Learning and unlearning fear: A clinical and evolutionary perspective

Many fears, phobias and rituals seem to arise from prepared phylogenetic mechanisms which favor old over new evolutionary dangers and affect the rules of aversive learning which govern the acquisition of fear. Recent developments in several forms of aversive learning (sensitization, conditioning, extinction, observational learning) can improve them as paradigms of the acquisition, spread and maintenance of normal and clinical fears. The most reliable treatment for phobias and rituals is exposure, whose effects closely parallel the habituation of normal defensive responses and the extinction of conditioned fear and avoidance in animals. Habituation during exposure is usually slow and step by step, and generalizes little, but once attained tends to endure. Conditioned fear extinction and fear habituation have similar courses and may depend on similar neural processes. To be reduced, avoidance has to be prevented or the safety intervals that it heralds must be given up. Some phobias may result less from enhanced acquisition than from insufficient exposure to attain habituation. Finally, the review discusses the limits of habituation and the instability of fear extinction in relation to the long-term efficacy of exposure therapy.

[1]  R. Willmuth,et al.  RECOVERY FROM TRAUMATIC EXPERIENCE IN RATS: SPECIFIC "TREATMENT" VS. PASSAGE OF TIME. , 1964, Behaviour research and therapy.

[2]  M. D. Shalter Effect of spatial context on the mobbing reaction of pied flycatchers to a predator model , 1978, Animal Behaviour.

[3]  J. Lanzetta,et al.  Facial expressions of emotion as conditioned stimuli for human autonomic responses. , 1980, Journal of personality and social psychology.

[4]  L. Petrinovich,et al.  Habituation, sensitization, and behavior , 1984 .

[5]  E. Foa,et al.  Preparedness and resistance to extinction to fear-relevant stimuli: a failure to replicate. , 1986, Behaviour research and therapy.

[6]  G. Gallup,et al.  Habituation and tonic immobility in domestic chickens. , 1976, Journal of comparative and physiological psychology.

[7]  M. Rohrbaugh,et al.  Paradoxical enhancement of conditioned suppression. , 1972, Behaviour research and therapy.

[8]  D. Levis,et al.  Symptom maintenance: an infrahuman analysis and extension of the conservation of anxiety principle. , 1979, Journal of abnormal psychology.

[9]  S. Mineka,et al.  Comparison of various flooding procedures in reducing fear and in extinguishing jump-up avoidance responding , 1982 .

[10]  M. Kozak,et al.  Emotional processing of fear: exposure to corrective information. , 1986, Psychological bulletin.

[11]  D. Riccio,et al.  Memory retrieval deficits based upon altered contextual cues: a paradox. , 1984, Psychological bulletin.

[12]  K. Hugdahl,et al.  Acquisition of agoraphobia, mode of onset and anxiety response patterns. , 1983, Behaviour research and therapy.

[13]  Michael Davis CHAPTER 8 – Intrinsic and Extrinsic Mechanisms of Habituation and Sensitization: Implications for the Design and Analysis of Experiments , 1984 .

[14]  D. Woods Paradoxical Enhancement of Learned Anxiety Responses , 1974, Psychological reports.

[15]  I. Maltzman,et al.  Stimulus significance and bilateral SCRs to potentially phobic pictures. , 1984, Journal of abnormal psychology.

[16]  A. Tobeña,et al.  Handling-habituation prevents the effects of diazepam and alprazolam on brain serotonin levels in rats , 1990, Behavioural Brain Research.

[17]  G. Horn Habituation and Memory , 1971 .

[18]  P. Emmelkamp,et al.  Behavioral treatment of obsessive-compulsives: inpatient vs outpatient. , 1988, Behaviour research and therapy.

[19]  S. Maier,et al.  Librium prevents the analgesia and shuttlebox escape deficit typically observed following inescapable shock , 1984, Pharmacology Biochemistry and Behavior.

[20]  K. Melvin Vicious circle behavior. , 1971 .

[21]  S. Mineka Effects of flooding an irrelevant response on the extinction of avoidance responses. , 1976 .

