Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit

Pascoe, Jeffrey P.; Kapp, Bruce S.

doi:10.1016/0166-4328(85)90087-7

Cited by 234 publications

(133 citation statements)

References 33 publications

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Section: Abstract: Limbic Thalamus; Cingulate Cortex; Amygdala; Learmentioning

confidence: 99%

“…A central role of amygdalar neurons is indicated by findings that amygdala lesions impair the acquisition of conditioned immobility (LeDoux et al, 1988; Fanselow and K im, 1994;LeDoux, 1995), autonomic responding (Blanchard and Blanchard, 1972;Spevack et al, 1975;Kapp et al, 1979;Gentile et al, 1986;Iwata et al, 1986;Helmstetter, 1992) and fear-potentiated startle behavior (Davis, 1986(Davis, , 1992Hitchcock and Davis, 1987;Sananes and Davis, 1992). Also, amygdalar neurons exhibit associative, training-induced activity (TIA) during Pavlovian conditioning (Umemoto and Olds, 1975;Applegate et al, 1982;Pascoe and Kapp, 1985;Nishijo et al, 1988; Muramoto et al, 1993;McEchron et al, 1995;Quirk et al, 1995).An involvement of the medial geniculate (MG) nucleus in aversively motivated learning is indicated by the observation of TIA in the medial division of the MG nucleus (MGm) (Olds et al., 1972;Gabriel et al, 1975;Gabriel et al, 1976;Ryugo and Weinberger, 1978;Birt and Olds, 1981;Weinberger, 1982;Edeline, 1990;Edeline and Weinberger, 1992;McEchron et al, 1995), and by impaired conditioning in animals with MG lesions (Iwata et al, 1986;Jarrell et al, 1986; LeDoux et al, 1986a,b;McCabe et al, 1993). Amygdalar and MG neurons are involved in aversively motivated instrumental conditioning processes, as well as in classical aversive conditioning.…”

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Medial Geniculate Lesions Block Amygdalar and Cingulothalamic Learning-Related Neuronal Activity

Poremba

Gabriel

1997

J. Neurosci.

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This study assessed the role of the thalamic medial geniculate (MG) nucleus in discriminative avoidance learning, wherein rabbits acquire a locomotory response to a tone [conditioned stimulus (CS)ϩ] to avoid a foot shock, and they learn to ignore a different tone (CSϪ) not predictive of foot shock. Limbic (anterior and medial dorsal) thalamic, cingulate cortical, or amygdalar lesions severely impair acquisition, and neurons in these areas develop training-induced activity (TIA): more firing to the CSϩ than to the CSϪ. MG neurons exhibit TIA during learning and project to the amygdala. The MG neurons may supply afferents essential for amygdalar and cingulothalamic TIA and for avoidance learning. To test this hypothesis, bilateral electrolytic or excitotoxic ibotenic acid MG nuclear lesions were induced, and multiunit recording electrodes were chronically implanted into the anterior and posterior cingulate cortex, the anterior-ventral and medial-dorsal thalamic nuclei, and the basolateral nucleus of the amygdala before training. Learning was severely impaired and TIA was abolished in all areas in rabbits with lesions. Thus learning and TIA require the integrity of the MG nucleus. Only damage in the medial MG division was significantly correlated with the learning deficit. The lesions abolished the sensory response of amygdalar neurons, and they attenuated (but did not eliminate) the sensory response of cingulothalamic neurons, suggesting the existence of extra geniculate sources of auditory transmission to the cingulothalamic areas. Key words: limbic thalamus; cingulate cortex; amygdala; learning; instrumental conditioning; anterior ventral nucleus; medial dorsal nucleusThere is currently a great interest in the neural circuitry underlying aversively motivated learning (for review, see Davis, 1992;Gabriel, 1993;Lennartz and Weinberger, 1994;LeDoux, 1995;McGaugh et al., 1995;. A central role of amygdalar neurons is indicated by findings that amygdala lesions impair the acquisition of conditioned immobility (LeDoux et al., 1988; Fanselow and K im, 1994;LeDoux, 1995), autonomic responding (Blanchard and Blanchard, 1972;Spevack et al., 1975;Kapp et al., 1979;Gentile et al., 1986;Iwata et al., 1986;Helmstetter, 1992) and fear-potentiated startle behavior (Davis, 1986(Davis, , 1992Hitchcock and Davis, 1987;Sananes and Davis, 1992). Also, amygdalar neurons exhibit associative, training-induced activity (TIA) during Pavlovian conditioning (Umemoto and Olds, 1975;Applegate et al., 1982;Pascoe and Kapp, 1985;Nishijo et al., 1988; Muramoto et al., 1993;McEchron et al., 1995;Quirk et al., 1995).An involvement of the medial geniculate (MG) nucleus in aversively motivated learning is indicated by the observation of TIA in the medial division of the MG nucleus (MGm) (Olds et al., 1972;Gabriel et al., 1975;Gabriel et al., 1976;Ryugo and Weinberger, 1978;Birt and Olds, 1981;Weinberger, 1982;Edeline, 1990;Edeline and Weinberger, 1992;McEchron et al., 1995), and by impaired conditioning in animals with MG lesions (Iwata et al., 198...

