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50]
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“The hypothalamus, the anterior thalamic nucleus, the cingulate constitute the limbic system are:
gyrus, the hippocampus and their interconnections, constitute a 1. Limbic cortex
harmonious mechanism which may elaborate the functions of central i. Cingulate gyrus
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emotion as well as participate in the emotional expression.” ii. Parahippocampal gyrus
James Papez, 1937 2. Hippocampal formation
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i. The dentate gyrus
The limbic system consists of the phylogenetically old ii. Hippocampus
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limbic lobe and other subcortical structures and their iii. Subicular Complex
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connections. Although not empirically proven, the limbic 3. Amygdala
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system is a functional concept which may be employed to 4. Septal area
explain various brain functions.[1] 5. Hypothalamus
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HISTORY
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emotion.[5]
Paul Pierre Broca in 1878 spoke of ‘le grand lobe limbique’ or
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the great limbic lobe and applied the term “limbic” (from Limbic lobe
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the Latin limbus for border) to the curved rim of the cortex The limbic lobe situated at the inferomedial aspect of
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which incudes the cingulate and the parahippocampal the cerebral hemispheres, consists of two concentric gyri
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gyri. However, its putative role in emotion was elaborated surrounding the corpus callosum. Broca proposed that the
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by the American physician, James Papez in 1937 in the larger outer gyrus be named “limbic gyrus” and the smaller
seminal paper titled ‘A proposed mechanism of emotion’. inner one “the intralimbic gyrus”. The limbic gyrus (limbic
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This anatomical model is referred to as the Papez circuit.[2] lobe) consists of the isthmus of the cingulate gyrus, the
Yakovlev in 1948 proposed Yakovlev’s circuit in the control parahippocampal gyrus (both of which are continuous
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of emotion involving the orbitofrontal, insular and anterior via a bundle of white matter called “cingulum”) and the
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temporal lobe cortex, the amygdala and the dorsomedial subcallosal area.[6]
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term “limbic system” to describe Broca’s limbic lobe and The cingulate gyrus (Latin = Belt ridge) dorsal to the corpus
related subcortical nuclei as the collective neural substrate callosum is heavily interconnected with the association
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for emotion.[1] MacLean was also instrumental in proposing areas of the cerebral cortex. The parahippocampal gyrus in
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and defining the Triune concept of the brain. MacLean’s the medial temporal lobe contains several distinct regions,
evolutionary “Triune brain theory” proposed that the human the most important being the entorhinal cortex (ERC).
brain was in reality three brains in one: the R-complex The ERC funnels highly processed cortical information to
(reptilian complex), the limbic system and the neocortex.[4] the hippocampal formation and serves as its major output
The concept of the limbic system has since been further pathway.[5]
expanded and developed by Nauta, Heimer and others.
The hippocampal formation
COMPONENTS OF THE LIMBIC SYSTEM Hippocampal formation in the temporal lobe has three
distinct zones:
There is no universal agreement on the total list of structures, 1. The dentate gyrus
which comprise the limbic system. The brain regions that 2. The hippocampus proper
3. The subiculum
Correspondence: Dr. V. Rajmohan,
Elite Mission Hospital, Thrissur, India.
Embryologically, the hippocampal formation is an extension
E-mail: emohandas53@gmail.com
of the medial edge of the temporal lobe. The entire
hippocampal formation has a length of about 5 cm from its
How to cite this article: Rajmohan V, Mohandas E. The Limbic
anterior end at the amygdala to its tapering posterior end
system. Indian J Psychiatry 2007;49:132-9.
near the splenium of the corpus callosum.[5]
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CA4 is not part of the Cornu Ammonis but is a separate virus into a cat’s hippocampus and monitoring its progression
structure—the dentate hilus. The thin layer of fibers through the brain, unraveled the basis of cortical control of
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adjacent to the polymorphic layer of the hippocampus emotion. Further elaboration of the circuit has included the
is known as the alveus. These fibres coalesce to form the prefrontal cortex (PFC), amygdala and septum among other
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fimbria and subsequently, the crura of the fornix (main areas [Figure 1].[1,2]
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efferent pathway of the hippocampal formation). The crura
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of the fornix converge to form the body of the fornix, which Hippocampal afferents
later forms the columns of the fornix and pass through the The major input to the hippocampal formation arises
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hypothalamus into the mammillary bodies.[5,7] from neurons in layers II and III of the entorhinal cortex.
