Amygdalar Efferents Initiate Auditory Thalamic Discriminative Training-Induced Neuronal Activity

Abstract

It is well known that neurons of the medial geniculate (MG) nucleus of the thalamus send axonal projections to the amygdala. It has been proposed that these projections supply information that supports amygdalar associative processes underlying acquisition of acoustically cued conditioning and learning. Here we demonstrate the reverse direction of influence. Temporary inactivation of the amygdala using the GABA A receptor agonist muscimol just before the onset of discriminative avoidance conditioning permanently blocked the development of training-induced discriminative neuronal activity in the MG nucleus of rabbits. No discriminative activity developed when the amygdala was inactivated or during later training to criterion without muscimol. Thus, amygdalar processing at the outset of training is necessary for the development of training-induced discriminative activity of neurons in the MG nucleus.Key words: muscimol; GABA A agonist; temporary lesion; rabbits; associative conditioning; retention; multiunit neuronal activity It is well established that neurons in the amygdala and the medial geniculate (MG) nucleus, the auditory region of the sensory thalamus, are importantly involved in mediating acoustically cued Pavlovian and instrumental aversive conditioning Jarrell et al., 1986;LeDoux et al., 1986;McEchron et al., 1995;Maren and Fanselow, 1996;Davis, 1997; Poremba and Gabriel, 1997a,b;Armony et al., 1998;Ferry et al., 1999). Yet controversy remains as to the separate and distinct contributions of these nuclei, and little is known about how their neurons interact in mediating learning and performance.These issues could have been neatly resolved years ago had it been possible to confirm the hypothesis that neurons of the MG nucleus act simply to relay acoustic data to the amygdala via the direct axonal pathway documented by LeDoux et al. (1985). On this simple view, the function of MG nuclear neurons is sensory coding and transmission of acoustic signals. Interaction within the amygdala of the acoustic information with information concerning reinforcing stimuli would promote the development of plasticity at amygdalar synapses, which would thenceforth allow amygdalar neurons to respond uniquely to associatively significant acoustic cues, thus inducing the output of learned emotional responses and behaviors in other parts of the learning-relevant circuitry.A finding not easily incorporated into the foregoing model is the occurrence of training-induced associative neuronal activity, not simply sensory transmission, in the MG nucleus itself. For example, conditioning-induced, brief-latency discriminative neuronal activity develops in the medial region of the MG nucleus, and this activity exhibits reversal, during acquisition and reversal learning of a discriminative avoidance response (for review, see Gabriel et al., 1982). In the discriminative avoidance task, rabbits learn to avoid a foot shock by locomoting in response to a tone, the positive conditional stimulus (CSϩ), and they ignore a different tone, the CS...

Enhancement of Inhibitory Avoidance and Conditioned Taste Aversion Memory With Insular Cortex Infusions of 8-Br-cAMP: Involvement of the Basolateral Amygdala

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Specific long-term memory traces in primary auditory cortex

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“…In summary, available evidence strongly suggests that Hebbian neural changes occur in LA during fear conditioning, and these changes are critical for the conditioning of fear responses to an auditory CS. Although LA may not be the only site of such changes (e.g., Weinberger 1995;Maren et al 2001;Poremba and Gabriel 2001), it is very likely a site where changes relevant to behavioral fear learning occur. We now discuss synaptic events that might underlie these neural changes in LA.…”