Breathing

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The Modification of Breathing Behavior : Pavlovian and Operant Control in Emotion and Cognition
Ronald Ley Behav Modif 1999 23: 441 DOI: 10.1177/0145445599233006 The online version of this article can be found at: http://bmo.sagepub.com/content/23/3/441
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Ley / MODIFICATION OF BREATHING BEHAVIOR MODIFICATION / July 1999
The purpose of this article is to bring attention to breathing as a behavior that can be modified by means of Pavlovian and operant principles of control. With this aim in mind, this paper (a) reviews a selection of early and recent conditioning studies (Pavlovian and operant paradigms) in respiratory psychophysiology, (b) discusses the bidirectional relationship between breathing and emotion/cognition, and (c) discusses theoretical and applied implications that point to new directions for research in the laboratory and clinic. Emphasis is placed on dyspnea/suffocation fear and the acquisition of anticipatory dyspnea/suffocation fear in panic, anxiety, and stress disorders and their concomitant cognitive deficits. Discussions throughout the article focus on research relevant to theory and application, especially applications in programs of remedial breathing (breathing retraining) designed for the treatment of psychophysiological disorders (e.g., panic, anxiety, and stress) and the accompanying cognitive deficits that result from cerebral hypoxia induced by conditioned hyperventilation.
The Modification of Breathing Behavior

