontal
lobe patient to overcome a previously established response pattern on the Wisconsin Card
Sorting Test (Milner, 1964). Also, the qualities
of the perseverated act may be controlled by
environmental-reward contingencies. Pribram,
Ahumada, Hartog, and Ross (1964) suggested
that when a reward situation was constant for
the duration of a problem and then changed
to an equally consistent reinforcement pattern
(similar in many ways to the Wisconsin Card
Sorting Test), frontally lesioned monkeys perseverated the response that had been successful
in the immediately preceding condition. If,
however, the reward situation varied from trial
to trial within the condition, the monkeys responded with increased variability. This extended random search behavior itself seemed
to become a perseverative tendency. In this
manner the task itself affected the presence
(and possibly the type) of perseveration.
Perseveration occurs commonly in patients
following frontal damage, but it can also be
seen in patients without any frontal damage
and is not present in all frontal-damaged patients. Whether perseveration indicates size of
lesion, correlation of frontal damage with basal
ganglia damage, a special environment/reward
correlation, or some mixture of these is currently unclear. That inflexibility and perseveration are important findings in many individuals with frontally determined behavior
problems is clear, however, and these findings
pervade many of the other frontal signs.

Language
The occurrence of language defects with
frontal pathology has been recognized since
the revolutionary demonstrations of Broca
(1861, 1865), and like so much of the field,
frontal communication disorders have been a
source of controversy. Marie (1906) challenged
the notion of language in the frontal area, suggesting instead that anarthria, a speech defect,
occurred following damage there. Although
never totally accepted, his suggestion has only
recently been disproved, and there remains
more mystery than accepted fact in the speech
and language functions of the frontal lobes.
For discussion of frontal language activities,
some long accepted but unproved concepts
must be used. Most investigators accept the
language dominance of the left frontal lobe
and, for convenience, the comparatively wellaccepted terms of classic aphasiology will be
used for this discussion. In this system Broca
aphasia, transcortical motor aphasia, aphemia,
and the aphasia of the supplementary motor
area are the language disturbances germane
to discussion of frontal communication disorders. Although these syndromes are not accepted as specific entities by all investigators,
the basic features have been well described.
Broca Aphasia
This generally accepted aphasia syndrome
has always been associated with pathology involving the frontal lobe. Primarily an expressive disturbance, Broca aphasia is characterized by a nonfluent (sparse, effortful, dysarthric, dysprosodic, and agrammatic) output,
relatively good comprehension, poor repetition
and troubles with naming, reading, and writing. Traditionally, involvement of the posterior-inferior frontal lobe (Broca's area) of the
dominant hemisphere is said to underly Broca
aphasia but most recognize that considerably
bigger lesions, particularly deep into the insula,
are necessary for the entire syndrome (Kleist,
1934b;Mohr, 1973; Mohretal., 1978). Along
with the aphasia there is usually a right hemiplegia and a number of other behavioral findings may be present,
Aphemia

Also known as pure word dumbness and

anarthria, this disorder is a vocal output dis-

NEUROPSYCHOLOGICAL STUDIES OF THE FRONTAL LOBES

turbance with no abnormality of language

comprehension (spoken or written) and normal language production through writing.
Aphemia often starts with mutism, but even^
tually there is a return of verbal output of poor
quality, breathy, soft, slow, and dysprosodic.
It is usually suggested that the pathology in
aphemia involves Broca's area or tissue just
below this area (Bastian, 1898; Benson, 1979),
but there is no significant cortical or deep
spread. That aphemia represents a portion of
the full Broca aphasia picture appears probable
but unproved.
Transcortical Motor Aphasia
Closely resembling Broca aphasia with the
exception that repetition is comparatively intact, cases with transcortical motor aphasia
(TCM) almost invariably show pathology that
spares Broca's area but involves cortical areas
anterior or superior to it in the frontal lobe,
Apraxia involving either bucco-facial or limb
activities is common, and some degree of right
hemiplegia is always present. An inability to
initiate spontaneous speech, but no difficulty
in the act of repetition, is the striking feature,
leading to functional descriptive terms such
as frontal dynamic aphasia, verbal adynamia,
and so on. Luria (1966) has stressed this dynamic quality as a frontal language disturbance. Again, some degree of TCM may be
present in the Broca aphasia syndrome.
Supplementary Motor Area
That output disturbances occur with supplementary motor area pathology has been
recognized for years (Foerster, 1936; Penfield
& Roberts, 1959), but only recently has a clear,
consistent syndrome been outlined (Rubens,
1976; Alexander & Schmidt, 1980). The disturbance is characterized by a decrease of verbal output, facial expression, and gesture, but
normal comprehension and repetition, an ab*
senee of paraphasia, and normal emotional
facial responses (Damasio, Van Hoesen, &
Damasio, 1980), The underlying characteristic
is a lack of dynamism in spontaneous activities
that disappears during automatic response and
thus closely resembles TCM.
The dynamic quality of the last two entities
represents one of the more characteristic frontal language features and is present to some