In addition, some septal and hypothalamic fibres reach the
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Subicular complex hippocampal formation via the fornix. A few fibres also
The subicular complex has three components: the arrive from the contralateral hippocampal formation via the
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Amygdala
Identified by Burdach in the early 19th century, amygdala, Table 1: Hypothalamic nuclei
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the anterior end of the hippocampal formation and the Supraoptic Supraoptic nucleus Lateral nucleus
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anterior tip of the inferior horn of the lateral ventricle, it Paraventricular nucleus Part of Supraoptic
Anterior nucleus nucleus
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merges with the periamygdaloid cortex, which forms part Suprachiasmatic nucleus
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of the surface of the uncus. The amygdaloid complex is Tuberal Dorsomedial nucleus Lateral nucleus
structurally diverse and comprises of approximately 13 Ventomedial nucleus Lateral tuberal nuclei
nuclei. These are further divided into subdivisions that have Arcuate nucleus
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Posterior nucleus
major groups are:
A. Basolateral nuclei Perforant
B. Cortical-like nuclei Entorhinal Pathway
Hippocampus
C. Centromedial nuclei Cortex
D. Other amygdaloid nuclei Fornix (F)
E. Extended Amygdala[8] (centromedial amygdala,
sublenticular substantia innominata and bed nucleus of
the stria terminalis)[9] Parahippocampal Mammillary
Gyrus Body
from the entorhinal area, dentate gyrus, Ammon’s horn and Association Cingulate
the subiculum. The three primary pathways of this area are Cortices Cortex
path from the entorhinal area to Ammon’s horn through the Cortex
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Brainstem and
mossy fibers then extend from the dentate gyrus to CA3 Spinal cord
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(pyramidal layer), although some efferent fibers from CA3
Figure 3: Connections of the hippocampal formation (F: Fornix,
project to the fimbria. Many axons of CA3, however, give
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MTT: Mammilothalamic tract)
off the Schaffer collaterals that reach the dendrites of CA1.
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CA1 is considered the main output of the hippocampus with Circuits of amygdala
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fibers extending to the alveus, fimbria and then fornix. A Amygdala serves to integrate information processing
supplementary linkage with the subiculum also is believed between prefrontal / temporal association cortices and
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to be present [Figure 2].[10] the hypothalamus. The amygdala has two major output
pathways:
Hippocampal efferents
kn kno ee • Dorsal route via stria terminalis projects to the septal
The efferent fibers from the hippocampal region form three area and hypothalamus.
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groups: precommissural fornix, postcommissural fornix and • Ventral route via the ventral amygdalofugal pathway
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nonfornical fibers. The precommissural fibers of the fornix terminates in the septal area, hypothalamus and the
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may originate from the cornu ammonis or the subiculum. medial dorsal thalamic nucleus [Figure 4].
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the fornix. The cornu ammonis fibers terminate exclusively The amygdala has also got connections with the basal
in the lateral septal nucleus, whereas the subicular ganglia circuit via its projections to the ventral pallidum and
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fibers are distributed to nucleus accumbens, anterior ventral striatum, which is relayed back to the cortex via the
olfactory nucleus, lateral septal nucleus, precommissural dorsomedial nucleus of the thalamus [Figure 5].
