Lesions of periaqueductal gray dissociate-conditioned freezing from conditioned suppression behavior in rats.

It is commonly assumed that suppression of an ongoing behavior is an indirect measure of freezing behavior. We tested whether conditioned suppression and freezing are the same or distinct conditioned responses. Rats were trained to press a bar for food and then given fear-conditioning sessions in which a tone was paired with a foot shock (two pairings a day for 2 days). They then received either sham or electrolytic lesions of the periaqueductal gray (PAG). Post-training PAG lesions blocked freezing to the conditioned stimulus (CS), but had no effect on the suppression of operant behavior to the same CS. Thus, conditioned suppression and freezing, which both cause a cessation in activity, appear to be mediated by separate processes.

[1]  M. Halpern.  Effects of midbrain central gray matter lesions on escape-avoidance behavior in rats , 1968 .

[2]  Joseph E LeDoux,et al.  Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  Joseph E LeDoux,et al.  Topographic organization of neurons in the acoustic thalamus that project to the amygdala , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  J. Konorski.  Conditioned reflexes and neuron organization. , 1948 .

[5]  Joseph E LeDoux,et al.  Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of temporal cortex in the rat. , 1993, Cerebral cortex.

[6]  D. Blanchard,et al.  Innate and conditioned reactions to threat in rats with amygdaloid lesions. , 1972, Journal of comparative and physiological psychology.

[7]  F. Mascagni,et al.  Corticoamygdaloid and corticocortical projections of the rat temporal cortex: APhaseolus vulgaris leucoagglutinin study , 1993, Neuroscience.

[8]  T. Gray,et al.  The amygdalo-brainstem pathway: Selective innervation of dopaminergic, noradrenergic and adrenergic cells in the rat , 1989, Neuroscience Letters.

[9]  Joseph E LeDoux,et al.  Fear conditioning induces associative long-term potentiation in the amygdala , 1997, Nature.

[10]  Joseph E LeDoux,et al.  The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  O. Phillipson.  Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: A horseradish peroxidase study in the rat , 1979, The Journal of comparative neurology.

[12]  John P. Aggleton,et al.  The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction. , 1992 .

[13]  Wallace R. McAllister,et al.  CHAPTER 2 – Behavioral Measurement of Conditioned Fear1 , 1971 .

[14]  J. R. Millenson,et al.  Motivational Properties of Conditioned Anxiety , 1972 .

[15]  Michael Davis,et al.  The role of the amygdala in emotional learning. , 1994, International review of neurobiology.

[16]  M. Fanselow,et al.  Distinct Regions of the Periaqueductal Gray Are Involved in the Acquisition and Expression of Defensive Responses , 1998, The Journal of Neuroscience.

[17]  J. Schwartzbaum,et al.  Discrimination Behavior and Conditioned Suppression (CER) following Localized Lesions in the Amygdala and Putamen , 1964 .

[18]  M. Bouton.  Conditioning, remembering, and forgetting. , 1994 .

[19]  M. Herkenham,et al.  Thalamoamygdaloid projections in the rat: A test of the amygdala's role in sensory processing , 1991, The Journal of comparative neurology.

[20]  R. Rescorla,et al.  Two-process learning theory: Relationships between Pavlovian conditioning and instrumental learning. , 1967, Psychological review.

[21]  T. Robbins,et al.  Amygdala-ventral striatal interactions and reward-related processes. , 1992 .

[22]  Michael Davis,et al.  Double Dissociation between the Involvement of the Bed Nucleus of the Stria Terminalis and the Central Nucleus of the Amygdala in Startle Increases Produced by Conditioned versus Unconditioned Fear , 1997, The Journal of Neuroscience.

[23]  Joseph E. LeDoux,et al.  Extinction of emotional learning: Contribution of medial prefrontal cortex , 1993, Neuroscience Letters.

[24]  Joseph E LeDoux,et al.  Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: Parallel recordings in the freely behaving rat , 1995, Neuron.

[25]  M. Lyon.  The role of central midbrain structures in conditioned responding to aversive noise in the rat , 1964, The Journal of comparative neurology.

[26]  Michela Gallagher,et al.  Amygdala central nucleus lesions: Effect on heart rate conditioning in the rabbit , 1979, Physiology & Behavior.

[27]  T. Robbins,et al.  Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala , 1997, Nature.

[28]  A. Black,et al.  Heart Rate: Changes during Conditioned Suppression in Rats , 1966, Science.

[29]  R. Bolles,et al.  Conditioned fear assessed by freezing and by the suppression of three different baselines , 1980 .

[30]  Joseph E LeDoux,et al.  Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. , 1992, Behavioral neuroscience.

[31]  Joseph E LeDoux.  The emotional brain , 1996 .

[32]  D C Blanchard,et al.  Crouching as an index of fear. , 1969, Journal of comparative and physiological psychology.

[33]  M. Fanselow.  The Midbrain Periaqueductal Gray as a Coordinator of Action in Response to Fear and Anxiety , 1991 .

[34]  B. Roozendaal,et al.  Central amygdala lesions affect behavioral and autonomic balance during stress in rats , 1991, Physiology & Behavior.

[35]  B. Skinner,et al.  Some quantitative properties of anxiety , 1941 .

[36]  Joseph E LeDoux,et al.  Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala , 1997, Trends in Neurosciences.

[37]  M. McKERNAN,et al.  Fear conditioning induces a lasting potentiation of synaptic currents in vitro , 1997, Nature.

[38]  R. Bolles,et al.  The effect of predictive cues on freezing in rats , 1976 .

[39]  M. Davis,et al.  Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  T. Robbins,et al.  Effects of excitotoxic lesions of the central amygdaloid nucleus on the potentiation of reward-related stimuli by intra-accumbens amphetamine. , 1996, Behavioral neuroscience.

[41]  J. Liebman,et al.  Mesencephalic central gray lesions and fear-motivated behavior in rats. , 1970, Brain research.

[42]  I. Marks,et al.  The development of normal fear: a review. , 1987, Journal of child psychology and psychiatry, and allied disciplines.

[43]  R. Bevins,et al.  Conditioned Stimulus Determinants of Conditioned Response Form in Pavlovian Fear Conditioning , 1996 .

[44]  Joseph E LeDoux,et al.  Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to an explicit conditioned stimulus and to contextual stimuli. , 1997, Behavioral neuroscience.

[45]  T. Gray,et al.  Organization of amygdaloid projections to brainstem dopaminergic, noradrenergic, and adrenergic cell groups in the rat , 1992, Brain Research Bulletin.

[46]  Joseph E. LeDoux,et al.  Somatosensory and auditory convergence in the lateral nucleus of the amygdala. , 1993, Behavioral neuroscience.

[47]  Joseph E LeDoux.  Emotion: clues from the brain. , 1995, Annual review of psychology.