15

degree in all frontal language disturbances: The

difficulty can be described as a problem in
speech initiation and is illustrated using the
word fluency test (Milner, 1964), probably
better labeled a word-generation test. In this
test the patient is asked to produce a list of
words belonging to a given category (animals,
clothing, words beginning with the letter S,
etc.). Other investigators (Benton, 1968; Hecaen & Ruel, 1981; Ferret, 1974; Ramier &
Hecaen, 1970) have demonstrated that individuals with frontal pathology are particularly
poor at generating words. Caution is needed
in interpretation, however; both right and left
pathology can disturb performance on this test
(although there appears to be some hemispheric specificity), as dp aphasias from other
left hemisphere areas and the cortical dementias. In contrast, prefrontal leukotomy did not
result in impaired word, generation (Stuss &
Benson, 1983a). Newcombe (1969) found no
specific frontal lobe impairment with semantic
(e.g., lists of animals) fluency tests, In general,
however, the word fluency tests are sensitive
and demonstrate one primary manifestation
of frontal language disorder; they are not specific for frontal pathology, however.
A second major characteristic of frontal
language disturbance involves syntactical language usage. Although agrammatism, a tenr
dency to omit all syntactical language structures, has long been described in the verbal
output of Broca aphasia (Goodglass & Berko,
1960), it has also been demonstrated that
frontal pathology produces similar problems
in the comprehension of grammatic structures
of both spoken and written language (Samuels
& Benson, 1979; Zurif, Caramazza, & Myersoh, 1972). It has even been suggested that an
anterior (syntactic) versus posterior (semantic)
division of linguistic capabilities can be considered. Although definitive proof remains
scanty^ there is a strong suggestion that syntactical language functions are primarily a left
(frontal) function.
The ability to maintain a sequence, either
verbal or nonverbal, is also reported as a frontal
characteristic (Albert, 1972) and, as such, affects the comprehension of language. Thus,
many patients with frontal pathology will
comprehend individual words well, but if given
a sequence of words, will appear to comprehend only a few (either the first or the last).

16

DONALD T. STUSS AND D. FRANK BENSON

Some investigators have considered the limited

ability of certain patients to repeat an auditory
span disturbance (Warrington & Shallice,
1969); others emphasize the rank ordering aspect of sequential comprehension as the major
defect. Both aspects are subsumed under the
term sequence, a function that can be severely
disturbed by frontal pathology.
Finally, it has been proposed that a loss of
the regulatory power of language can result
from frontal damage (Luria, 1966). Thus,
frontal patients may verbalize a task correctly
but cannot use the verbalization to direct behavior. Luria (1973) described frontal and parietal patients who were asked to squeeze hard
or soft to a signal (red, hard; green, soft). Neither group performed this test well, but when
instructed to use verbal cues to aid in the task,
the parietal patients improved dramatically
and the frontal patients remained poor. This
is a verbal-action dissociation and will be discussed further in the section on cognition.
Nonetheless, it can be considered another example of frontal language disturbance.
In summary, pathological involvement of
the frontal lobe produces a variety of language
abnormalities that reflect loss of control. In
addition, there is a strong suggestion that some
specific, high-level attributes (syntactical language) are primarily or totally under frontal
control.
Memory
The idea of a memory deficit after frontal
lobe damage comes from the early animal experiments. Jacobsen (1935, 1936) observed
that monkeys with frontal lobe damage successfully performed immediate discrimination
tasks but were impaired if delayed response
was required. Subsequent research has looked
at factors such as distractibility (Finan, 1942;
Malmo, 1942), drive (Pribram, 1950), and
stimulus and task specificity (Jacobsen & Nissen, 1937; Pribram, 1961) to replace the concept of a memory deficit. Gross and Weiskrantz (1964) suggested that it was not a
memory loss but an inability to use the memories that were stored.
The possibility of a memory deficit with
human frontal lobe pathology has also been
raised. Hecaen (1964), on the basis of his own
tumor series and review of the literature, con-

