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

Abstract

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...

Neurocognitive effects of phobia-related stimuli in animal-fearful individuals

“…According to this account, the elaboration in memory (e.g., rehearsing or reactivating) of belonging pairs of stimuli (phobia-related and aversive) disrupts the elaboration of nonbelonging pairs of stimuli (neutral and aversive). Importantly, the elaboration of belonging pairs of stimuli in memory may occur as a psychological corollary of amygdalar involvement in aversively motivated associative learning (see, e.g., Davis, 1992;Phelps & Anderson, 1997;Poremba & Gabriel, 1997; see also Kopp et al, 2005).…”

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

“…Amygdalar and MG neurons are involved in aversively motivated instrumental conditioning processes, as well as in classical aversive conditioning. TIA develops rapidly in these areas during discriminative avoidance learning in rabbits (Gabriel et al, 1975(Gabriel et al, , 1976(Gabriel et al, , 1991bMaren et al, 1991) and amygdalar lesions severely impair behavioral acquisition (Poremba and Gabriel, 1997).…”

“…Intriguingly, cingulothalamic TIA and behavioral learning are blocked in rabbits with bilateral amygdalar lesions (Poremba and Gabriel, 1997), suggesting that amygdalar efferents are essential for the cingulothalamic TIA.…”

“…It has been proposed (Poremba and Gabriel, 1997) that the rapid amygdalar TIA may represent the acquisition of conditioned fear, whereas the more gradual cingulothalamic TIA development may reflect changes underlying acquisition of the instrumental behavior.…”

“…Amygdalar and MG neurons are involved in aversively motivated instrumental conditioning processes, as well as in classical aversive conditioning. TIA develops rapidly in these areas during discriminative avoidance learning in rabbits (Gabriel et al, 1975(Gabriel et al, , 1976(Gabriel et al, , 1991bMaren et al, 1991) and amygdalar lesions severely impair behavioral acquisition (Poremba and Gabriel, 1997).Results of neuronal recording and lesion studies demonstrate a critical involvement of cingulate cortex and related limbic areas [the anterior and medial dorsal (MD) nuclei] of the thalamus in discriminative avoidance learning (for review, see Gabriel., 1993; see also Kubota et al, 1996). Intriguingly, cingulothalamic TIA and behavioral learning are blocked in rabbits with bilateral amygdalar lesions (Poremba and Gabriel, 1997), suggesting that amygdalar efferents are essential for the cingulothalamic TIA.…”