Basolateral amygdaloid multi-unit neuronal correlates of discriminative avoidance learning in rabbits

Abstract

Basolateral (BL) amygdaloid multi-unit activity was recorded as male albino rabbits learned to avoid a foot-shock unconditioned stimulus (US) by stepping in an activity wheel to an acoustic (pure tone) warning stimulus (CS+). A second tone (CS-) of different auditory frequency than the CS+ was presented in an irregular order on half of the conditioning trials but was never followed by the US. BL amygdaloid neurons developed, in the first session of conditioning, enhanced CS-elicited discharges relative to discharges recorded during pretraining with tones and noncontingent US presentations (excitatory plasticity), and greater discharges to the CS+ than to the CS- (discriminative plasticity). The discriminative plasticity attained maximal magnitude as the rabbits reached the asymptote of behavioral discrimination, and persisted during post-asymptotic training. Peak excitatory plasticity occurred in the session of the first significant behavioral discrimination and declined during the asymptotic and post-asymptotic stages of training. Similar patterns of excitatory and discriminative plasticity in structures directly interconnected with the BL nucleus (anterior cingulate cortex; medial dorsal thalamic nucleus) and effects of lesions suggest that the neurons in these areas participate in a circuit involved in mediation of avoidance learning.

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

“…Four rabbits given sham (saline) injections and recording electrodes served as controls for assessment of the behavioral effects of the ibotenic acid lesions. Control data for assessment of the effects of the lesions on amygdalar training-related neuronal activity were obtained from rabbits in a previous study (Maren et al, 1991). Although there was a substantial time gap between the collection of these control data and the present study, the amygdalar changes observed in 1991 were replicated very recently with the same procedures (Freeman et al, 1997).…”

“…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).…”

“…Statistically significant discriminative TIA developed in both areas during the first conditioning session, the magnitude of the effect reached maximum early in training, and the effect declined in both areas as the rabbits reached the acquisition criterion Maren et al, 1991). In contrast, neurons in posterior cingulate cortex, the AV thalamic nucleus and the MD thalamic nucleus did not exhibit maximal discriminative TIA until criterion was reached (for review, see Gabriel, 1993).…”

“…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.…”

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

“…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).…”