cluded that some patients with frontal lobe

tumors were impaired in learning verbal paired
associates. Deficits in maze learning by frontal
lobe patients have been reported (Corkin,
1965; Milner, 1965; Walsh, 1960). Frontal lobe
pathology can result in impaired judgment of
recency (Milner, 1971, 1974; Ladavas, Umilta,
& Provincial!, 1979). These results suggest that,
as indicated in the animal literature, frontal
lobe pathology interferes with certain memory
functions.
Negative results have been obtained in many
studies, however. Moreover, the frontal amnesia suggested above may be, in some instances, more apparent than real (Milner,
1964). Many frontal disorders, including unconcern, perseveration, and lack of initiative,
suggest that apparent frontal memory impairment may merely reflect other disorders
of complex behavior. Thus, deficits in maze
learning may be more parsimoniously interpreted as a disregard for instructions and rules
plus perseveration; the recency effect may primarily represent disordered sequencing rather
than a true memory disorder.
Luria suggests that the frontal memory disorder is a binary deficit, consisting of an inability to create a stable intention to remember
plus an impairment of shifting recall from one
trace to another (Luria, 1971, 1973). Hecaen
and Albert (1978) similarly proposed a deficit
of selective attention and lack of initiative as
the primary source of the apparent memory
deficit. The disorder is a "forgetting to remember" in which the details have not been
forgotten, but cannot be accessed at the time.
Study of the memory function in patients
who had undergone prefrontal leukotomy
many years earlier lends support to these findings (Stuss, Kaplan, Benson, Weir, Chiulli, &
Sarazin, 1982). These patients could learn new
material (logical memory, paired associates)
in an apparently normal manner. If an interference task were superimposed before retesting (Cermak & Butters, 1972; Peterson &
Peterson, 1959), however, the performances
were significantly impaired. An exaggerated
inability to maintain new information in the
face of interference would appear to be an
important frontal memory deficit (Malmo,
1942, 1948; Malmo & Amsel, 1948).
These cumulative observations suggest that
frontal damage does lead to disturbed function

NEUROPSYCHOLOGICAL STUDIES OF THE FRONTAL LOBES

on formal memory tests but that the frontal

memory problems differ distinctly from temporal or diencephalic amnesias. Details of this
difference remain vague, however, and much
work needs to be done to isolate the role of
the frontal lobe in the overall memory function.
Cognitive Functions
Much of the controversy and confusion
concerning frontal lobe function derives from
the observations and studies of cognitive functions in frontal lobe damaged patients. Historically, the prefrontal area was considered
by many to be the cortical region associated
with the highest human functions (Jackson,
1932). Individual case studies suggested that
extensive bilateral frontal damage could result
in cognitive deficiencies (Ackerly & Benton,
1948), and loss of abstract thought was considered to be an early sign of frontal lobe damage (Goldstein & Gelb, 1918). Loss of abstract
thinking was reported in psychosurgery studies
(Malmo, 1942) except after topectomy, where
impairment was only transient (Mettler, 1949).
Similar results have been noted in both lesion
and tumor studies (Halstead, 1947; Rylander,
1939).
Certain evidence conflicted with this stand,
however. Cognitive deficits were not present
in all patients with frontal lobe damage
(Feuchtwanger, 1923; Rylander, 1939) and,
even when noted, were often difficult to replicate (Rylander, 1943). In a series of studies,
Hebb concluded that frontal lobe patients did
not perform inferiorly on tests of intelligence
compared with patients with posterior lesions.
One patient, in fact, improved after extensive
bilateral frontal lobectomy (Hebb, 1939, 1945;
Hebb & Penfield, 1940). These negative results
on intelligence tests were later replicated (Pollack, 1960;Teuber, 1959; Weinstein & Teuber,
1957).
Additional research has pointed out some
possible reasons for the apparently discrepant
findings. In general, the observations have been
correct, but underlying the demonstrated cognitive deficits there are often complicating disorders such as difficulties in attention, problems in planning, and impaired monitoring of
performance (Halstead, 1947; Hecaen & Albert, 1975;Luria, 1973;Milner, 1964; Teuber,