[22]  M. Akiyama Relation between Extinction Techniques and Extinction of Avoidance Response in Albino Rats , 1969 .

[23]  P. Lang,et al.  Preparedness and phobia: effects of stimulus content on human visceral conditioning. , 1986, Journal of abnormal psychology.

[24]  R. Solomon,et al.  Traumatic avoidance learning: the outcomes of several extinction procedures with dogs. , 1953, Journal of abnormal psychology.

[25]  A. Bandura Principles of behavior modification , 1969 .

[26]  J. Weiss,et al.  Behavioral depression produced by an uncontrollable stressor: Relationship to norepinephrine, dopamine, and serotonin levels in various regions of rat brain , 1981, Brain Research Reviews.

[27]  M. Baum Flooding (response prevention) in rats: the effects of immediate vs. delayed flooding and of changed illumination conditions during flooding. , 1972, Canadian journal of psychology.

[28]  R. Rescorla Pavlovian conditioning. It's not what you think it is. , 1988 .

[29]  G. Fava,et al.  Prodromal symptoms in panic disorder with agoraphobia. , 1988, The American journal of psychiatry.

[30]  R. Moos,et al.  Health and the social environment , 1974 .

[31]  M. Baum,et al.  Extinction of well-established avoidance responses through response prevention (flooding). , 1971, Behaviour research and therapy.

[32]  D. Walton,et al.  THE APPLICATION OF LEARNING PRINCIPLES TO THE TREATMENT OF OBSESSIVE-COMPULSIVE STATES IN THE ACUTE AND CHRONIC PHASES OF ILLNESS. , 1963, Behaviour research and therapy.

[33]  R. Solomon The opponent-process theory of acquired motivation: the costs of pleasure and the benefits of pain. , 1980, The American psychologist.

[34]  L. Rosenblum,et al.  Imipramine and alprazolam treatment of lactate-induced acute endogenous distress in nonhuman primates. , 1989, The American journal of psychiatry.

[35]  K. Melvin,et al.  Fear responses of Bobwhite Quail (Colinus virginianus) to a model and a live Red-tailed Hawk (Buteo jamaicensis) , 1964, Psychologische Forschung.

[36]  Morrie Baum,et al.  Extinction of an avoidance response following response prevention: Some parametric investigations. , 1969 .

[37]  P. L. Broadhurst The Maudsley Reactive and Nonreactive strains of rats: A survey , 1975, Behavior genetics.

[38]  M. Spetch,et al.  Backward conditioning: a reevaluation of the empirical evidence. , 1981, Psychological bulletin.

[39]  F. Samelson J. B. Watson's Little Albert, Cyril Burt's twins, and the need for a critical science. , 1980 .

[40]  H. Eysenck The learning theory model of neurosis--a new approach. , 1976, Behaviour research and therapy.

[41]  Edward L. Thorndike,et al.  The psychology of wants, interests, and attitudes , 1936 .

[42]  U. Ernst,et al.  Cultural Transmission of Enemy Recognition: One Function of Mobbing , 1978, Science.

[43]  M. McDaniel,et al.  The time course of learned helplessness, inactivity, and nociceptive deficits in rats , 1979 .

[44]  R. F. Thompson,et al.  Habituation: a model phenomenon for the study of neuronal substrates of behavior. , 1966, Psychological review.

[45]  O. Mowrer On the dual nature of learning—a re-interpretation of "conditioning" and "problem-solving." , 1947 .

[46]  Michael Davis Neural Systems Involved in Fear‐Potentiated Startle , 1989, Annals of the New York Academy of Sciences.

[47]  E. Murray,et al.  The origins of fear of snakes. , 1979, Behaviour research and therapy.

[48]  J. Pratt,et al.  Chronic handling modifies the anxiolytic effect of diazepam in the elevated plus-maze. , 1990, European journal of pharmacology.

[49]  P. Lelliott,et al.  Onset of panic disorder with agoraphobia. Toward an integrated model. , 1989, Archives of general psychiatry.

[50]  A. Broadhurst,et al.  Theoretical and experimental bases of the behaviour therapies , 1976 .