Pavlovian and Operant Control in Emotion and Cognition
RONALD LEY
University at Albany, State University of New York
Breathing is the only vital function under direct voluntary control as well as involuntary control. With this said, let me hasten to state that the range of voluntary control (the breaking point of breath holding at one extreme and the loss of consciousness by means of overbreathing/hyperventilation at the other) falls within limits determined by involuntary controls, which are maintained primarily by neural pathways with origins in the medulla and pons. As fundamental as the behavioral control of breathing is in the science of psychophysiology and the art of clinical psychophysiotherapy, laboratory and clinical work on the effects of modifying breathing behavior on emotion and cognition has been neglected (Blanton & Alpher, 1983). The purpose of this paper is to bring attention to the fundamental role of breathing in applied psychophysiology and to
BEHAVIOR MODIFICATION, Vol. 23 No. 3, July 1999 441-479 1999 Sage Publications, Inc.
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encourage research on the modification of breathing behavior. With this aim in mind, this paper will (a) review a selection of early and recent studies in respiratory psychophysiology in which Pavlovian (classical/respondent) and instrumental/operant conditioning paradigms have been employed, (b) discuss the bidirectional relationship between breathing and emotion and cognition with emphasis on the effects of breathing on emotion and cognition, and (c) discuss some theoretical and applied implications of research findings for new directions for research in the laboratory and the clinic.
CONDITIONED BREATHING AND EMOTIONS
From the breath that marks the beginning of life to the breath that marks the end, breathing is a basic behavioral expression of the psychological and physiological state of human beings. Vocalizations that range from reflexive cries of the distressed infant (unconditioned responses) to the persuasive speech of the sophisticated orator depend on breathing maneuvers reinforced by their effects (i.e., operant control). Similarly, the frequency and intensity of the grunts and groans, cries and shrieks, sighs and gasps, and titter and laughter that are emitted in the oral language of everyday discourse and that convey a part of the emotional message that underlies the denotative meaning of our words are rooted in breathing. The volitional nature of breathing that provides the means for blatant to subtle communication also provides us with primal behavioral advantages. The ability to hold ones breath is an adaptive response that aids concealment and the ability to swim and hunt beneath water; and overbreathing is an adaptive response that prepares us for fighting or fleeing a threatening force. Although the physiological/vegetative role of respiration in gas transference (i.e., delivery of oxygen [O2] to support metabolism and removal of carbon dioxide [CO2] as a byproduct) and maintenance of acid-base balance (pH) may be fairly uncommon knowledge, the psychological role of breathing on emotion/cognition is even more esoteric. In terms of research, a vast amount of work in respiratory physiology has led to a relatively comprehensive understanding of the physiology of involuntary control of breathing (e.g., Bouhuys, 1977; Comroe, 1974; Fenn & Rahn, 1964; Gray, 1950; Jennett, 1995),
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whereas a relatively meager amount of research in respiratory psychophysiology has provided little more than a rudimentary understanding of voluntary control of breathing (Ley, 1995; Ley, Timmons, Kotses, Harver, & Wientjes, 1996; Timmons & Ley, 1994). Because Pavlovian conditioning procedures provide the means for exploring the extent to which involuntary/reflexive changes in breathing can be acquired (i.e., controlled by the contextual environment in which responses can be elicited), research designed to study the parameters of conditioned changes in breathing holds the promise for results that should contribute greatly to a more complete understanding of the means by which breathing behavior can be modified in the treatment of chronic lung diseases (e.g., asthma, bronchitis, and emphysema), breathing-related behavioral disorders (e.g., panic disorder), stressinduced psychosomatic complaints (e.g., carpal-tunnel syndrome), anxiety disorders (e.g., test anxiety), occupational health (e.g., chronic fatigue syndrome), and other disorders in which dysfunctional breathing is involved (see Timmons & Ley, 1994).
PAVLOVIAN CONDITIONING
Pavlovian conditioning is fundamental to an understanding of psychology in general and to the psychophysiology of breathing in particular because it provides a paradigm from which a theoretical framework for a process of learning can be derived, a framework that unites emotion, cognition, and instrumentally conditioned behavior (voluntary responses). Contemporary liberalized interpretations of Pavlovian conditioning have expanded the scope of the process from its origin in the issues of spit-and-twitch reflexes of Pavlovs (1897/1902) psychic secretion, Sherringtons (1900) conditioned emotional anxiety, and Twitmyers (1905) conditioned knee-jerk (patellar tendon reflex) to the complex issues of everyday living (e.g., Jones, 1924; Watson, 1924; Watson & Rayner, 1920; Wolpe, 1958, 1990), especially issues related to the treatment of anxiety-motivated dysfunctional behavior. The details of a modern conception of Pavlovian conditioning can be found in reviews by Rescorla (1967, 1988), and the implications of a liberalized interpretation for behavior therapy are presented in an article by Davey (1989). For the purposes of
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this paper, Pavlovian conditioning can best be understood from both an information-theory point of view (S-S), in which subjects evaluate events in a specified context (time and place) on the basis of their previous experiences for the purpose of determining the likelihood that one event (CSconditioned stimulus) reliably signals a subsequent second event (UCSunconditioned stimulus), and from a reflextheory point of view (S-R). Humans, by their nature, appear to be correlational cogitators, animals who demonstrate a profound need to predict events in an attempt to control their environment. Perhaps, more than anything else, this attribute underlies the spirit of scientific inquiry. We also have a profound curiosity that makes us ask the question: What leads to what? And when answers are not forthcoming, we often experience psychological unrest that expresses itself in feelings of frustration and anxiety. A liberalized interpretation of Pavlovian conditioning encapsulates the adaptive process by which we increase the accuracy of our predictions. Sometimes, however, misinformation and unfortunate vagaries of life can lead to maladaptive conditioned associations that interfere with attainment of goals of everyday living. This is especially true of associations that give rise to anxiety that inhibits our behavior.
THE CONDITIONED EMOTIONAL RESPONSE
Although the association between Pavlovian conditioning and the drooling dog is well established, the association between Pavlovian conditioning and the panting dog is not. Perhaps C. S. Sherringtons (1900) discovery of conditioned emotional anxiety provides an example closer to the concerns of respiratory psychophysiologists. Sherrington (1900), whose interest centered on vasomotor reflexes of the circulatory system, used a procedure that required surgical exposure of a nerve through which he could pass an electric current generated by an inductorium which emitted a vibratory humming noise during a warm-up period prior to delivery of the electric current. During the course of his experiments, Sherrington made the serendipitous observation that circulatory system responses (changes in heart rate and blood pressure) occurred following the onset of his noisy shock
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generator, but prior to delivery of the electric shock. Because the changes were consistent with what might be expected if shock were anticipated, Sherrington called the response to the noise of the shock generator emotional anxiety. Although Sherrington (1900) is little remembered for this work, electric shock as a UCS is by far the most commonly used technique in current studies that follow Pavlovian conditioning procedures (Mongeluzi, 1996). The reason for this is not only because of the relative simplicity and ease of experimental control, but because the conditioning of fear (the conditioned emotional response) is of utmost relevance to the study of human behavior, whereas salivation is not. It may be important to add that the term anxiety is often used to distinguish signaled fear (CRconditioned response) from unsignaled fear (UCRunconditioned response), a distinction that is fundamental to an understanding of the significance of Pavlovian conditioning in human adaptation. In a concise statement that nicely incorporates Cannons (1915) concept of a fight/flight response, Salter (1961) said, anxiety is thus basically anticipatory in nature and has great biological utility in that it adaptively motivates living organisms to deal with (prepare for or flee from) traumatic events in advance of their actual occurrence, thereby diminishing their harmful effects (p. 221). This statement illustrates how Pavlovian conditioning unites the psychological concepts of emotion (anxiety) with cognition (the anticipation of a threatening event) and behavior (preparation for encounter with or flight from the threatening event).
CONDITIONED FEAR/ANXIETY AND BREATHING
When Sherrington (1900) reported on his discovery of conditioned emotional anxiety, he made only a small mention of breathing. This is not because changes in ventilation did not occur in response to the electric shock (UCS) or the sound of his noisy inductorium (CS), but because Sherrington limited his measure of ventilation to respiratory frequency. There are at least two reasons why he did so. One is that his interest was focused on the circulatory system, not respiration; the
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other is that the methods of measuring ventilation during his time were complicated, crude, inaccurate, and intrusive.
Problems of Measurement
Hyperventilation is defined as breathing a volume of air that exceeds metabolic demand for O2. (See Ley, 1991b, for a demonstration of the distinction between hyperventilation and hyperpnea.) Although hyperventilation is typically measured in terms of low PCO2 (i.e., PaCO2, the partial pressure of CO2 in arterial blood, or PetCO2, the proportion of CO2 at the peak of end-tidal expiration), a basic underlying metric of ventilation is the volume of air breathed. Thus, if metabolic demand is constant, an increase in ventilation (i.e., an increase in minute volume, the amount of air breathed in terms of liters per minute) indicates hyperventilation. With a little thought, the complications of measuring minute volume become apparent. The measuring technique requires either a closed system in which the volume of air breathed is carefully monitored via an inhalation mask, canopy, or mouthpiece with nose clip, or an open system in which changes in the displacement of the trunk are used as an index of the volume of air used to swell the thoracic cavity. Aside from instrumentation complications, all these methods are fairly intrusive and bring the subjects attention to the fact that breathing is being measured, an unsettling fact which can alter ventilation from what it would be if it werent being measured, an interesting psychological phenomenon in its own right (see Ley, 1987b). Perhaps for these reasons, more than any others, research in respiratory psychophysiology prior to the advent of the infra-red gas analyzer (the capnometer/capnograph as a noninvasive and unobtrusive means by which alveolar pCO2 is measured) limited measurement of breathing behavior to respiratory frequency, respiratory volume, respiratory mode (diaphragmatic vs. thoracic), or temporal pattern of breathing (e.g., apneic and apneusic pauses, panting, inspirationexpiration ratio). Crude though these methods of measurement might be, they did yield evidence that indicated ventilatory changes accompanying emotions and that these changes are amenable to the effects of Pavlovian conditioning.
