Journal of Neuroscience, Vol 16, 1538-1549, Copyright © 1996 by Society for Neuroscience
Context-specific multi-site cingulate cortical, limbic thalamic, and hippocampal neuronal activity during concurrent discriminative approach and avoidance training in rabbits
JH Freeman Jr, C Cuppernell, K Flannery and M Gabriel
Department of Psychology, University of Illinois, Urbana 61801, USA.
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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