The amygdala central nucleus and appetitive Pavlovian conditioning: lesions impair one class of conditioned behavior

Rats with neurotoxic lesions of the amygdala central nucleus (CN) were trained using appetitive Pavlovian conditioning procedures. Conditioned responses (CRs) that are representative of 2 classes of behavior were monitored. One type of CR resembled the orienting responses that were elicited by the conditioned stimuli (CSs) prior to pairing with food reinforcement: the other type of CR resembled the behavior elicited by food reinforcement itself. Holland (1977, 1984) has referred to these as CS-generated and unconditioned stimulus (US)-generated CRs, respectively. During differential conditioning, some lesioned and unlesioned rats received reinforced presentations of a visual cue and nonreinforced presentations of an auditory cue, and the others in each lesion condition received reinforced auditory and nonreinforced visual cue presentations. Relative to the control group, the CN-lesioned rats were impaired in the acquisition of CS-generated CRs to both visual and auditory CSs. Orienting responses and habituation to the CSs were, however, comparable for the lesion and control groups. Moreover, rats with CN lesions readily acquired the US-generated CRs. Thus, a specific class of conditioned behavior was impaired by CN damage. Many studies using aversive Pavlovian procedures have suggested that CN lesions impair fear conditioning. The present results suggest another role for CN in the conditioning of orienting/attentional responses.

[1]  N. Schneiderman,et al.  The role of amygdaloid central nucleus in the retention of differential pavlovian conditioning of bradycardia in rabbits , 1986, Behavioural Brain Research.

[2]  B. Campbell,et al.  Role of the central nucleus of the amygdala in olfactory heart rate conditioning. , 1989, Behavioral neuroscience.

[3]  P. Holland.  Conditioned stimulus as a determinant of the form of the Pavlovian conditioned response. , 1977, Journal of experimental psychology. Animal behavior processes.

[4]  P. Holland,et al.  Differential effects of omission contingencies on various components of Pavlovian appetitive conditioned responding in rats. , 1979, Journal of experimental psychology. Animal behavior processes.

[5]  D. Amaral,et al.  An autoradiographic study of the projections of the central nucleus of the monkey amygdala , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  L. Weiskrantz,et al.  Behavioral changes associated with ablation of the amygdaloid complex in monkeys. , 1956, Journal of comparative and physiological psychology.

[7]  Pharmacological and anatomical analysis of fear conditioning using the fear-potentiated startle paradigm. , 1986 .

[8]  G. Stock,et al.  Cardiovascular changes during arousal elicited by stimulation of amygdala, hypothalamus and locus coeruleus. , 1981, Journal of the autonomic nervous system.

[9]  Michael Davis,et al.  Pharmacological and anatomical analysis of fear conditioning using the fear-potentiated startle paradigm. , 1986, Behavioral neuroscience.

[10]  A. Riolobos,et al.  Open field activity and passive avoidance responses in rats after lesion of the central amygdaloid nucleus by electrocoagulation and ibotenic acid , 1987, Physiology & Behavior.

[11]  Joseph E LeDoux,et al.  Intrinsic neurons in the amygdaloid field projected to by the medial geniculate body mediate emotional responses conditioned to acoustic stimuli , 1986, Brain Research.

[12]  B. Kaada.  Stimulation and Regional Ablation of the Amygdaloid Complex with Reference to Functional Representations , 1972 .

[13]  Jeffrey P. Pascoe,et al.  Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit , 1985, Behavioural Brain Research.

[14]  M. Gallagher,et al.  Multiple unit activity recorded from amygdala central nucleus during Pavlovian heart rate conditioning in rabbit , 1982, Brain Research.

[15]  D. Amaral,et al.  The afferent connections of the substantia innominata in the monkey, Macaca fascicularis , 1985, The Journal of comparative neurology.

[16]  Michael Davis,et al.  Lesions of the amygdala, but not of the cerebellum or red nucleus, block conditioned fear as measured with the potentiated startle paradigm. , 1986, Behavioral neuroscience.

[17]  C. L. Hull.  Learning: II. The Factor of the Conditioned Reflex. , 1934 .

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

[19]  L. Heimer,et al.  New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: The striatopallidal, amygdaloid, and corticopetal components of substantia innominata , 1988, Neuroscience.

[20]  L. Swanson.  The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[21]  Joseph E. LeDoux,et al.  Cardiovascular responses elicited by stimulation of neurons in the central amygdaloid nucleus in awake but not anesthetized rats resemble conditioned emotional responses , 1987, Brain Research.

[22]  P. Holland.  Origins of Behavior in Pavlovian Conditioning , 1984 .

[23]  Sanger Brown,et al.  An Investigation into the Functions of the Occipital and Temporal Lobes of the Monkey's Brain , 1888 .

[24]  M. Gallagher,et al.  β-adrenergic manipulation in amygdala central n. alters rabbit heart rate conditioning , 1980, Pharmacology Biochemistry and Behavior.

[25]  Jeffrey P. Pascoe,et al.  Opiate effects in the amygdala central nucleus on heart rate conditioning in rabbits , 1981, Pharmacology Biochemistry and Behavior.

[26]  James L. McGaugh,et al.  Brain Organization and Memory: Cells, Systems, and Circuits , 1992 .

[27]  Behavioral effects after ibotenic acid, 6-OHDA and electrolytic lesions in the central amygdala nucleus of the rat , 1986, Physiology & Behavior.

[28]  M. Gallagher,et al.  Cardiovascular responses elicited by electrical stimulation of the amygdala central nucleus in the rabbit , 1982, Brain Research.