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PAVLOVIAN CONDITIONING AND VENTILATORY RESPONSES
In view of recent interest in Brown, Kalish, and Farbers (1951) use of startle response in rats in the study of emotion and Merymans (1953) demonstration of potentiation of electrodermal conductivity in humans (cf. Lang, Bradley, & Cuthbert, 1990), it may be important to note that ventilatory changes accompany this most rudimentary of adaptive reflexes. In the startle response, contraction of the abdominal muscles compresses the gut, thus restricting contraction of the diaphragm and increasing contraction of intercostals to accommodate the increase in ventilation that accompanies the heightened arousal (sympathetic dominance of autonomic nervous system); the increased minute ventilation will be expressed in either increased tidal volume or increased respiration frequency (i.e., panting) or both. Both the startle response (a reflexive contraction of muscles in response to the sudden, sharp onset of a relatively intense unsignaled stimulususually a sound) and the orientation reflex (i.e., Pavlovs (1927) what is it? reflex) involve ventilation. In the case of the startle response, the ventilatory behavior consists of a spasmodic gasp (rapid inhalation of a single breath) followed by apneusis (cessation of breathing in the inhalation phase of the respiratory cycle); in the case of the orientation reflex, ventilatory behavior is characterized by apnea (cessation of breathing in the exhalation phase of the respiratory cycle). Some of the following studies use these adaptive reflexes in their demonstration of conditioned modifications in breathing.
EARLY STUDIES
Ventilatory conditioning has a long history in the relatively short history of the science of psychology; and psychologists who played important roles in the early years of the development of their science recognized the sensitivity of respiration to conditioning procedures (Watson, 1916; Bekhterev, 1917/1932). A survey of a selection of studies published between 1929 and 1946 reveals clear evidence that a variety of animals, including humans, have been conditioned to modify their breathing (increase in respiration frequency or volume or
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both, pattern of breathing, apneic pauses) by means of the Pavlovian paradigm. The basic design of most of these studies involved the use of an auditory stimulus (CS) paired with a shock to a limb (UCS), and the reported results included an increase in respiratory frequency or volume or both (CR). Consistent results were obtained in guinea pigs (Horton, 1933; Upton, 1929), cats (Wever, 1930), rats (Kappauf & Scholsberg, 1937), dogs (Allen, 1942; Walker & Kellogg, 1939), goats (Goldman, 1939), sheep (Anderson & Parmenter, 1941), and humans (Finkelstein, Alpern, & Gantt, 1945; Garvey, 1933; Scott, 1930). Two of the studies surveyed measured the effect of a Pavlovian auditory stimulus-discrimination task on breathing. Dworkin (1939), who used cats and dogs, reported that as the difference between the frequencies of two tones grew smaller, depth of respiration (volume) grew larger. Gantt (1944), who used dogs, reported that the increasing difficulty in discriminating between two tones led to polypnea (rapid respiratory frequency) and inspiratory gasps. Long apneic pauses following very large numbers of conditioning trials (8,000), in which an auditory stimulus was paired with shock, were observed in goats and sheep after the first 3,000 of 8,000 trials by Minami, Moore, and Liddell (1943). Caldwell (1946), who used 2,740 to 2,920 shock trials with sheep, reported stimulus generalization of the lengthy apneic pauses. In one of the earliest studies to combine instrumental conditioning with an aversive stimulus designed to elicit changes in ventilation, Masserman (1943) used food as a positive reinforcer in a task that required cats to lift the lid of a box following the onset of a light or auditory signal (CS). After the lid lifting response was well established, lifting the lid following onset of the CS was punished by a blast of air (UCS). On subsequent test trials, the onset of the CS was followed by disturbances in patterns of breathing (CR). Another unique study with considerable relevance for the purpose of this paper was conducted by Finesinger and Mazick (1940). Human participants were subjected to a brief but painful cutaneous stimulus (pinpricks to the flesh of a hand). After an interval following the subsidence of pain, participants were instructed to recall the painful stimulation. The recall period was found to be accompanied by an increase in respiration. The significance of this simple demonstration has
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broad implications for the connection between physical pain, emotion, cognition, and breathing.
RECENT STUDIES
In those studies cited previously in which increases in respiration frequency or volume or both were acquired as CRs, the strong inference is that these increases indicate hyperventilation. This would assuredly be the case if one makes the very reasonable assumption that metabolic demand was relatively constant during conditioning trials. That is, if the increases in ventilation exceeded metabolic demand, then hyperventilatory breathing had been acquired as a CR. The reasonableness of the assumption of a relatively stable metabolic rate is based on the fact that the conditioning procedures required the animals to be immobilized during conditioning trials by devices such as the Pavlovian sling, a harness that suspends the animal in the air, thus preventing it from moving away from the experimental station where the CS and UCS are delivered. Because the animal cannot move and is not required to support its weight by standing, metabolic demand should be very low. As reasonable as the assumption of stable metabolism is, the observation of conditioned breathing is not incontrovertible proof of conditioned hyperventilation. Direct evidence requires a measure of PaCO2 or a measure of PetCO2. A few recent studies have used the capnograph to monitor changes in PetCO2 during Pavlovian conditioning procedures. If the level of PetCO2 in response to the CS subsequent to conditioning trials is lower than the level in response to the CS prior to conditioning trials, then virtually irrefutable evidence of conditioned hyperventilation has been demonstrated.
Conditioned Overbreathing
One research program designed to study the modification of breathing behavior (respiratory learning) and psychosomatic complaints has employed a ventilatory conditioning paradigm in which small concentrations of CO2 in room air (5.5% to 7.5%) have been used as the UCS paired with a CS consisting of odors (niaouli or dilute
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ammonia) or oral statements designed to elicit fear-inducing thoughts, namely, listening to descriptions of anxiety-eliciting scenes and instructions to imagine the anxiety-eliciting scenes (Stegen, Van den Bergh, & Van de Woestijne, 1995; Van den Bergh, Kempynck, Van de Woestijne, Baeyers, & Eelen, 1995; Van den Bergh, Stegen, & Van de Woestijne, 1995a, 1995b). More recent research (Van den Bergh, Stegen, & Van de Woestijne, 1997) has produced some evidence of conditioned ventilatory responses (respiration frequency, tidal volume, and minute volume), but the results are not clear-cut because test trials following the differential conditioning paradigm (CS+ is stimulus paired with UCS and CS is stimulus not paired with UCS) showed that ammonia was an effective CS+ but niaouli was not. Additional interactions indicated that conditioning depended on gender difference, that is, women responded with larger respiratory frequencies than men did, whereas men responded with larger tidal volume. Aside from the difficulty in interpreting these data, the use of CO2 as a UCS is problematic. Although CO2 will increase ventilation (e.g., prolonged breathing of 5% CO2 in air will triple minute volume), it precludes hyperventilation because it increases PetCO2 by about 10 mmHg (see Ley, 1991b). Although it is true that hyperventilation follows immediately on the termination of the CO2 UCS, the UCR (breathing during presentation of the UCS) consists of increases in frequency and volume (conditions that typically produce hyperventilation when breathing room air, i.e., air that accompanies the CS), but it increases PetCO2 (a condition which indicates hypoventilation when breathing room air) as well. This may be an inconsequential criticism because an increase in ventilation (CR), regardless of the means by which it is acquired, will produce hyperventilation when breathing room air, given no corresponding increase in metabolism. These criticisms aside, the new research cited here is an important first step in the attempt to condition hyperventilatory breathing by means of a paradigm for testing the parameters of conditioning and offers a means for studying breathing-related psychosomatic complaints.
Conditioned Hyperventilation
Another recently begun research program (Ley, Ley, & Bassett 1996) has been successful in its initial attempt to provide a demonstra-
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tion of conditioned hyperventilation. In earlier studies, in which CRs were defined as increases in respiration frequency or volume or both, conditioned hyperventilation almost certainly occurred; but these studies did not measure PCO2 and thus could not provide definitive evidence of conditioned hyperventilation. Ley, Ley, and Bassett (1996), however, monitored PetCO2 continuously in healthy young adults (college students) throughout all phases of a conditioning procedure in which mental stress/workload (serial 7s/17s taskcounting backward from a given number in the hundreds by 7s or 17s) was used as the UCS and a buzzer (500 Hz at about 60 db) served as the CS. The level of PetCO2 (CR) in response to the CS following four pairings of the CS and UCS was found to be significantly lower when compared with the level of PetCO2 in response to the CS prior to conditioning trials but following two habituation trials (presentations of the CS before pairing with the UCS). Confirmatory evidence of conditioning was found in concomitant measures of respiration frequency, heart rate, and electrodermal conductivity (inverse correlates of PetCO2, all of which showed corresponding increases). The clinical significance of these findings lies in their support of Lums (1976) well reasoned and persuasive thesis that a wide range of hyperventilation-related psychosomatic complaints are experienced by susceptible individuals [who] have acquired a habit of breathing in such a way that the day-to-day level of arterial CO2 is low, or that the normal hyperventilatory response to physical or emotional stimuli is exaggerated. . . . With frequent repetition, the response takes on the characteristics of a conditioned reflex. (p. 198). If hyperventilatory breathing can be acquired, then therapies aimed at the treatment of psychosomatic complaints should evaluate breathing in the course of diagnosis and add the modification of dysfunctional breathing (i.e., remedial breathing) to relevant treatment strategies. Although the preliminary findings of Ley, Ley, and Bassett (1996) and those of Van den Bergh et al. (1997) are encouraging, considerable research remains to be conducted for the purpose of establishing the parameters of their conditioning procedures and testing those procedures in the context of appropriate conditioning phenomena (e.g., stimulus generalization and discrimination, extinction, UCS intensity, numbers of conditioning trials, trace delay, etc.) with clinical as well as diverse nonclinical populations.