17

1964). Another problem stems from confusion

in terminology (e.g., the use of abstract words
versus the ability to think abstractly; Goldstein,
1944). Research in the last few years has gradually defined some characteristic cognitive deficits suffered by patients with frontal lobe
damage.
Frontal lobe patients have no difficulty with
the basic operations (e.g., adding and subtracting) required to complete arithmetical
tasks. When given more complex problems
requiring multiple steps, the patient tends to
respond impulsively to an early stimulus and
fails to analyze or execute the component steps
required for problem solution. Luria presents
examples of questions designed to isolate this
deficit (Luria, 1973; Luria & Tsvetkova, 1964).
Certain arithmetic questions from the WAIS
are useful. For example, "The price of canned
peas is two cans for 31 cents. What is the price
of one dozen cans?" is almost impossible for
many frontal lobe patients to answer, even
though the direct arithmetical task of multiplying 6 times 31 is completed with comparative ease.
Block design tasks appear sensitive to frontal
lobe dysfunction in a special way. Lhermitte
et al. (1972) documented specific steps in block
building solutions during which the frontal
lobe patients may fail. Walsh .(1977) studied
subjects with modified prefrontal leukotomy
who had comparable pre- and postoperative
IQ levels. Performance in block design improved considerably when the patients, tested
postoperatively, were assisted by partial programming. This suggests that an organizational
deficit was the primary problem. Goodglass
and Kaplan (1979) noted that the patients with
right frontal pathology focused on the salient
feature of the block design, leading to a broken
external configuration.
Maze tests also appear sensitive to frontal
lobe dysfunction. Perhaps the most frequently
used in the Porteus Maze Test (Porteus, 1950),
which requires advanced planning of the route
to be followed, anticipation of possible blocked
passages, and completion of the planned action. Almost all postleukotomy studies demonstrated clear impairment on the Porteus
Maze (Malmo, 1948; Mettler, 1952; Petrie,
1949; Porteus & Kepner, 1944; Porteus & Peters, 1947). Other maze tests are not as specifically susceptible to the effect of frontal lobe

18

DONALD T. STUSS AND D, FRANK BENSON

damage as the Porteus Maze, but with most, Frontal patients, however, are unable to
frontal patients will show specific qualitative "change responses in accordance with varying
errors. Although the patients apparently un- environmental stimuli" to overcome previderstood and could repeat the rules, they were ously established response patterns (Milner,
unable to follow them or use knowledge of 1964). There is a tendency to perseverate preincorrect performance to alter their behavior vious responses, seemingly replicating the ten(Benton, Elithorn, Fogel, & Kerr, 1963; Milner, dency to perseverate seen in frontal animals
(Harlow & Settlage, 1948; Mishkin, 1964;Pri1964; Walsh, 1960).
Perhaps the most widely accepted measure bram et al., 1964). There is a curious dissoto show executive functional deficit is the sort- ciation between knowing and doing (Luria,
ing task. One unpublished study, reported by 1973; Milner, 1964; Teuber, 1964), such that
Shallice (1982), stated that the category sorting verbalization no longer controls active behavior
task was the only one of 10 tests for frontal (Luria & Homskaya, 1964). Frontal lobe paskills that produced significant anterior-pos- tients know their errors, but are unable to use
terior difference. Sorting tasks are not pri- that knowledge to modify behavior (Konow
marily tests of abstraction or concept for- & Pribram, 1970). This thought-action dismation but, under certain methods of admin- sociation has been described as a disconnection
istration, measure application of rules rather of feedback-feedforward systems so that
than knowledge of facts. Although some degree knowledge of errors cannot be utilized (Priof abstraction is required, performance in bram, 1971). Milner (1982) suggests that this
sorting tasks can be severely impaired in pa- characteristic frontal disorder is a more general
tients who readily recognize and verbalize (ab- problem in the use of external cues to direct
responses rather than a selective verbal regstract) all of the underlying concepts.
Halstead (1940, 1947; Shure & Halstead, ulation deficit. There is, in addition, a dis1958), using the Halstead Category Test, dem- tinctive lack of self-criticism that has been deonstrated that frontal lobe patients had greater scribed as "a general loss of some feedback
impairment than patients with lesions else- mechanism, a disturbance in signals of error,
where in the brain. This differential effect was or an inadequate evaluation of the patient's
not replicated with Grant and Berg's (1948) own action . . . a deficit in matching action
modification of the Weigl (1941) Sorting Test carried out with the original intention" (Luria
(Teuber, Battersby, & Bender, 1951). These & Homskaya, 1964). Superimposed on this
authors found that frontal damage after missile problem is a basic unconcern, a common feawounds resulted in less impairment on this ture in frontal lobe disturbance.
test than did damage in parietal areas. Their
A study of cognitive function in prefrontal
modification of the test, however, did not allow leukotomy patients illustrates some of the imbuildup of the prior correct response before portant distinctions that must be considered
criterion change. Milner (1963, 1964), using (Stuss et al., 1983; Stuss, Kaplan, & Benson,
patients who had lobectomies for seizure ther- 1982). Three groups of leukotomized schizoapy reasons, used the same test (Wisconsin phrenic patients were compared with two conCard Sorting Test) but changed the criterion trol groupsa nonleukotomized schizowithout warning after 10 consecutive correct phrenic group and a normal control group.
responses. With this technique, frontal lobe Four tests were administered: the Wechsler
patients were more impaired than patients Adult Intelligence Scale, a test of comprehenwith damage elsewhere. These findings have sion in metaphorical language (Winner &
been replicated frequently in patients with pa- Gardner, 1977), a visual-verbal test of abthology in frontal systems from many etiol- straction (Feldman & Drasgow, 1,960), and the
ogies (Drewe, 1974; Walsh, 1978) including Wisconsin Card Sorting Test. The results
Parkinson's dementia (Bowen, Kamienny, clearly demonstrated that some patients with
Burns, & Yahr, 1975).
very large bifrontal lesions could perform adSeveral factors underlying impairment in equately on general intellectual tests such as
Wisconsin Card Sorting Test (WCST) perfor- the WAIS. These patients could also perform
mance can be discriminated. Subjects nor- basic tests of abstraction competently. They
mally verbalize the three underlying criteria. had difficulty, however, in verbalizing abstract