[51]  R. Solomon,et al.  An opponent-process theory of motivation. I. Temporal dynamics of affect. , 1974, Psychological review.

[52]  S. Mineka,et al.  Unpredictable and uncontrollable events: a new perspective on experimental neurosis. , 1978, Journal of abnormal psychology.

[53]  S. Rachman,et al.  Panic, fear reduction and habituation. , 1988, Behaviour research and therapy.

[54]  S. Mineka,et al.  The role of cognitive biases in the origins and maintenance of fear and anxiety disorders , 1989 .

[55]  S. Morley The incubation of avoidance behaviour: Strain differences in susceptibility , 1977 .

[56]  R. Hendersen Forgetting of conditioned fear inhibition , 1978 .

[57]  D. Charney,et al.  Neurobiological mechanisms in human anxiety evidence supporting central noradrenergic hyperactivity , 1983, Neuropharmacology.

[58]  R. Rescorla,et al.  Associations in second-order conditioning and sensory preconditioning. , 1972, Journal of comparative and physiological psychology.

[59]  D. Delprato,et al.  Counterconditioning and exposure-only in the treatment of specific (conditioned suppression) and generalized fear in rats. , 1973, Behaviour research and therapy.

[60]  G. M. Harrington,et al.  Maudsley reactive and non-reactive rat strains: Differential performance in a conflict task , 1986, Physiology & Behavior.

[61]  N. Miller Learning of visceral and glandular responses. , 1969, Science.

[62]  S. Mineka,et al.  Observational conditioning of fear to fear-relevant versus fear-irrelevant stimuli in rhesus monkeys. , 1989, Journal of abnormal psychology.

[63]  D. Delprato An animal analogue to systematic desensitization and elimination of avoidance. , 1973, Behaviour research and therapy.

[64]  S. Mineka,et al.  Controllability and predictability in acquired motivation. , 1985, Annual review of psychology.

[65]  L. Rosenblum,et al.  A nonhuman primate model of panic disorder , 1988, Psychiatry Research.

[66]  W. Rees,et al.  Lactate-induced anxiety: therapeutic application. , 1971, The British journal of psychiatry : the journal of mental science.

[67]  S. Mineka The frightful complexity of the origins of fears , 1985 .

[68]  M. D. Shalter Lack of spatial generalization in habituation tests of fowl. , 1975 .

[69]  R. Hinde Factors governing the changes in strength of a partially inborn response, as shown by the mobbing behaviour of the chaffinch (Fringilla coelebs) III. The interaction of short-term and long-term incremental and decremental effects , 1961, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[70]  M. Bouton,et al.  Context and ambiguity in the extinction of emotional learning: implications for exposure therapy. , 1988, Behaviour research and therapy.

[71]  K. Hugdahl,et al.  Acquisition of phobias and anxiety response patterns in clinical patients. , 1981, Behaviour research and therapy.

[72]  R. B. Clark Habituation of the polychaete Nereis to sudden stimuli. 1. General properties of the habituation process , 1960 .

[73]  A. Ohman,et al.  The premise of equipotentiality in human classical conditioning: conditioned electrodermal responses to potentially phobic stimuli. , 1976, Journal of experimental psychology. General.

[74]  R. Hendersen,et al.  Acquisition and retention of control of instrumental behavior by a cue-signaling airblast: How specific are conditioned anticipations? , 1980 .

[75]  R. Bolles Species-specific defense reactions and avoidance learning. , 1970 .

[76]  A. Tobeña,et al.  What do the neurosciences tell us about anxiety disorders? A comment , 1986, Psychological Medicine.

[77]  Mark E. Bouton,et al.  Sources of relapse after extinction in Pavlovian and instrumental learning , 1991 .

[78]  K Kuch,et al.  Post-Traumatic Stress Disorder after Car Accidents , 1985, Canadian journal of psychiatry. Revue canadienne de psychiatrie.

[79]  R. Katzev,et al.  Effects of exteroceptive feedback stimuli on extinguishing avoidance responses in Fischer 344 rats. , 1971, Journal of comparative and physiological psychology.