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Conditioned Respiratory Resistance
Total respiratory resistance (the impedance in the flow of air by the airways, lung tissue, and chest wall) is an important factor in the maintenance of good health in general and a critical factor in disease, especially chronic lung disease (asthma, bronchitis, and emphysema). Because asthma is so prevalent in the general population, the asthmatic attack (dyspnea evoked by the reduction in breathing that results from insufficient expiration) is commonly understood to be caused by constriction of the bronchioles, that is, an acute increase in total respiratory resistance. Although the rudimentary physiology of asthma (involuntary controls of breathing) have been well researched, voluntary control of breathing as a factor in the evocation of asthmatic breathing has received relatively little attention. Several studies that point to the conditionability of airways/respiratory resistance will be noted here. Dekker, Pelser, and Groen (1957) conducted one of the first studies of classical conditioning to demonstrate that an asthma attack could be acquired as a conditioned response. Although an increase in total respiratory resistance is an underlying feature of asthma attacks, the conditionability of increased respiratory resistance need not be limited to asthmatics if an agent other than an asthma-specific allergen could be identified as a UCS for the evocation of an increase in respiratory resistance as the UCR. Kotses, Westland, and Greer (1987) identified such an agent: a mental stress test consisting of the arithmetical computations required to count backward by 17s. Utilizing a differential classical conditioning paradigm, Miller and Kotses (1995) paired one of two colored (red or green) lights with a UCS (counting backward by 17s) that evoked an increase in total respiratory resistance. Over the last of seven conditioning trials, the increase in total respiratory resistance elicited by the CS+ was greater than that elicited by the CS; that is, increased total respiratory resistance in healthy young adults can be acquired as a CR by means of Pavlovian conditioning. Because dyspnea is the sensation that accompanies increased respiratory resistance, these findings have important implications for the diagnosis and treatment of respiratory psychophysiological disorders in general and for Leys (1989) dyspnea/suffocation fear theory of panic attacks in particular. That is, increased respiratory resistance, a common UCR to stress, may contribute to the heretofore inexplicable
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out-of-the-blue onset of uncontrollable dyspnea and its accompanying dyspneic/suffocation fear, the fear that characterizes the classic Type I panic attack (see Ley, 1989, 1992).
Conditioned Increase in Duration of the Respiratory Cycle
The respiratory cycle consists of an inspiratory phase and an expiratory phase, but recent neurological evidence reported by Bianchi, Denavit-Saubie, and Champagnat (1995) suggests that distinct excitation of several respiratory nerves during the apneic pause that follows the inspiratory phase may indicate a third phase. Regardless, the total time for the respiratory cycle remains the same. Gallego and Perruchet (1991a) have demonstrated that an increase in the duration of the respiratory cycle can be classically conditioned by pairing a tone (100 Hz at about 20 db) with a hypoxic UCS, that is, a UCS that consists of a reduction of O2 in inspired air to about 3%. These findings not only make a strong case for the relative ease of conditionability of a ventilatory response (8 respiratory cycle trials), but also provide strong experimental evidence that supports the efficacy of modifying breathing behavior by means of breathing retraining programs:
It is worth noting that only eight trials were needed to obtain the conditioned response. Given that ventilatory stimuli are frequently associated with numerous sensory stimuli in everyday life, the findings provide some insights into the potential impact of conditioning in breathing and strengthen the assumption made by several authors on this point. They also provide some support for the hypothesis implicit to many breathing therapies that breathing pattern can be changed through learning. (Gallego & Perruchet, 1991a, p. 680)
OPERANT CONTROL OF BREATHING
Operant conditioning has been used widely in the study of physiological systems, especially pharmacological effects on cardiovascular and endocrine systems in which changes in the system are measured as concomitant variables, that is, variables that change under conditions in which the operant (e.g., a lever press) is controlled by nega-
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tively reinforced fixed-interval or fixed-ratio schedules. Although complications in the measurement of respiratory parameters appear to have limited their inclusion in the study of effects of drugs on operant behavior, Howell and Landrum (1994) provide a clear demonstration of how breathing can be monitored continuously in the rhesus monkey (or other primates) by means of a pressure-displacement-head plethysmograph. Although Howell and Landrum (1994) did not measure PetCO2, the system they describe could be readily adapted to accommodate a capnograph; their minute volume and respiration frequency data suggest strongly that hyperventilation occurred during fearmotivated test trials. In addition to biofeedback procedures, physiological responses have been studied directly as conditioned operants. Such research has concentrated for the most part on heart rate and blood pressure as operant behaviors for the purpose of studying their role in the etiology of hypertension (e.g., Engel & Schneiderman, 1984). Programs of remedial breathing (often referred to as breathing retraining) provide obvious examples of clinical applications of operant conditioning in correcting dysfunctional breathing (see Timmons, 1994), and programs of research on operant control of breathing in the laboratory are gaining attention (e.g., Gallego et al., 1986; Gallego & Camus, 1989; Gallego & Perruchet, 1991a, 1991b). Preliminary evidence that inspiration duration, as a conditioned operant, can be modified in the rat by means of reinforcement consisting of electrical stimulation of the medial forebrain bundle can be found in a study by Gallego et al. (1994). Although this single-case study limits generalizations, the unique method for the measurement of ventilation employed provides an exemplary model for future research in this promising but relatively unexplored region of respiratory psychophysiology. Another recent study by Esteve, Blanc-Gras, Gallego, and Benchetrit (1996) provides evidence to support Gallego and Perruchets (1991a) claim that breathing patterns can be changed. In a controlled experiment with patients suffering chronic obstructive lung disease, patients randomly assigned to a biofeedback breathing pattern training group (n = 9) showed a significant improvement of (a) 22% in FEV1 (forced expiratory flow, i.e., the ratio of the volume of air expired during the first second of exhalation, following a full capacity
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inhalation, to total forced vital capacity) and (b) 19% in FVC (forced expiratory vital capacity, i.e., the rate at which air is expired during a full capacity exhalation following a full capacity inhalation). Control group patients (10 subjects who did not receive the biofeedback breathing pattern training) showed no significant changes. This study lends strong support to the underlying rationale of breathing retraining programs (i.e., remedial breathing programs), namely, that breathing patterns (behaviors) can be modified by conditioning procedures, procedures that have a salutary effect on health in general and on the health of patients who suffer breathing disorders. For the purposes of this paper, the significance of the basic research cited here lies in the clear demonstration of the fact that breathing behavior is amenable to the principles of Pavlovian and operant conditioning. The implications of this fact bear directly on the development of treatment strategies aimed at correcting dysfunctional breathing (i.e., improving breathing) and its psychophysiological sequelae. If dysfunctional breathing is a consequence of conditioning, then functional breathing should obtain, as a consequence of remedial breathing, methods that would include counterconditioning.
FRUSTRATION, STRESS, AND HYPERVENTILATION
The frustration effect is the increase in force of a response that occurs during the first few nonreinforced trials following a series of continuously reinforced acquisition trials. Marzocco (1951) first demonstrated the effect by comparing the force that rats exerted on the lever of an instrumental conditioning apparatus during continuously reinforced trials with the force exerted during extinction (nonreinforced) trials. Results indicated an increase in force from 28 grams on the first nonreinforced trial to 35.9 grams on the following nonreinforced trial. In subsequent research on a force-discrimination task with human subjects, Blixt and Ley (1969) demonstrated the frustration effect following positive reinforcement, and Ditkoff and Ley (1974) demonstrated the effect following negative reinforcement. Although the frustration effect has been studied extensively (e.g., Amsel, 1958; Brown &
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Farber, 1951; Daly, 1974; Graham & Longstreth, 1970; Lambert & Hammond, 1970; Levine & Loesch, 1967; Ryan & Watson, 1968), no physiological correlates of frustration were reported until Otis and Ley (1993) studied the time course of the frustration effect in a forcediscrimination task. Aside from discovering that the effect is shortlived in humans, Otis and Ley (1993) found a positive correlation (r = .74) between the magnitude of the frustration response (force on a reset lever) and the amplitude of the electrodermal response (i.e., increase in electrical conductivity of skin) only for that group which demonstrated the frustration effect (i.e., brief delay). The significance of this finding lies in the fact that the electrodermal response is, albeit not exclusively, a direct and immediate consequence of hyperventilation (Kartsounis & Turpin, 1987) and has been observed on the occasion of adventitious panic attacks in the laboratory during physiological assessment by Lader and Mathews (1970) and in a clear-cut demonstration of a classic Type I panic attack (see Ley, 1992, for a detailed discussion of the psychological and physiological distinctions between types of panic attacks) by Sanderson (1987) and Sanderson, Rapee, and Barlow (1988). More recent evidence of the direct effects of frustration on breathing has been reported by Schleifer and Ley (1994, 1996). In a study of stress on data-entry tasks among video-display-terminal operators working on an incentive-pay basis, Schleifer and Ley (1994) monitored respiration rate and PetCO2. Constant monitoring during two 120-minute work periods each day for three consecutive days showed consistent changes in breathing. Each session began with a 5-minute baseline period in which subjects sat quietly with eyes closed followed by a 5-minute period of progressive muscle relaxation instructions followed by 120 minutes of numerical data entry work. During the relaxation period following each 5-minute baseline period, respiration rate dropped and PetCO2 increased. Throughout the work period of the third day, immediately following the relaxation period, respiration frequency showed a sharp increase and PetCO2 showed a sharp decrease, which are findings consistent with hyperventilatory breathing and increased arousal. These findings are of special interest to applied psychology because they demonstrate the sensitivity of respiration to the beneficial effects of relaxation as well as to the detrimen-