NEUROPSYCHOLOGICAL STUDIES OF THE FRONTAL LOBES

responses, shifting perceptual sets even within

a simple abstraction test, and maintaining long
sequences of correct responses.
Recent efforts have been made to understand frontal lobe deficits in terms of cognitive
psychology and artificial intelligence theory
(Shallice, 19 82; Shallice & Evans, 1978). Shallice (1982) postulates two separate operations
in problem solving. Contention scheduling is
the term used to describe the fast, efficient,
routine use of limited resources. With the introduction of nonroutine factors (e.g., a new
problem), a general programming, planning,
and monitoring system, the Supervisory Attentional System, is made operational. Using
a "Tower of London" task that appears to depend entirely on the general programming unit
rather than on known routine programs, Shallice was able to demonstrate the effect of left
anterior pathology. This selective deficit may
be similar to the concept of left hemisphere
(frontal) dominance for the programming of
voluntary actions (Milner, 1982).
, - In summary, patients with frontal lobe
damage do suffer significant cognitive distunbances. The disability, however, is different
from that suffered by patients with lesions in
other cortical areas and can be missed by many
of the current tests of cognition. Improved
neuropsychological techniques, possibly assisted by theoretical concepts and experimental
procedures, from cognitive psychology, will
lead to a better understanding of the role of
the frontal lobes in cognition.
Frontal Lobe Personality
General Description
Probably the most widely accepted (and obvious) alteration secondary to frontal lobe abnormality concerns change in personality, "the
frontal lobe personality," or "frontal-lobishness," Although widely recognized and totally
accepted, specific descriptions of this alteration
are difficult to present; a morass of behavioral
abnormalities have been described under the
term frontal lobe personality. These include
unrestrained and tactless behavior; mood
changes including jocularity and bawdy, puerile joking ("Witzelsucht"); blunted feelings;
callous unconcern; boastfulness; and grandiose, obstinate, and childishly egocentric behavior. Related intellectual changes include

19

deterioration of memory and intellectual abilities, although these are often said to be more
apparent than real. There appears to be
suppression or actual inability to produce
imaginative or original thinking; there is a distinct diminution of spontaneity and initiative.
Inattentiveness, distractibility, and ineffective
or careless working habits are frequently observed. Apathy, dullness, indifference, and
slowness of thought are described as-part of
the syndrome. At times drowsiness, lethargy,
and general retardation may be present, most
often in progressive tumor situations. A vacancy of facial expression has been observed,
as well as a tendency to be careless in dress,
to eat gluttonously, and be unconcerned. With
progressive frontal disorder, complications
such as generalized convulsions, dysphasia,
grasp reflex, forced groping, and frontal motor
disturbances may all be seen. Through all of
this, there is almost constantly a striking lack
of insight. Descriptions of frontal lobe personality, therefore, cover a vast variety of
symptomatology and there is considerable
variation among patients.
The first report of change in personality following frontal injury dates-to 1835 (Blumer
& Benson, 1975) and describes an adolescent
with a self-inflicted frontal gunshot wound.
Although the patient became blind, the patient
was described as happy, vivacious, and jocular.
The most widely recognized early case of frontal personality alteration is that of Phineas
Gage (Harlow, 1868), a hard-working, sober,
reliable, family-oriented construction foreman
who sustained a major injury to the frontal
lobes. Miraculously, the patient survived his
injury without basic neurologic disability but,
in the words of his fellow workers, "he was no
longer Gage." Harlow (1868) described Gage's
post-injury personality as follows:
The equilibrium or balance, so to speak, between his intellectual faculties and animal propensities seems to have
been destroyed. He is fitful, irreverent, indulging at times
in the grossest profanity, manifesting but little deference
for his fellows, impatient of restraint or advice when it
conflicts with his desires, at times pertinaciously obstinate,
yet capricious and vacillating, devising many plans of operation, which are no sooner arranged than they are abandoned in turn for others appearing more feasible. A child
in his intellectual capacity and manifestations, he has the
animal passions of a strong man. (pp. 339-340)