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body, although some fibers also project to the anterior This circuit is relayed via the basolateral amygdala. This
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thalamic nucleus, bed nucleus of the stria terminalis and circuit consists of the orbitofrontal and anterior temporal
ventromedial hypothalamic nucleus. The nonfornical fibers cortex, amygdala (especially the basolateral amygdala) and
project directly from the hippocampus to the entorhinal magnocellular division of the dorsomedial nucleus of the
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area as well as to the posterior cingulate and retrosplenial thalamus (frontothalamic pathway), which relays back to
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cortices and the amygdala [Figure 3].[10] the orbitofrontal cortex.[11] This circuit encodes information
Pathway
Figure 5: Amygdala basal ganglia circuit Figure 7: Olfactory role of limbic system
about social signals and social plans for social acts. The
circuit has been proposed as a substrate for the human Appetite and eating behaviors
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ability to infer the intentions of others from their language, Amygdala plays a role in food choice and emotional
gaze and gestures (Theory of mind and social cognition) modulation of food intake. The lateral nucleus of the
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[Figure 6].[12] hypothalamus is the center for control of feeding whereas
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the ventromedial nucleus functions as the satiety center.[14]
FUNCTIONS OF THE LIMBIC SYSTEM
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Sleep and dreams
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The functions of the various structures of limbic system are Positron emission tomography (PET) and functional magnetic
outlined below [Table 2]. resonance imaging (fMRI) have shown that the limbic system
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is one of the most active brain areas during the process
of dreaming. The limbic system probably interweaves
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Olfaction
unconscious primal emotions with our conscious cognitive
The limbic structures are closely related to the olfactory
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Nucleus of
Thalamus Cortex (TMN), the serotonergic dorsal and median raphe nucleus
and the noradenergic locus coeruleus. It also sends axons
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Ventral Uncinate
that terminate within the cholinergic basal forebrain, the
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Amygdalofugal Fasciculus
Pathway pedunculopontinethalamic nucleus (PPT) and lateral dorsal
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Anterior Temporal
Amygdala
Cortex
are inhibitory in nature as they are γ-aminobutyric acid-ergic
(GABAergic) and galaninergic. The VLPO via its inhibition of
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Figure 6: Basolateral circuit promoting sleep. Its reciprocal relationship with the major
arousal areas helps it to function as one half of a ‘flip-
flop’ circuit, the stable firing (flip-flop) of which prevents
Table 2: Functions of individual structures and connections intermediate states of sleep and wakefulness. The VLPO by
Areas Functions its disinhibition of the PPT-LDT also promotes REM sleep.
Cingulate gyrus Autonomic functions regulating heart rate and The lateral hypothalamic area (LHA) contains orexinergic
blood pressure as well as cognitive, attentional neurons that promote wakefulness. The orexinergic neurons
and emotional processing. inhibit the sleep-promoting VLPO and the REM sleep-
Parahippocampal gyrus Spatial memory
Hippocampus Long-term memory
promoting neurons in the PPT-LDT. The orexinergic neurons
Amygdala Anxiety, aggression, fear conditioning; also increase the firing of the locus coeruleus, dorsal raphe
emotional memory and social cognition. and the TMN and in a way, act as a finger pressing the ‘flip
Hypothalamus Regulates the autonomic nervous system via flop’ circuit switch into the wakefulness position.[16]
hormone production and release. Secondarily
affects and regulates blood pressure, heart rate,
hunger, thirst, sexual arousal and the circadian Emotional responses
rhythm sleep / wake cycle. Fear
Mammilary body Memory Fear responses are produced by the stimulation of the
Nucleus accumbens Reward, Addiction
hypothalamus and amygdala. Amygdalar destruction
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of the midbrain. Bilateral destruction of the amygdala
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results in placidity. However, when the ventromedian Hypothalamus
nucleus is destroyed after the destruction of the amygdala,
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the placidity generated is converted to rage.[14]
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Autonomic and endocrine responses to emotion
Limbic stimulation causes changes in respiration and
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Autonomic Somatic Immune Endocrine
blood pressure. The stimulation of the cingulate gyrus
and hypothalamus can elicit autonomic responses. There
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is however little evidence for localization of autonomic Figure 8: Limbic system and autonomic and endocrine
responses in limbic circuitry.[14] Hypothalamic autonomic
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responses
responses are triggered by a complex phenomenon mediated
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by the cortical and limbic structures processing drives and Afferent Efferent
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is called the —fiight or fright response“. Stress via cortical and Olfactory
Bulb
limbic connections causes release of corticotropin-releasing
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Sexual behavior Figure 9: Neural Circuit of Male Sexual Behavior CTF: Central
The medial preoptic area of the hypothalamus is a key
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ability. Extracellular glutamate in the MPOA increases during in understanding and dealing with other people. Social
copulation, especially during ejaculation and increased cognition involves regions that mediate face perception,
glutamate facilitates copulation and genital reflexes.[20] emotional processing; theory of mind (TOM); self-reference
and working memory. Together, the functioning of these
Addiction and motivation regions would support the complex behaviors necessary
The reward circuitry underlying addictive behavior includes for social interactions. Limbic structures involved are the
amygdala and nucleus accumbens. The amygdala plays a central cingulate gyrus and amygdala.[12]
role in cue-induced relapse. Relapse associated with cues, stress
and a single dose of a drug of abuse (Comment: which one? CLINICAL IMPLICATIONS
What kind?) results in release of excitatory neurotransmitters
in brain areas like hippocampus and amygdala. The pathway of Epilepsy
motivated behavior involves the prefrontal cortex, the ventral Temporal lobe epilepsy is the most common epilepsy in
tegmental area (VTA), the amygdala especially the basolateral adults and is most often caused by hippocampal sclerosis.