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Section: Abstract: Limbic Thalamus; Cingulate Cortex; Amygdala; Learmentioning

confidence: 99%

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confidence: 99%

Medial Geniculate Lesions Block Amygdalar and Cingulothalamic Learning-Related Neuronal Activity

Poremba

Gabriel

1997

J. Neurosci.

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“…This hypothesis was based on the following results: (1) the traininginduced plasticity of amygdalar, anterior cingulate cortical and MD thalamic neurons develops in parallel, in the early stages of learning; the plasticity in these areas diminishes as asymptotic levels of performance are attained (Applegate et al, 1982;Pascoe and Kapp, 1985;Nishijo et al, 1988;Gabriel, 1990;Maren et al, 1991); (2) amygdalar neurons send axons directly to the anterior cingulate cortex and the MD nucleus (Krettek and Price, 1978;Porrino et al, 1981;Price and Amaral, 1981;Price et al, 1987); and (3) the amygdala is involved in mediating acquisition of other aversively motivated behaviors (Blanchard and Blanchard, 1972;Spevack et al, 1975;Gentile et al, 1986;Hitchcock and Davis, 1987;LeDoux et al, 1988;Cahill and McGaugh, 1990;Willner et al, 1991;Helmstetter, 1992;Kapp et al, 1992;Fanselow et al, 1994).…”

Section: Abstract: Limbic Thalamus; Cingulate Cortex; Amygdala; Learmentioning

confidence: 99%

Amygdalar Lesions Block Discriminative Avoidance Learning and Cingulothalamic Training-Induced Neuronal Plasticity in Rabbits

Poremba

Gabriel

1997

J. Neurosci.

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Learning to fear dangerous situations requires the participation of neurons of the amygdala. Here it is shown that amygdalar neurons are also involved in learning to avoid dangerous situations. Amygdalar lesions severely impaired the acquisition of acoustically cued, discriminative instrumental avoidance behavior of rabbits. In addition, the development of anterior cingulate cortical and medial dorsal thalamic training-induced neuronal plasticity in the early stages of behavioral acquisition was blocked in rabbits with lesions. The development of training-induced neuronal plasticity in the medial dorsal and anterior thalamic nuclei in late stages of behavioral acquisition was also blocked in rabbits with lesions. These results indicate that the integrity of the amygdala is essential for the establishment of both early and late training-induced cingulothalamic neuronal plasticity. It is hypothesized that amygdalar traininginduced neuronal plasticity in the initial trials of conditioning represents a substrate of learned fear, essential for the early and late cingulothalamic plasticity that is involved in mediation of acquisition of the instrumental avoidance response.Key words: limbic thalamus; cingulate cortex; amygdala; learning; operant conditioning; anterior ventral nucleus; medial dorsal nucleus Much information concerning the neural mediation of learned behavior has been provided by studies using the "model system" approach. These studies focus effort on the analysis of a single learning paradigm in a particular species (Carew et al., 1984;Steinmetz and Thompson, 1991;Gabriel, 1993). The present study continues an analysis of discriminative avoidance, wherein rabbits learn to step in an activity wheel in response to a tone that predicts foot shock, and they learn to ignore a different tone that does not predict foot shock.Past studies using lesions and multisite recording of neuronal activity have demonstrated that the cingulate cortex and the interconnected medial dorsal (MD) and anterior thalamic nuclei are essential for learning, and that neurons in these areas exhibit massive training-induced neuronal plasticity during learning (for review, see Gabriel, 1993). The thalamic training-induced neuronal plasticity does not depend on cerebral cortical afferents, because lesions in projecting cingulate cortical and hippocampal formation areas did not interfere with, indeed they enhanced, the development of the thalamic plasticity (Gabriel et al., 1987.Here, we tested the hypothesis that the integrity of the amygdala is essential for the development of training-induced plasticity in the anterior cingulate cortex and MD nucleus. This hypothesis was based on the following results: (1) the traininginduced plasticity of amygdalar, anterior cingulate cortical and MD thalamic neurons develops in parallel, in the early stages of learning; the plasticity in these areas diminishes as asymptotic levels of performance are attained (Applegate et al., 1982;Pascoe and Kapp, 1985;Nishijo et al., 1988;Gabriel, 1990;Maren et al...