This description has stood the test of time and

20

DONALD T. STUSS AND D. FRANK BENSON

remains a classic description of frontal lobe

personality.
Another excellent description of profound
frontal lobe personality changes was provided
by Brickner (1936), discussing the behavioral
alterations of an individual who had both
frontal lobes removed surgically as treatment
for a perisagittal meningioma. Detailed descriptions of this individual's personality both
before and after surgery provide much the
same picture noted above.
Many descriptions of frontal lobe personality changes came from the physicians who
cared for the brain-injured of the two World
Wars. Sizeable numbers of individuals survived with major frontal lesions, and their residual psychiatric and personality disorders
were carefully recorded (Faust, 1960; Kleist,
1934a; Lishman, 1966). Again, large lists of
symptoms were presented by most authors but
some grouping by phenomena was done. For
instance, Kretschmer (1956) divided the frontal brain injury group into three major classes:
a lateral convexity injury group whose major
characteristic was apathy and lack of drive;
an orbital group whose major finding was unrestrained, disinhibited actions; and a basal
group whose personality problems were complicated by autonomic abnormalities.
Luria (1966) reported evaluations of many
patients with frontal damage caused by both
trauma and tumor, and emphasized the personality alterations. He suggested that the alterations were the result of disturbances of attention and concentration plus the inability
to handle activities demanding a complex sequence of mental activities.
Certain information on frontal lobe personality changes was available from the studies
of patients who had undergone psychosurgery
for psychiatric disease. In one large study,
Greenblatt and Solomon (1958/1966) defined
four major alterations in behavior that were
present following prefrontal leukotomy: shallowness of affect, decreased drive, social unconcern, and inability to anticipate (plan
ahead). These subjects should have provided
invaluable information because they had
carefully positioned, relatively precise frontal
lobe lesions, making them almost an ideal
subject group for frontal studies. The results
proved to be difficult to evaluate, however,
largely because of their premorbid psychiatric

problems, and there is relatively little substantiated information on personality changes

subsequent to prefrontal psychosurgery.
Finally, Blumer and Benson (1975) described two significantly different personality
types based on structural damage to different
portions of the frontal lobe. Following Kleist,
they suggested that there was a dorsal-lateral
convexity disturbance characterized by apathy,
lack of drive, inability to plan ahead, and total
unconcern. They noted that these patients appeared to have depressed mentation but that
tests of intellectual function demonstrated
normal or near normal capabilities, so the term
pseudo-depressed was suggested for this group.
Examples were presented of both tumor and
trauma presenting with this personality alteration and having a focus of pathology in the
dorsal-lateral convexity.
The second frontal personality abnormality
listed by Blumer and Benson was quite different. In this personality change the major
characteristics were a puerile, jocular attitude,
sexually disinhibited humor, and inappropriate
and near total self-indulgence with a corresponding lack of concern for others. Based on
the nature of these characteristics the term
pseudo-psychopathic was suggested. Again,
several varieties of pathology including both
trauma and tumor were capable of producing
this personality alteration. The common factor
was the location of pathology in the orbital
aspect of the frontal lobe.
Although they noted that all of their cases
had suffered bilateral frontal involvement,
Blumer and Benson admitted the possibility
that frontal personality alterations might follow
unilateral disease. The nature of the more
common causes of frontal pathology (tumor
and trauma) were such, however, that purely
unilateral involvement was rarely noted. There
is some suggestion from the psychosurgery literature that alterations in personality did occur
following unilateral frontal leukotomy procedures (Greenblatt & Solomon, 1958/1966).
Only a small number of unilateral operations
were performed, however, and they are difficult
to interpret because of the premorbid psychiatric abnormality. The question whether a
significant frontal personality alteration can
occur with unilateral frontal disease remains
open but there is good evidence that major
personality changes do occur following frontal

