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.

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Rabbits with bilateral transecting lesions of the mamillothalamic tract, control (tract-sparing and sham) lesions, or no lesions, and chronic, fixed-position anterior ventral (AV) and medial dorsal (MD) thalamic and posterodorsal subicular complex unit recording electrodes were trained to step in an activity wheel in response to a 0.5 sec tone (CS+) in order to avoid a brief foot shock. The rabbits also learned to ignore a different tone (CS-) not predictive of shock. Behavioral acquisition was significantly retarded in rabbits with mamillothalamic tract transection compared to controls. When trained, transected rabbits failed to avoid the shock more often than controls. Mamillothalamic tract transection abolished and control lesions attenuated AV thalamic discriminative training-induced activity (i.e., development with training of greater discharges in response to the CS+ than to the CS-). Transection and control lesions attenuated AV thalamic excitatory training-induced activity (greater elicited activity during training than during unpaired tone-shock presentations before training) as well as AV thalamic “spontaneous” baseline unit activity. CS-elicited discharge magnitude was reduced by control lesions and it was further reduced by tract transecting lesions. Significant lesion-related changes were not found in the subicular or MD thalamic neuronal receptor. Mamillothalamic tract afferent information flow is thus essential for AV thalamic discriminative training-induced activity, excitatory training-induced activity, tone- elicited discharges and maintenance of conditioned avoidance responses. The effects of the control lesions suggested that afferents which course in parallel with and near the mamillothalamic tract may contribute to AV thalamic spontaneous activity and excitatory training- induced activity.