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“…fear circuitry | learning and memory | long-term depression | long-term potentiation | synaptic plasticity D ecades of research involving various techniques have identified that the amygdala is essential for both innate and learned fear (1). Evidence indicates that neurons in the basolateral amygdalar complex (BLA) (basal and lateral nuclei) (2) are responsive to both the conditional stimulus (CS) and unconditional stimulus (US) (3,4), undergo plastic changes during fear conditioning (5), and are necessary for producing fear responses (6,7). Indeed, a recent study has shown that optogenetically induced depolarization of pyramidal neurons in the lateral amygdala (LA) can elicit a fear unconditional response (UR) and, when repeatedly paired with auditory CS, supports fear conditioning via Hebbian-like synaptic plasticity (8).…”

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confidence: 99%

Dorsal periaqueductal gray-amygdala pathway conveys both innate and learned fear responses in rats

Kim¹,

Horovitz

Pellman³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

157

132

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The periaqueductal gray (PAG) and amygdala are known to be important for defensive responses, and many contemporary fearconditioning models present the PAG as downstream of the amygdala, directing the appropriate behavior (i.e., freezing or fleeing). However, empirical studies of this circuitry are inconsistent and warrant further examination. Hence, the present study investigated the functional relationship between the PAG and amygdala in two different settings, fear conditioning and naturalistic foraging, in rats. In fear conditioning, electrical stimulation of the dorsal PAG (dPAG) produced unconditional responses (URs) composed of brief activity bursts followed by freezing and 22-kHz ultrasonic vocalization. In contrast, stimulation of ventral PAG and the basolateral amygdalar complex (BLA) evoked freezing and/or ultrasonic vocalization. Whereas dPAG stimulation served as an effective unconditional stimulus for fear conditioning to tone and context conditional stimuli, neither ventral PAG nor BLA stimulation supported fear conditioning. The conditioning effect of dPAG, however, was abolished by inactivation of the BLA. In a foraging task, dPAG and BLA stimulation evoked only fleeing toward the nest. Amygdalar lesion/inactivation blocked the UR of dPAG stimulation, but dPAG lesions did not block the UR of BLA stimulation. Furthermore, in vivo recordings demonstrated that electrical priming of the dPAG can modulate plasticity of subiculum-BLA synapses, providing additional evidence that the amygdala is downstream of the dPAG. These results suggest that the dPAG conveys unconditional stimulus information to the BLA, which directs both innate and learned fear responses, and that brain stimulation-evoked behaviors are modulated by context. fear circuitry | learning and memory | long-term depression | long-term potentiation | synaptic plasticity D ecades of research involving various techniques have identified that the amygdala is essential for both innate and learned fear (1). Evidence indicates that neurons in the basolateral amygdalar complex (BLA) (basal and lateral nuclei) (2) are responsive to both the conditional stimulus (CS) and unconditional stimulus (US) (3, 4), undergo plastic changes during fear conditioning (5), and are necessary for producing fear responses (6, 7). Indeed, a recent study has shown that optogenetically induced depolarization of pyramidal neurons in the lateral amygdala (LA) can elicit a fear unconditional response (UR) and, when repeatedly paired with auditory CS, supports fear conditioning via Hebbian-like synaptic plasticity (8).However, stimulation-induced fear conditioning is not only achievable through the amygdala. Other studies have found that stimulation of the dorsal periaqueductal gray (dPAG) is an effective US in fear conditioning (9, 10). The PAG has long been implicated in generating defensive behaviors (11), and it has been suggested that its stimulation can support fear conditioning to a CS because it transmits the aversive US information to the LA (9, 12). Some have a...

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Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit

Cited by 234 publications

References 33 publications

Medial Geniculate Lesions Block Amygdalar and Cingulothalamic Learning-Related Neuronal Activity

Medial Geniculate Lesions Block Amygdalar and Cingulothalamic Learning-Related Neuronal Activity

Amygdalar Lesions Block Discriminative Avoidance Learning and Cingulothalamic Training-Induced Neuronal Plasticity in Rabbits

Dorsal periaqueductal gray-amygdala pathway conveys both innate and learned fear responses in rats

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