NEUROPSYCHOLOGICAL STUDIES OF THE FRONTAL LOBES

21

tion. For movement, the location of the lesion

on the lateral convexity is relevant. More posterior frontal lesions tend to result in difficulties in organization of movement, whereas
more anterior lesions result in deficits in motor
programming and a dissociation between language and behavior (Luria, 1965, 1973). A
number of reports of findings following psychosurgery suggested that dorsal-lateral lesions
led to greater behavioral deficits (Girgis, 1971;
Hamlin, 1970; Lewis, Landis, & King, 1956;
Malmo, 1948; Petrie, 1952; Smith & Kinder,
1959). Also Milner (1971) reports that performance on the Wisconsin Card Sorting Test
is maximally impaired with dorsal-lateral lesions.
Possible reasons for the freedom from deficit
on standardized intellectual tests by patients
with orbital-frontal lesions are summarized by
Walsh (1978). The tests depend on long-stored
information and on skills relatively insensitive
to subtle changes of behavioral regulation.
Walsh (1978) reported, however, that not even
Localization And Hemispheric Asymmetry medial orbital lesions were completely free
from intellectual changes. Moreover, research
of Frontal Lobe Function
in cognitive functions in patients with orbiThe. questions of localization and asym- tal-frontal pathology suggested that although
metry of frontal lobe function overlap and re- IQ may be unimpaired, specific errors related
volve about the organizational specificity of to perceptual shifts and an inability to mainthis cortical area. Without question, the frontal tain consistent patterns of organized responses
lobes have proved to be the most difficult cor- could be seen (Stuss et al., 1983; Stuss, Kaplan,
tical area to map. Many of the frontal defects & Benson, 1982).
Basal-medial lesions have often been related
that have been described appear global in nature, with little evidence for specific localiza- to disturbed impulse control, faulty activation,
tion. Part of this problem stems from the non- and shallow affective responses. Seemingly, this
focal nature of the more common pathology. disorder is responsible for fantastical confabFrontal tumors usually produce bilateral ef- ulation (Luria, 1973; Stuss et al., 1978), and
fects and are frequently undetected until ex- underlies certain personality disturbances.
tensive damage has occurred. Significant fron- Personality alterations can occur with patal head trauma almost always results in wide- thology anywhere in the frontal lobes, however,
spread, nonlocalized pathology. In addition, a and specific behavioral patterns appear to dereview of the neuroanatomy of distant con- pend on lesion localization. Thus, convexity
nections to various parts of the frontal lobes lesions are characterized by a lack of drive,
fails to provide simple stimulus-response pat- disinhibition, indifference, lack of productive
terns. Multiple factors serve to make local- thinking, euphoria, and inability to make deization within the frontal lobe difficult. Despite cisions, whereas orbital lesions result in
these difficulties, however, some localizing aggression, disinhibition, demanding and interfering actions, and increased sexual potency.
specificity is apparent.
Hemispheric specificity or unilateral domThe most generalized concept of localization
is the division between the dorsal-lateral and inance of a single frontal function is not clearly
the basal-medial section (Girgis, 1971). The demonstrable. A verbal/nonverbal split is most
dorsal convexity is most often associated with often cited, with the best examples using redisorders of movement and intellectual func- cency and fluency tests. Milner (1971, 1974)
lobe damage and that more than one personality type may result.
Although widely accepted, the concept of
frontal lobe personality alteration remains
vague. At least two behaviorally separable
frontal lobe personality syndromes, described
above as pseudo-depressed and pseudo-psychopathic, are reported, but most individuals
with significant frontal pathology have some
mixture of these problems. In addition, most
of the personality abnormalities described in
the literature include alterations in both affective state and intellectual quality. Better
understanding of the frontal lobe personality
demands a better understanding of the multiple, interrelated disorders that follow frontal
lobe damage (Damasio & Van Hoesen, 1983;
Stuss & Benson, 1983b). It seems probable
that premorbid personality features are also
significant in the final clinical picture, although
this is far more difficult to prove than to surmise.