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amygdala and extended amygdala, the nucleus accumbens Hippocampal sclerosis with additional involvement of the
core and the ventral pallidum. This pathway is involved in amygdala and parahippocampal gyrus is termed mesial
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the motivation to take drugs of abuse (drug-seeking) and the temporal sclerosis (MTS). CA1 or the Sommer sector, is
compulsive nature of drug-taking [Figure 10].[21] the region most vulnerable to hypoxia. CA4, sometimes
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described as the endfolium, has intermediate vulnerability
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Memory to insults, whereas CA3, which enters the concavity of the
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Emotional memory gyrus dentate, is only slightly vulnerable. CA2 is the most
Emotion has powerful influence on learning and memory. resistant and well-preserved sector. The frequency and
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Amygdala, in conjunction with prefrontal cortex and medial widespread distribution of these cerebral abnormalities
temporal lobe, is involved in consolidation and retrieval suggest that MTS is not limited to the medial temporal lobe
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of emotional memories. Amygdala, prefrontal cortex and but instead, represents a limbic system disorder.[24]
hippocampus are also involved in the acquisition, extinction
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critical for long-term, declarative memory storage.[22] Limbic encephalitis is a paraneoplastic syndrome that has
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Medial temporal lobe memory system other primaries. The mechanism of disease is not known
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The components include the hippocampus and adjacent but it manifests as encephalitis that primarily involves the
cortex, the parahippocampal regions (PHG) and the hippocampus, amygdala, cingulate gyrus, insula and orbital
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entorhinal and perirhinal regions. This memory system is frontal cortex. Afflicted patients develop subacute onset of
involved in the storage of new memories.[23] memory loss, dementia, involuntary movements and ataxia.[25]
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The diencephalic memory circuit consists of the hypothalamus, Degenerative changes in the limbic system likely have a role
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mammillary body and the dorsomedial nucleus of thalamus. in the genesis of neurodegenerative diseases, particularly
This circuit is important for the storage of recent memory; a Pick’s disease and Alzheimer’s disease. Marked atrophy is
dysfunction of this circuit results in Korsakoff’s syndrome.[23] found in the limbic system, most notably the dentate gyrus
is
Anxiety disorders
Anxiety disorders may be the result of a failure of the anterior
cingulate and hippocampus to modulate the activity of the
amygdala (top-down regulation). A fear circuitry, involving
the amygdala, prefrontal and anterior cingulate has been
described (bottoms-up regulation).[27]
Schizophrenia
Studies have shown reduced limbic volumes in schizophrenia.
The Papez circuit is probably involved in schizophrenia.