[80]  J. Wolpe,et al.  Panic disorder: a product of classical conditioning. , 1988, Behaviour research and therapy.

[81]  T. Carew,et al.  Behavioral dissociation of dishabituation, sensitization, and inhibition in Aplysia. , 1988, Science.

[82]  D. Page Theory of learning , 1993 .

[83]  R. McNally,et al.  The etiology and maintenance of severe animal phobias. , 1985, Behaviour research and therapy.

[84]  E R Kandel,et al.  From metapsychology to molecular biology: explorations into the nature of anxiety. , 1983, The American journal of psychiatry.

[85]  G. Bock,et al.  Antidepressants and receptor function. , 1986, Ciba Foundation symposium.

[86]  A. Ohman,et al.  Cardiovascular and electrodermal responses conditioned to fear-relevant stimuli. , 1979, Psychophysiology.

[87]  S. Mineka,et al.  Dissociative effects of flooding on a multivariate assessment of fear reduction and on jump-up avoidance extinction , 1981 .

[88]  L. Janda,et al.  An exploratory investigation of the origin and maintenance of phobias. , 1977, Behaviour research and therapy.

[89]  M. Seligman On the generality of the laws of learning , 1970 .

[90]  K. Hugdahl,et al.  Electrodermal conditioning to potentially phobic stimuli in male and female subjects , 1976, Biological Psychology.

[91]  R. Katzev,et al.  Factors involved in the rapid elimination of avoidance behavior. , 1972, Behaviour research and therapy.

[92]  P. Soubrié Reconciling the role of central serotonin neurons in human and animal behavior , 1986, Behavioral and Brain Sciences.

[93]  M. Baum,et al.  Extinction of avoidance responding in rats: the noise-intensity parameter in noise-facilitation of flooding , 1985 .

[94]  S. File The contribution of behavioural studies to the neuropharmacology of anxiety , 1987, Neuropharmacology.

[95]  M. Baum On the Validity of the Animal Model for Exposure Therapy (Flooding) , 1988, Behavioural Psychotherapy.

[96]  J. Watson,et al.  Conditioned emotional reactions , 1920 .

[97]  E. Kandel,et al.  A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. , 1983, Science.

[98]  S. Siegel,et al.  Morphine tolerance acquisition as an associative process. , 1977, Journal of experimental psychology. Animal behavior processes.

[99]  J. P. Watson,et al.  Relevant and irrelevant fear in flooding: A crossover study of phobic patients. , 1971 .

[100]  R. Solomon,et al.  Traumatic avoidance learning: the principles of anxiety conservation and partial irreversibility. , 1954, Psychological review.

[101]  M. Davis,et al.  Effects of interstimulus interval length and variability on startle-response habituation in the rat. , 1970, Journal of comparative and physiological psychology.

[102]  J M Gorman,et al.  Lactate provocation of panic attacks. I. Clinical and behavioral findings. , 1984, Archives of general psychiatry.

[103]  J. Gray,et al.  The psychology of fear and stress , 1971 .

[104]  C. Osgood Method and theory in experimental psychology , 1953 .

[105]  J. Harsh,et al.  Choosing between predictable and unpredictable shock conditions: Data and theory. , 1979 .

[106]  S. Rachman,et al.  Agoraphobia--a safety-signal perspective. , 1984, Behaviour research and therapy.

[107]  M. Baum,et al.  Increased efficacy of flooding (response prevention) in rats through positive intracranial stimulation. , 1971, Journal of comparative and physiological psychology.

[108]  A. Black,et al.  Conditioned suppression as a monitor of fear of the CS in the course of avoidance training. , 1963, Journal of comparative and physiological psychology.

[109]  J. Schull A Conditioned Opponent Theory of Pavlovian Conditioning and Habituation1 , 1979 .

[110]  R. Katzev Extinguishing avoidance responses as a function of delayed warning signal termination. , 1967, Journal of experimental psychology.

[111]  I. Marks,et al.  Physiological habituation to continuous phobic stimulation. , 1972, Behaviour research and therapy.

[112]  M. Rohrbaugh,et al.  Paradoxical enhancement of learned fear. , 1970, Journal of abnormal psychology.