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tal effects of stress in the context of the video display terminal work environment, the modal workplace of the future, if not the present.
CONDITIONED FEAR, FRUSTRATION, AND HYPERVENTILATION
The studies cited previously make it clear that the procedure for conditioning ventilatory responses (viz., hyperventilation or hyperventilation interspersed with apneic pauses) is the same procedure used to condition fear or frustration. In the case of fear, the UCS consists of a hedonically negative and physically noxious stimulus that produces physical pain and threatens tissue injury (e.g., electric shock); whereas in the case of frustration, the UCS consists of a hedonically negative and psychologically noxious stimulus that produces psychological pain (anguish?) and threatens psychological integrity (e.g., an unsolvable discrimination). Thus, it is quite reasonable to assume that the vast experimental literature on fear (e.g., Ley, 1965; Miller, 1951; Mowrer, 1939; Pavlov, 1927; Solomon & Wynne, 1953; Watson & Rayner, 1920; Wolpe, 1952) and frustration (e.g., Amsel & Rousel, 1952; Blixt & Ley, 1969; Brown & Farber, 1951; Daly, 1971, 1974; Ditkoff & Ley, 1974; Otis & Ley, 1993) applies to conditioned hyperventilation as a counterpart of conditioned fear and conditioned frustration. The behavioral technique for measuring the strength of conditioned fear (and conditioned frustration) is based on the inference that the aversive emotion acts as an acquired drive, that is, a noxious state whose reduction is reinforcing. Thus, the vigor of instrumental avoidance responses negatively reinforced by fear reduction reflects the strength of the underlying conditioned fear. Lengthy programs of research (McAllister & McAllister, 1971, 1991; McAllister, McAllister, Scoles, & Hampton, 1986) attest to the soundness of this paradigm. If hyperventilation is a conditionable counterpart of conditioned emotional responses, then those parameters that affect conditioned fear should have a parallel effect on conditioned ventilation. Thus, Miller and Lawrences (1950) demonstration that the strength of conditioned fear is a direct function of the intensity of the UCS would
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apply to the hyperventilatory response. That is, the magnitude of overbreathing should also be a function of the intensity of the UCS. Kalishs (1954) demonstration that the strength of conditioned fear is a function of the number of conditioning trials (CS-UCS pairings) and extinction trials (CS not paired with UCS) should also apply to conditioned overbreathing. Aside from these basic parameters of conditioning, other conditioning phenomena such as the generalization of conditioned fear (Porter, 1959) would be expected to apply to conditioned hyperventilation. Caldwell (1946) reported observations of heightened breathing among sheep in rooms adjacent to the experimental conditioning chamber. Furthermore, the individual differences in ventilatory conditionability mentioned by Caldwell is consistent with Leys (1975) observation that individual differences in emotionality of rats (measured in terms of fecal boluses) during fear conditioning trials was positively correlated (r = .63) with the strength of conditioned fear. If ventilatory conditioning parallels the process of fear conditioning, then the one-trial traumatic fear conditioning in dogs reported by Solomon and Wynne (1953) may have special relevance for conditioned ventilation. This experimentally derived effect supports clinical reports that one severe hyperventilatory panic attack, marked by dyspnea/suffocation fear, can sometimes lead to what appears to be intractable panic disorder so severe that some sufferers meet the DSM-IIIR criteria for post-traumatic stress disorder (McNally & Lukach, 1992). Although the bulk of experimental research on escape and avoidance behavior has used electric shock or acquired fear or both as sources of motivation, there have been a few studies that have used aversive ventilatory states (dyspnea) for this purpose. (It should be kept in mind, in this context, that the need for air leads the list of biological needs immediately essential for the maintenance of life.) In one such study, Broadhurst (1957) submerged rats in water and required them to learn to discriminate between the brighter of two sides of an underwater maze in order to escape. Three levels of difficulty in discrimination were studied in conjunction with five different intervals of submersion (0, 2, 4, 6, or 8 s) prior to release in the maze. Although the outcome of this research with respect to Broadhursts
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(1957) hypotheses is not relevant here, it is of interest to note that there was an interaction between the difficulty of the discrimination and the time of air deprivation prior to release in the maze. That is, performance in the maze was a function of level of air deprivation. Thus, levels of dyspnea (or the fear of anticipated suffocation, i.e., dyspnea/suffocation fear) can motivate behavior in a manner parallel to levels of deprivation of a primary appetitive need (e.g., hunger or thirst) or levels of a primary aversive need (e.g., pain) or levels of strength of an acquired motive (e.g., fear or frustration). Another study that demonstrates the noxious motivational state of air deprivation was conducted by Leukel and Quinton (1964). In this study, rats were trained to jump a hurdle to escape shock. After 15 conditioning trials, a subgroup of animals was subjected to CO2 anesthetization immediately following the hurdle jump. Poor performance on subsequent opportunities for avoidance responses of shock indicated the noxious character of breathing CO2 when concentrations were so high that they produced coma, findings that indicate an avoidanceavoidance conflict in which dyspnea/suffocation fear overrode shock fear. These findings are consistent with those of Ley and Walker (1973), who observed in human subjects that the brief immediate effect of single inhalations of 65% CO2 and 35% O2 was noxious.
Dyspnea/Suffocation Fear
Dramatic evidence that dyspnea/suffocation fear can be acquired as a CR in humans following a single conditioning trial is provided by Campbell, Sanderson, and Laverty (1964). In a controlled experiment, Campbell et al. paired a tone (CS) with a 90- to 100-second period of respiratory paralysis (UCS) induced by succinylcholine chloride dihydrate. On subsequent presentations of CS, subjects exhibited virtually inexhaustible bouts of increased respiration rate, heart rate, electrodermal conductivity, and self-reports of fear (CR). Additional evidence that dyspnea/suffocation fear can be conditioned in one trail is given by Mongeluzi, Rosellini, Caldarone, Stock, and Abrahamsen (1996), who placed rates in an atmospherically controlled chamber permeated with the odor of vanilla (CS) for a 5-minute period, the last 30 seconds of which the chamber was infused with 100% CO2 (UCS).
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The day following this single conditioning trial, half the animals were placed in the test chamber containing the odor of vanilla in room air (i.e., CS but no UCS) for an 8-minute period during which freezing behavior (inhibition of movement, an index of fear) was measured. The other half of the conditioned animals were tested in the absence of the CS; a third group that had not been conditioned were tested in the presence of the CS. The results pointed clearly to the fear-eliciting potency of the CS in the context of the conditioning chamber for the animals that had received the single conditioning trial on the day prior to testing, an effect that was notably resistant to extinction. These results were replicated in a second experiment (Mongeluzi, Caldarone, Stock, Rosellini, & Ley, 1998) in which the intensity of the UCS (i.e., concentrations of CO2: 0%, 5%, 35%, 100%) was manipulated and resistance to extinction was measured as well. Animals exposed to 100% CO2 showed greater resistance to extinction (i.e., a more gradual decrease in magnitude of CR over extinction trials) than animals exposed to 35% CO2 and 5% CO2 (no evidence of conditioning in the 0% CO2 group), results which suggest strongly that the magnitude of fear conditioned was a direct function of the severity of dyspnea experienced during the single conditioning trial. This animal model lends strong support to the dyspnea/suffocation fear theory of panic disorder. The Broadhurst (1957), Campbell, Sanderson, and Laverty (1964), Leukel and Quinton (1964), and Mongeluzi et al. (1996) studies illustrate nicely the extent to which negative ventilatory states can provide strong motivation for the acquisition or inhibition of instrumental (volitional) behavior. The significance of this research becomes clearer when considered in the context of agoraphobic panic-avoidance behavior motivated by dyspnea/suffocation fear (Ley, 1989).
BREATHING AND EMOTIONS
The foregoing discussion of conditioned emotions and breathing makes it clear that emotional arousal gives rise to changes in ventilation. The next issue centers on the effect of voluntary changes in ventilation on emotional arousal. Is the connection between emotions and breathing a bidirectional relationship in which changes in one lead to
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changes in the other? Anecdotal evidence suggests that the answer is yes, but everyday experiences and folklore only provide a starting point for medicine and the controlled observations of science. Perhaps the oldest systematic, albeit nonscientific, study of the effects of breathing on experience and behavior can be found in the yogic methods of meditation. (For concise reviews, see Chandra, 1994; Fried, 1987). Modification of these breathing exercises, free of mystical trappings, has been incorporated into the remedial breathing techniques used by respiratory therapists in the treatment of chronic lung diseases (asthma, bronchitis, and emphysema); stress-related disorders; and virtually all successful behavioral, cognitivebehavioral, and cognitive programs designed to treat panic disorder and related anxiety disorders. Although clinical assessments of the efficacy of such programs have been favorable (e.g., Lum, 1976, 1983), a growing number (see Ley, 1991a, 1993) have demonstrated objective measures of physical as well as psychological indices of positive change (e.g., Bonn, Readhead, & Timmons, 1984; Clark, Salkovskis, & Chalkley, 1985; DeGuire, Gevirtz, Hawkinson, & Dixon, 1996; DeGuire, Gevirtz, Kawahara, & Maguire, 1992; Rapee, 1985; Salkovskis, Jones, & Clark, 1986). Among those studies that have focused on the direct effect of controlled breathing on physiological and psychological measures of experimentally induced emotional arousal, McCaul, Solomon, and Holmes (1979) reported that voluntary retardation of breathing rate was found to reduce physiological arousal (decreased electrodermal response and increased finger-pulse volume) and psychological arousal (reduced scores on self-reports of anxiety). In a related study, Cappo and Holmes (1984) demonstrated that breathing controlled by means of voluntary prolongation of the exhalation phase of the respiratory cycle relative to the inhalation phase (i.e., brief inhalation and prolonged exhalation) reduced physiological and psychological arousal induced by the threat of electric shock. Perhaps the most direct test of the connection between hyperventilation and emotional arousal was conducted by Thyer, Papsdorf, and Wright (1984). In this study of normal, healthy, college students, measures of PetCO2, finger temperature, and self-reports of anxiety were made prior to a brief period of voluntary hyperventilation. Post-
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test measures revealed a significant drop in PetCO2 (evidence that the breathing procedure produced hyperventilation), a significant drop in finger temperature, and a significant increase in anxiety, findings which support the emotional arousing capability of hyperventilation.
BREATHING AND COGNITION