Figure 10: Pathway for motivated or goal directed behavior(modified The evidence for this is the distortion of cortical neuronal
from Kalivas and Volkow)[21] organization of layer II of the ERC, decreased size of
hippocampus and the reduced number of GABAergic cells and orbitofrontal cortex may contribute to behavioral
in the cingulate and anterior thalamus with resultant disinhibition seen in individuals with ADHD.[31]
glutamatergic excitotoxicity. The other circuit involved is
the basolateral circuit which mediates the social cognition Kluver-Bucy syndrome
deficits in schizophrenia.[28] Kluver-Bucy syndrome results due to a bilateral
destruction of the amygdaloid body and inferior temporal
Affective disorders cortex. It is characterized by visual agnosia, placidity,
Studies have shown variation in the volumes of the frontal hypermetamorphosis, hyperorality and hypersexuality.
lobes, basal ganglia, amygdala and hippocampus in affective This disorder may be caused by many conditions including
disorders. Functional studies have revealed decreased cerebral trauma; infections including herpes and other
prefrontal and anterior cingulate activity in affective disorders. encephalitides; Alzheimer’s disease and other dementias;
The anterior cingulate is the center for integration of Niemann-Pick disease and cerebrovascular disease.[14]
attentional and emotional output and helps effortful control
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of emotional arousal.[29] Recently, researchers have posited Korsakoff ’s psychosis
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that this spectrum of affective and cognitive symptomatology Korsakoff’s psychosis is caused by damage to mammillary
represents dysfunction within a single extended network— bodies, dorsomedial nucleus of thalamus and hypothalamus
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the anterior limbic network, which includes prefrontal regions (diencephalic memory circuit). It is a syndrome associated
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and subcortical structures such as the thalamus, striatum with chronic prominent impairment of recent and remote
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and the amygdala. The dysfunction of this system (anterior memory. Recent memory is characteristically more
limbic network) is suggested in bipolar disorder, but its role disturbed than remote memory. Immediate recall is
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in depression is unclear [Figure 11].[30] usually preserved. Confabulation may be marked but is not
invariably present.[20]
ADHD
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Limbic structures have been implicated in the genesis Autism
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of attention deficit / hyperactivity disorder (ADHD). Autism and Asperger’s syndrome involve the
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The enlarged hippocampus in children and adolescents disproportionate impairment in specific aspects of social
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with ADHD may represent a compensatory response to cognition. Limbic structures involved include the cingulate
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the presence of disturbances in the perception of time, gyrus and amygdala, which mediate cognitive and affective
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temporal processing
and stimulus-seeking associated processing. The basolateral circuit integral for social
with ADHD. Disrupted connections between the amygdala cognition is disrupted in autism spectrum disorders.[28]
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CONCLUSION
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Behavior Feelings
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Thalamus Hypothalamus The limbic system plays a pivotal role in behavior. The
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Ventromedial Striatum Rostral Insula anterior cingulate, the trisynaptic hippocampal circuitry
underlying cognitive functioning and the significance of
hypothalamus in various neurovegetative functions suggest
Ventrolateral PFC Medial OFC the integral role of the limbic system in understanding
(BA 10, 47) (BA 11)
human behavior and its aberrations.
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News
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The WHO Global Forum for Community Mental Health held its ›rst meeting in Geneva in May 2007. This was attended by mental health
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professionals, consumers, carers, NGOs and policy planners. The Forum provides a foundation for sharing information, providing mutual
support, and a sense of belonging for users, families and providers, and all who are interested in shifting mental health care from long-term
is
institutions to effective community-based care. Forum partners included non-governmental organizations, professional associations and
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interested individuals. Viable options available to communities to improve the lives of people living with mental disorders and exercise their
rights to community-level detection and treatment of mental disorders include:
• Integrating mental health care within the primary health care system;
• Rehabilitating long-stay mental hospital patients in the community;
• Implementing anti-stigma programmes for communities;
• Initiating population-based effective preventive interventions; and
• Ensuring full participation and integration of people with mental disorders within the community.
More information on the Global Forum for Community Mental Health: www.gfcmh.com.
Anybody who is interested in Community Mental Health can be part of the Forum and visit the web site or contact
Dr. R. Thara
Director, Schizophrenia Research Foundation
(SCARF).
R/7A, North Main Road, West Anna Nagar Extension
Chennai - 600101, India, Tel: 26153971, 26151073
E-mail: scarf@vsnl.com. www.scar›ndia.org