[113]  T. Carew CHAPTER 6 – An Introduction to Cellular Approaches Used in the Analysis of Habituation and Sensitization in Aplysia , 1984 .

[114]  J. Wolpe,et al.  Psychotherapy by reciprocal inhibition , 1958, Conditional reflex.

[115]  I. Martin,et al.  Differences in benzodiazepine receptor binding in Maudsley reactive and Maudsley non-reactive rats. , 1978, European journal of pharmacology.

[116]  I. Marks Cure and care of neurosis , 1979, Psychological Medicine.

[117]  S. Mineka,et al.  Second-order conditioning and overshadowing in the observational conditioning of fear in monkeys. , 1987, Behaviour research and therapy.

[118]  M. Baum Extinction of avoidance in rats: the effects of chlorpromazine and methylphenidate administered in conjunction with flooding response (prevention). , 1973, Behaviour research and therapy.

[119]  R. McNally,et al.  The preparedness theory of phobias: the effects of initial fear level on safety-signal conditioning to fear-relevant stimuli. , 1984, Psychophysiology.

[120]  Richard D. Alexander,et al.  The search for a general theory of behavior , 1975 .

[121]  S. Mineka,et al.  Observational conditioning of snake fear in rhesus monkeys. , 1984, Journal of abnormal psychology.

[122]  R. Ross POSITIVE AND NEGATIVE PARTIAL-REINFORCEMENT EXTINCTION EFFECTS CARRIED THROUGH CONTINUOUS REINFORCEMENT, CHANGED MOTIVATION, AND CHANGED RESPONSE. , 1964, Journal of experimental psychology.

[123]  J. H. Reynierse,et al.  Effects of temporal placement of response prevention on extinction of avoidance in rats. , 1973, Behaviour research and therapy.

[124]  E. Kandel,et al.  Prospectuses of Neurobiology. (Book Reviews: From Neuron to Brain. A Cellular Approach to the Function of the Nervous System; The Cellular Basis of Behavior. An Introduction to Behavioral Neurobiology) , 1976 .

[125]  K. Hugdahl,et al.  Biological vs experiential factors in phobic conditioning. , 1981, Behaviour research and therapy.

[126]  R. McNally,et al.  Preparedness and phobias: a review. , 1987, Psychological bulletin.

[127]  N. Mackintosh,et al.  Neurobiology, psychology and habituation. , 1987, Behaviour research and therapy.

[128]  D. Alkon Learning in a marine snail. , 1983, Scientific American.

[129]  S. Mineka,et al.  Observational conditioning of snake fear in unrelated rhesus monkeys. , 1985, Journal of abnormal psychology.

[130]  A. Öhman,et al.  An Evolutionary Perspective on Human Social Behavior , 1984 .

[131]  N. Miller,et al.  Personality and Psychotherapy , 1951 .

[132]  M. Baum,et al.  Irrelevant stress vs response prevention (flooding) interpolated between avoidance acquisition and extinction in rats. , 1974, Journal of psychiatric research.

[133]  D. Delprato Postresponse exposure to warning signal in avoidance extinction , 1974 .

[134]  D. Delprato Exposure to the aversive stimulus in an animal analogue to systematic desensitization. , 1973, Behaviour research and therapy.

[135]  H. Spiegel,et al.  War stress and neurotic illness. , 1947 .

[136]  E. Griez,et al.  Treatment of phobophobia by exposure to CO2-induced anxiety symptoms. , 1983, The Journal of nervous and mental disease.

[137]  L. Kamin,et al.  The retention of an incompletely learned avoidance response. , 1957, Journal of comparative and physiological psychology.

[138]  R. Katzev,et al.  Effect of exposure to conditioned stimulus and control of its termination in the extinction of avoidance behavior. , 1974 .

[139]  I. Marks Fears and phobias , 1989, PSICOLOGIA.

[140]  S. Mineka,et al.  Determinants of fear over the course of avoidance learning , 1977 .

[141]  M. Baum,et al.  Facilitated extinction of an avoidance response through shortening of the inter-trial interval , 1968 .