THE EFFECTS OF THOUGHTS ON BREATHING
Polygraphy and Lie Detection
The scientific or systematic study of the effects of thoughts on breathing is most vividly illustrated in the polygraphic lie-detector test (Ekman, 1985; Lykken, 1984). One of the channels routinely monitored in polygraphic recordings of physiological functions is ventilation (Podlesny & Raskin, 1980). Increases in respiratory frequency, respiratory depth, or changes in mode of breathing from diaphragmatic to thoracic, along with several other correlated changes in physiological variables (e.g., electrodermal response and blood pressure) in response to the presentation of salient information are interpreted as evidence that the subject may have knowledge related to the salient information and may be trying to conceal it. Although lie-detector tests are far from foolproof (Ginton, Daie, Elaad, & Ben-Shakhar, 1982), they do indicate the relative sensitivity of breathing to emotion-eliciting thoughts.
The Think Test
Although polygraphic monitoring of breathing for the purpose of detecting lies or concealment of knowledge has found broad application in criminal investigations, the effects of emotion-eliciting thoughts on breathing have recently received attention in the diagnosis of emotionally based cardiac complaints and related psychosomatic disorders (Freeman, Conway, & Nixon, 1986; Nixon & Freeman, 1987a, 1987b; Nixon, Freeman, & King, 1987). The think test, which employs a modification of Hardonk and Beumers (1979)
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hyperventilation-provocation test, requires constant capnographic monitoring of PetCO2. Following a brief period of quiet relaxation during which baseline PetCO2 is established, patients are required to hyperventilate for approximately 3 minutes. After 3 or 4 minutes during recovery following the forced voluntary hyperventilation, patients are instructed to close their eyes and think about (i.e., imagine) the details of the episode in which their cardiac symptoms were first experienced. If during this think test period, PetCO2 drops 10 mmHg or more (testing at sea level atmospheric pressure), hyperventilation is positively indicated. Although the think test has been studied primarily with patients suffering from ischemic heart disease, hypertension, cardiac arrhythmia, chest pain, and blackouts, it may well prove to be a useful adjunctive procedure for the purpose of exploring the salience of life experiences in panic disorder, related hyperventilatory complaints, and psychological traumas related to general anxiety.
THE EXPECTATION OF NOXIOUS EVENTS AND BREATHING
The foregoing discussion of the effects of fear and frustration on breathing was limited to a behavioral analysis. If a cognitive analysis were applied to these same data, the concept of expectancy would be invoked. Although cognitive psychology is sometimes loosely defined as the flow of information through the mind of the information processor (e.g., Broadbent, 1963; Neisser, 1967), the sine qua non of cognitive theories that submits best to experimental research is the concept of expectancy. In the words of the foremost cryptophenomenologist, Edward C. Tolman (1959):
I would also assert that thinking, as we know it in human beings, is in essence no more than an activated interplay among expectancies resulting from such previously acquired readinesses which result in new expectancies and resultant new means-end readiness. (pp. 113-114)
Throughout his lengthy career in experimental psychology, Tolman (1932, 1938, 1948, 1959) emphasized the fundamental significance of the autochthonous construct of expectancy in the psychological lives of humans.
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Expectancy and Panic Attacks
On the basis of a dyspnea/suffocation fear interpretation of panic disorder, if the symptoms of hypocapnea or a stress-induced increase in total respiratory resistance persist to the point where the intensity of dyspnea is sensed as out of control and life threatening, dyspnea/suffocation fear and other sensations (e.g., tachycardia and dizziness) will be experienced, the occurrence of which defines the classic panic attack. Subsequent attacks (anticipatory attacks) can occur as conditioned responses if events (including thoughts and their antecedents) evoke an anticipatory response (including fear or anxiety) that signals the occurrence of an attack much like that previously experienced; the greater the similarity, the greater the intensity of the anticipatory attack. Attempts to determine the causal agents of panic attacks have led to a rash of studies, all of which report some partial success in provoking panic attacks among patients with a history of panic disorder. These so-called panicogenic agents include lactate infusions (for reviews, see Ley, 1988a; Margraf, Ehlers, & Roth, 1986; Shear, 1986), bicarbonate (Grosz & Farmer, 1972), yohimbine (Charney, Heninger, & Brier, 1984), caffeine (Charney, Heninger, & Jatlow, 1985), 5% CO2 in air (Gorman et al., 1984; Woods, Charney, Goodman, & Heninger, 1988), and a placebo injection (saline solutions) or anticipation of an injection (Goetz et al., 1993). A perusal of this considerable body of research leads to one clear and irrefutable conclusion: If panic patients expect that an agent (animal, vegetable, or mineral) might produce a panic attack, chances are it will.
Expectancy Is Not Enough
Although the search for causal chemical agents provides indirect support for a psychological agent, the concept of expectancy is not a sufficient explanation. As in the case of placebo effects, the observation of the effect cannot be an explanation for the effect. What then, accounts for the moderate correlation between expectancy of a panic attack, the phase following the threat of an attack, and the occurrence of an attack? The explanation for this expectancy effect in the production of panic attacks was hinted at by a study that provided evidence of the
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expectancy effect independent of any chemical agents. Margraf, Ehlers, and Roth (1987) reported a single-case study in which a panic-disorder patient experienced a panic attack following false feedback, which indicated that the subjects heart rate suddenly increased. The clue provided by this study lies in the emotional effect that information of a sudden increase in heart rate might induce in a person who suffers from panic attacks. If this information induces sufficient fear, then an increase in ventilation should be expected. And if the subject is immobilized by the equipment required for physiological monitoring, thus restricting increases in metabolic production of CO2, then the increase in ventilation would be hyperventilatory (see Ley, 1988b, 1988c). If this is the case, then the expectancy effect in the production of panic attacks could be explained parsimoniously by dyspnea/suffocation fear induced by hyperventilation (Ley, 1987a, 1989, 1992; Wolpe & Rowan, 1988) or stress-induced respiratory resistance or both.
An Unwitting Portrait of the Occurrence of Hyperventilation in a Panic Attack
Evidence that demonstrates the occurrence of hyperventilation in panic attacks can be found in a single-case study of a panic attack reported by Sanderson, Rapee, and Barlow (1988) based on a subject selected from an earlier experiment conducted by Sanderson (1987). In this single-case study (one of three such cases selected from the Sanderson study), a panic-disorder patient was required to breathe air through a gas inhalation mask for 5 minutes prior to a scheduled 20minute period during which the patient was led to believe that she would be breathing a gas mixture containing a 5.5% CO2. After 6 minutes of inhalation of room air (i.e., air that did not contain 5.5% CO2 but which the patient believed held the threat of producing a panic attack), the patient reported the experience of a panic attack: Respiration rate increased, end-tidal PCO2 dropped from 26 to 17 mmHg (indisputable physiological evidence that the patient was not breathing a 5.5% CO2 gas mixture), electrodermal response increased sharply, heart rate increased sharply (86 to 105 b/min), and self-rated anxiety increased sharply. The changes reported here provide a classic
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portrait of hyperventilation in the panic attack (see Ley, 1992, for a detailed description). This single-case study (one of three such cases) by Sanderson, Rapee, and Barlow (1988) is a very important piece of evidence in support of a dyspnea/suffocation theory of primary panic attacks. The serendipitous discovery of a significant drop in PCO2 during the minute in which panic was reported, together with the sharp increase in heart rate, increase in respiration rate, sharp increase in electrodermal response, and increase in anxiety, illustrate the central role of hyperventilation in at least one type of panic attack (see Ley, 1992).
THE EFFECTS OF BREATHING ON THOUGHTS
Although both underbreathing (hypoventilation) and overbreathing (hyperventilation) have dramatic effects on consciousness and cognitive processes, the effects of hyperventilation (i.e., hypocapnia) are of greater psychological interest because they can be induced through voluntary overbreathing or reflexive overbreathing from emotional arousal and sympathetic nervous-system excitation. On the other hand, the effects of hypoventilation (hypercapnia) cannot be induced voluntarily, except for relatively brief periods, because the build up of excessive arterial CO2 will stimulate the respiratory centers and thereby evoke involuntary control of breathing (Comroe, 1974). Thus, the effects of breathing on cognition discussed here are those that result from hyperventilation, a consequence of which is a drop in cerebral blood flow of about 43% from a base of 37 mmHg (pH = 7.412) to a nadir of 19 mmHg (pH = 7.596) (Wollman et al., 1968). Other active researchers in the field of panic disorder (viz., Papp, Coplan, Klein, Woods, Shear, Barlow, & Gorman, 1998) have currently acknowledged the salience of hyperventilation in the diagnosis and treatment prognosis of panic (Type I/classic attack). In the abstract of a recent paper, Papp et al. (1998) state that