22

DONALD T. STUSS AND D. FRANK BENSON

reported that the temporal ordering of events

was hemisphere specific, with left frontal lesions causing decreased verbal recency and
right frontal lesions causing decreased nonverbal recency. Benton (1968) noted that left
frontal patients are impaired in verbal fluency
but right frontals had more difficulty on constructional tasks and the copying of designs.
The fluency issue was further clarified, showing
a more specific dissociation between verbal
and nonverbal fluency and hemispheric dominance (Jones-Gotman & Milner, 1977). More
recently, Milner (1982) suggested a more precise hemispheric specificity based on analysis
of the temporal organization of behavior. Left
frontal lobe patients were impaired on all voluntarily (subjective) controlled ordering of actions, but the right-frontal patients were deficient only if the task was nonverbal. In contrast, for tasks demanding the monitoring of
the temporal sequencing of externally ordered
events (recency), the right-frontal patients were
impaired regardless of modality, whereas the
left frontal patients had a moderately severe
problem only for verbal stimuli.
Other hemispheric differences have been
noted. Smith (1966) originally reported no IQ
alterations with frontal lobe damage, but when
the patients were divided into left and right
frontals, a significant difference was noted,
with the left having lower IQ scores. McFie
and Thompson (1972) observed a selective deficit of picture arrangement capability after
right frontal lobe damage.
The results reported above suggest both
hemispheric differences and anatomically localized dysfunction following frontal damage,
but the tenuousness of the findings show an
obvious need for much more study before
diagnostically acceptable conclusions can be
made.
Summary
Although this article has outlined a number
of apparent frontal lobe functions, it is obvious
that the functions of this massive and phylogenetically novel prefrontal cortex are complex, interrelated, and as yet incompletely understood. Part of the riddle of the frontal lobes
derives from the size and complexity of the
cortical area in question, but knowledge has
also been hindered by inadequate test pro-

cedures and inability to obtain control of such

variables as lesion size, location, and even lateralization. Consequently, current explanations of apparent frontal lobe malfunction remain limited and vague. This does not lessen
the importance of the prefrontal area to human
behavior nor does it diminish the importance
of the clinical research and theoretical insights
made by investigators in past years.
It would appear that a few specific prefrontal
functions can be extracted. These are broad
and vague and certainly incomplete but do
provide direction for appropriate investigation
and a base for theoretical considerations.
1. Prefrontal damage can separate action
(response) from knowledge; this is illustrated
by tests in which the patient could verbally
define (and apparently understand) the action
expected but could not carry out the behavior
that corresponded to this knowledge. This impairment was striking in complex tests such
as the sorting task, but prefrontal patients were
often unable to use language (knowledge) to
correctly guide even simple motor actions.
2. Prefrontal damage can impair the ability
to handle sequential behaviors. Language assessment revealed an inability to put items in
an organized sequence; memory assessment
suggested deficient judgment of recency, a task
that requires ability to sequence; and sequential motor tasks were often impaired, resulting
in perseverative performance.
3. Prefrontal damage can impair the ability
to establish or change a set, resulting in apparently random or markedly perseverative
behavior. Impaired ability to both form and
alter a set was noted in tests of attention and,
most markedly, in the tasks of sorting and
planning.
4. Prefrontal damage can also impair the
ability to maintain a set in the face of interference. The performance of the leukotomized
subjects in the sorting task clearly revealed
this impairment. Interference as defined by
the Stroop test and the consonant trigram
memory tests also impeded performance in
many patients with prefrontal pathology.
5. Prefrontal damage impairs the ability to
monitor personal behavior. Erroneous actions
continue uncorrected. Striking examples of
this were noted in the inability of patients to
use feedback in the sorting tasks and appears
to underlie some of the frontal disturbances

NEUROPSYCHOLOGICAL STUDIES OF THE FRONTAL LOBES

such as confabulation and the Capgras syndrome.

6. Prefrontal tlamage can produce attitudes
of unconcern, unawareness, and apathy, such
that the patients ignore or actively deny many
of their difficulties.
These descriptions of impaired function do
not represent all malfunctions secondary to
prefrontal damage, but they appear in many
of the described incapacities of patients with
damage to this area. Whether they are facets
of one main deficit or based on functions of
specific location cannot yet be determined. In,
addition, as the frontal lobes are only infrequently disturbed individually, these problems
are often combined ;with impaired function
secondary to the damage in other brain areas.
These combinations make up a major portion
of the so-called frontal behaviors. The importance of the six abnormalities outlined
above to the resulting picture is usually discernable, but whether these impairments are
exclusive to frontal malfunction is yet to be
determined.
In conclusion, the neuropsyehblogic picture
secondary to prefrontal pathology is a complex
and confusing set of behaviors. With appropriate clinical/anatomical/psychological correlations many of these problems should become explicable, and in this process, much
will be learned about prefrontal functions specifically and human behavior in general.
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Received February 14, 1983

Revision received June 6, 1983