[142]  M. D. Shaker CHAPTER 10 – Predator–Prey Behavior and Habituation , 1984 .

[143]  D. Charney,et al.  Noradrenergic function in panic anxiety. Effects of yohimbine in healthy subjects and patients with agoraphobia and panic disorder. , 1984, Archives of general psychiatry.

[144]  M. Fredrikson,et al.  Orienting and defensive reactions to phobic and conditioned fear stimuli in phobics and normals. , 1981, Psychophysiology.

[145]  V. Tuason,et al.  The relationship of panic disorder to agoraphobia. , 1984, Comprehensive psychiatry.

[146]  T. Uno,et al.  Observational facilitation of response prevention. , 1973, Behaviour research and therapy.

[147]  P. Lang The Cognitive Psychophysiology of Emotion , 2019, Anxiety and the Anxiety Disorders.

[148]  A. U. Moore,et al.  Animal hypnosis: a study in the induction of tonic immobility in chickens. , 1950, Journal of comparative and physiological psychology.

[149]  J. Bancroft,et al.  Electric aversion therapy of sexual deviations. , 1968, Proceedings of the Royal Society of Medicine.

[150]  L. Kamin,et al.  The conditioned emotional response as a function of intensity of the US. , 1961, Journal of comparative and physiological psychology.

[151]  S. Rachman,et al.  Fear And Courage , 1978 .

[152]  E. N. Sokolov,et al.  Perception and the Conditioned Reflex , 1965 .

[153]  R. Bolles,et al.  Does CS termination reinforce avoidance behavior? , 1966, Journal of comparative and physiological psychology.

[154]  G. Razran,et al.  The observable unconscious and the inferable conscious in current Soviet psychophysiology: interoceptive conditioning, semantic conditioning, and the orienting reflex. , 1961, Psychological review.

[155]  H. Eysenck Atavisms in psychopathological theory , 1979, Behavioral and Brain Sciences.

[156]  S. Mineka Animal Models of Anxiety-Based Disorders , 2019, Anxiety and the Anxiety Disorders.

[157]  S. Rachman,et al.  Does escape behaviour strengthen agoraphobic avoidance? A preliminary study. , 1984, Behaviour research and therapy.

[158]  I. Marks,et al.  Psychogenic urinary retention: Treatment by prolonged exposure , 1973 .

[159]  Lars-Göran Öst Acquisition of blood and injection phobia and anxiety response patterns in clinical patients. , 1991 .

[160]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[161]  I. Marks,et al.  Fears, phobias, and rituals : panic, anxiety, and their disorders , 1987 .

[162]  H. B. English,et al.  Three cases of the “conditioned fear response.” , 1929 .

[163]  K. Hugdahl,et al.  TOWARDS AN EXPERIMENTAL MODEL FOR SIMPLE PHOBIC REACTIONS. , 1977 .

[164]  C. Nemeroff,et al.  One stressful event blocks multiple actions of diazepam for up to at least a month , 1988, Brain Research.

[165]  A. Tobeña,et al.  The anxiolytic action of benzodiazepines is not present in handling-habituated rats , 1988, Pharmacology Biochemistry and Behavior.

[166]  A. Tobeña,et al.  Comparison of two flooding procedures in reducing avoidance and skin conductance responses in human volunteers , 1988 .

[167]  T. L. Boyd The effects of shock intensity on fear incubation (enhancement): a preliminary investigation of Eysenck's theory. , 1981, Behaviour research and therapy.

[168]  R. Rescorla,et al.  Reinstatement of fear to an extinguished conditioned stimulus. , 1975, Journal of experimental psychology. Animal behavior processes.

[169]  S. Mineka The role of fear in theories of avoidance learning, flooding, and extinction. , 1979 .

[170]  J. Maser,et al.  Psychopathology : experimental models , 1977 .

[171]  J. Kagan,et al.  Biological bases of childhood shyness. , 1988, Science.

[172]  Habituation of the deimatic response in the mantid (Stagmatoptera biocellata). , 1971 .

[173]  D. Munjack The onset of driving phobias. , 1984, Journal of behavior therapy and experimental psychiatry.