One of the most consistently reported respiratory abnormalities in patients with panic disorder is the tendency to hyperventilate. If hyperventilation induced low end-tidal CO2 level is a state specific phenomenon, clinical remission, regardless of treatment modality, should normalize ETCO2. . . . ETCO2is a convenient respiratory parameter
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that can be easily utilized to predict and monitor treatment response in at least a subgroup of patients with panic disorder. Dyspnea/Suffocation Fear Theory of Panic Disorder
A dyspnea/suffocation theory of panic disorder (Ley, 1989, 1992, 1996, 1997) maintains that if under conditions of prolonged stress an event occurs (e.g., hyperventilation or increased respiratory resistance or tetany of diaphragm) that produces a sudden unexpected sense of strained breathing with uncontrollable dyspnea (e.g., dyspnea that accompanies loss of voluntary control or self-regulation of breathing, as when ones wind is knocked out, as opposed to voluntary breath holding), probability favors the occasion of a primary (Type I) panic attack. Secondary anticipatory panic attacks (Type II) are assumed to be conditioned responses (fear elicited by a contextual environment that increases the expectancy of strained breathing with uncontrollable dyspnea/suffocation) acquired through Pavlovian conditioning in which the UCS consists of events that give rise to the UCR, that is, a sense of strained breathing with uncontrollable dyspnea. (For a detailed discussion of types of panic attacks, see Ley, 1992.) According to this revised theory (Ley, 1989), the fear experienced during a primary panic attack is the consequence of dyspnea (a harbinger of suffocation) in a perceptual context in which sufferers believe they have no control over the dyspnea, that is, dyspneic fear is the emotional component of the UCR. As Aiken, Zeally, and Rosenthal (1970) have pointed out, Dyspnea may be felt as endangering to life to a greater extent than almost any other symptom: to the patient, the experience of dyspnea is regarded as something which, if it worsens to asphyxia, must be fatal (p. 256). Stimuli that provide sufficient predictive probability of the onset of uncontrollable hypocapnia or other dyspneic fear-inducing conditions such as extreme hypercapnia are CSs; and fear, independent of dyspnea, is the CR. Findings that support the central role of dyspnea in panic fear have been reported by Rachman, Levitt, and Lopatka (1987): The prominence of shortness of breath (dyspnea) is consistent with the emphasis placed on the role of hyperventilation in the onset of panics (e.g., Clark, 1986; Ley, 1985a). (p. 418)
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HYPERVENTILATION AND COGNITIVE DEFICIT
In the aforementioned revision of his hyperventilation theory of panic, Ley (1989) discussed the connection between cognitive deficits resulting from hyperventilation and dyspneic fear and catastrophic cognitions associated with panic attacks. The broad-ranging effects of hypocapnia on performance (see Wyke, 1963) have been reported by Balke and Lillehei (1956); Hall (1952); Hinshaw, Rushmer, and Boothby (1943); and Rushmer and Bond (1944). Such deficits have been demonstrated in word-association tests (Gellhorn & Kraines, 1937); tests of intellectual function (Gellhorn & Joslyn, 1937); motor coordination tests (Hinshaw, Rushmer, & Boothby, 1943); balancing and peg-board tests (Rushmer, Boothby, & Hinshaw, 1941); and tests of manual dexterity, choice reaction time, and multiplication time (Rahn et al., 1946).
Catastrophic Cognitions
The broad effects of hyperventilation on mental function may also be a causal factor underlying catastrophic cognitions associated with panic attacks. Because self-reported catastrophic cognitions are essentially expressions of thoughts that center on a strong expectation of imminent suffocation (dyspneic fear), it seems reasonable to suppose that if a sense of voluntary control or a strong expectation of resumption of self-regulation of breathing is maintained during a severe episode of dyspnea, neither panic fear nor catastrophic cognitions should occur. This would account for (a) false-negative hyperventilation-provocation tests, (b) panic attacks without fear (Beitman, Basha, Flaker, DeRosear, Mukerji, & Lanberti, 1987), (c) the symptoms of coronary artery disease (angina pectoris, rapid heart rate, and dyspnea) experienced by healthy patients who do not report concomitant fear, and (d) breath holding.
Hallucinations
Cognitive deficits that result from hyperventilation are not limited to mental abilities and perceptual motor skills. Allen and Agus (1968) reported the induction of hallucinations by means of voluntary hyper-
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ventilation, and Belcher (1988) reported the case of an institutionalized psychotic patient whose hallucinations were promptly terminated by forced exercise, a treatment which increases metabolic production of CO2, which in turn reduces hypocapnia (see Ley, 1988a, 1989).
TEST ANXIETY AND HYPERVENTILATION
Test anxiety, or evaluation anxiety, is the most pervasive emotional complaint among school-age children (Barios, Hartmann, & Shigentoni, 1981; Miller, 1983). Eysenck and Rachman (1965) estimated that 20% of grade school and high school pupils suffer performance debilitation as a consequence of anxiety experienced during testing, whereas Suinn (1969) estimates that the performance of an even larger percentage of college students (25%) is affected by test anxiety. If ventilation is increased during periods of test anxiety, then part of the decrement in performance observed among test-anxious students may be a consequence of the cognitive deficit that results from cerebral hypoxia induced by hyperventilation. Ley and Yelich (1998) reported an interaction between the effects of induced stress and test anxiety on end-tidal CO2 (ETCO2). In a study of 32 7th-, 8th-, and 9th-grade students identified as either high or low test anxious (scores selected from 15% of the high end and 15% of the low end of a distribution of 124 test-anxiety scores), baseline measures of ETCO2 were taken immediately prior to high stress-inducing instructions for half the subjects and low stress-inducing instructions for the other half followed by an arithmetical computation test for all subjects. ETCO2, monitored throughout the experiment, showed a decrease from baseline to test period for the high anxious but not the low anxious students under the high stress condition. Another notable finding of this study was a positive relationship, for students at the extremes of the anxiety test distribution, between scores on Haskins (1972) revision of the Suinn Test Anxiety Behavior Scale (50 statements that describe situations presumed to elicit anxiety in American junior high school students) and a slightly modified version of the Nijmegen Hyperventilation Syndrome Questionnaire (15 physiological complaints reported by adult residents of the Netherlands who suffered the effects of chronic or acute hyperventilation;
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van Doorn, Colla, & Folgering, 1982). Beyond this correlational fact is the observation that self-reports of symptoms of hyperventilation by the high anxiety group are accompanied by corresponding lower levels of ETCO2 during conditions of testing under high stress conditions. If this is indicative of a propensity to hyperventilate as a trait that requires stressful conditions for its expression as a negative emotional state, then hyperventilation complaints may, to some extent, be state dependent and thus contingent on the context in which hyperventilation occurs.
CONCLUDING REMARKS
Breathing behavior can be modified. This fact underscores the significance of respiratory psychophysiology, the study of the complex interactions between breathing behavior, physiology, and the concepts of emotion and cognition. A review of some of the research that falls within this domain illustrates how Pavlovian conditioning might provide a unifying paradigm. While the research reviewed here confirms the common observation that changes in breathing follow changes in emotion and cognition, it also points to the less commonly recognized fact that changes in breathing can lead to changes in emotion and cognition. The implications of this bidirectional relationship are especially important for the purposes of diagnosis and treatment in clinical practice. Regarding diagnosis, if breathing affects emotions and cognitions, then the routine diagnosis of psychological complaints should include a search for signs of dysfunctional breathing, especially under stress. Regarding treatment, if changes in emotion or cognition induced by changes in breathing ameliorate complaints, then new strategies of psychological intervention can be developed so that breathing-induced changes counteract the complaints. Programs of remedial breathing (breathing retraining) in the treatment of chronic lung disease (asthma, bronchitis, emphysema), panic disorders, anxiety disorders, and breathing-related psychophysiological complaints might benefit from an exploration of innovative applications of Pavlovian and operant conditioning techniques; programs of research in psychophysiology might benefit from the inclusion of res-
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piration as both a dependent and independent variable. The study of respiratory psychophysiology might lead to findings that bridge the gap between psychology and physiology.
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Ronald Ley, Ph.D., is a professor of psychology and statistics at the University of Albany, SUNY. He has authored or coauthored more than 100 articles and books. His current research in the field of respiratory psychophysiology is focused on panic disorder and Pavlovian conditioning of hyperventilation and its effects on emotion, cognition, and somatic disorders. In addition to numerous grants and fellowships, he has been the recipient of the Plenum Press Best Paper Prize and the Psychological Association of Northeastern New York Distinguished Psychologist Award.

