Context-specific multi-site cingulate cortical, limbic thalamic, and hippocampal neuronal activity during concurrent discriminative approach and avoidance training in rabbits

Abstract

This study assessed the context specificity of learning-related neuronal activity: whether the same physical stimuli would elicit different neuronal responses depending on the learning situation. Neuronal activity was recorded simultaneously in six limbic areas as rabbits learned to approach a spout for water reinforcement after a tone (CS+) and to ignore the spout after a different tone (CS-). The rabbits then received avoidance training in which they learned to prevent a foot-shock by stepping in an activity wheel after one tone (CS+) and to ignore a different tone (CS-). Avoidance training sessions were alternated (1 session daily) with sessions in the well learned approach task. The tone assigned as the CS+ for approach training was the CS- for avoidance training and vice versa. The neuronal records of the anterior ventral and medial dorsal thalamic nuclei and the anterior and posterior cingulate cortices showed neuronal discrimination appropriate to the approach task during pretraining in the avoidance training apparatus with unpaired presentations of the tones and foot-shock. This finding demonstrated that the discriminative neuronal activity for approach learning was unaffected by a change in context in the pretraining session. However, context-appropriate discrimination occurred in both tasks thereafter, with the exception that medial dorsal thalamic neurons no longer showed discrimination during overtraining in the approach task. Hippocampal area CA1 neurons showed entirely context-appropriate discrimination in both tasks, with no carryover of the approach-relevant discrimination to the avoidance training apparatus. Avoidance training stage-specific peaks of training-induced excitation in different brain areas were not elicited by the same physical stimuli during concurrent approach training sessions. The results are consistent with an involvement of limbic-circuit neuronal activity in the use of context cues for mnemonic retrieval. Differential persistence of the approach-related neuronal discrimination in anterior and posterior cingulate cortex confirmed the previously hypothesized distinct mnemonic functions of these areas.

Lesions of the entorhinal cortex disrupt behavioral and neuronal responses to context change during extinction of discriminative avoidance behavior

“…Our preferred view is that dynamic modulation of amygdalar and cingulothalamic neurons by hippocampal and entorhinal cortical neurons can prepare the cingulothalamic neurons to respond to task-relevant cues with context-specific patterns of activation which serve to defeat mnemonic pro-active and retro-active interference (Freeman et al 1996). These activation patterns are the first in a cascade of brain events that terminates in retrieval of context-appropriate behavior and memory.…”

Mediodorsal thalamic afferents to layer III of the rat prefrontal cortex: Synaptic relationships to subclasses of interneurons

“…It was previously shown that the MD is implicated in the normal functioning of different memory processes, both in rats (Floresco et al, 1999;Freeman et al, 1996;Hunt and Aggleton, 1998a;Hunt and Aggleton, 1998b) and monkeys (Gaffan and Parker, 2000;Tanibuchi and Goldman-Rakic, 2003). In one study, it was actually found that MD neurons fired during the delay period of a working memory task (Tanibuchi and Goldman-Rakic 2003).…”

“…Behavioral studies in rats subjected to MD lesions or electrophysiological recordings from MD showed that a series of cognitive functions, including object recognition (Mumby et al, 1993), working memory (Freeman et al, 1996), planning and prospective coding (Daum and Ackermann, 1994), depended on intact inputs from the MD.…”

Hippocampal Inactivation Disrupts the Acquisition and Contextual Encoding of Fear Extinction

“…The hippocampus plays an additional role in using contextual cues during the encoding of memory (Hirsh, 1974;Honey and Good, 1993;Freeman et al, 1996;Good et al, 1998;Kennedy and Shapiro, 2004;Smith et al, 2004). Although involvement of the hippocampus in the context-specific retrieval of extinction has begun to receive attention, no explicit attempts have been made to elucidate a role for the hippocampus in encoding the context specificity of extinction.…”