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Breathing

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Behavior Modification http://bmo.sagepub.

>> Version of Record - Jul 1, 1999 What is This?

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

Ley / MODIFICATION OF BREATHING BEHAVIOR MODIFICATION / July 1999

The Modification of Breathing Behavior

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BEHAVIOR MODIFICATION / July 1999

CONDITIONED BREATHING AND EMOTIONS

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Ley / MODIFICATION OF BREATHING

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

BEHAVIOR MODIFICATION / July 1999

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

Ley / MODIFICATION OF BREATHING

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

BEHAVIOR MODIFICATION / July 1999

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

Ley / MODIFICATION OF BREATHING

PAVLOVIAN CONDITIONING AND VENTILATORY RESPONSES

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

BEHAVIOR MODIFICATION / July 1999

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

Ley / MODIFICATION OF BREATHING

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

BEHAVIOR MODIFICATION / July 1999

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

Ley / MODIFICATION OF BREATHING

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

BEHAVIOR MODIFICATION / July 1999

Conditioned Respiratory Resistance

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Ley / MODIFICATION OF BREATHING

OPERANT CONTROL OF BREATHING

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BEHAVIOR MODIFICATION / July 1999

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Ley / MODIFICATION OF BREATHING

FRUSTRATION, STRESS, AND HYPERVENTILATION

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BEHAVIOR MODIFICATION / July 1999

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Ley / MODIFICATION OF BREATHING

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

BEHAVIOR MODIFICATION / July 1999

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

Ley / MODIFICATION OF BREATHING

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

BEHAVIOR MODIFICATION / July 1999

BREATHING AND EMOTIONS

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

Ley / MODIFICATION OF BREATHING

Downloaded from bmo.sagepub.com at University of Bucharest on January 14, 2013

BEHAVIOR MODIFICATION / July 1999

BREATHING AND COGNITION

Polygraphy and Lie Detection

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Ley / MODIFICATION OF BREATHING

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BEHAVIOR MODIFICATION / July 1999

Expectancy and Panic Attacks

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Ley / MODIFICATION OF BREATHING

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