Stimulus-related and movement-related single-unit activity in rabbit cingulate cortex and limbic thalamus during performance of discriminative avoidance behavior.

Neuronal discharges related to acoustic conditional stimuli and locomotive behavioral responses of 152 anterior and medial dorsal (MD) thalamic and cingulate cortical single-units sorted from multi-unit activity were recorded as rabbits performed in a discriminative avoidance task. The goals were: (1) to document the single-unit constituents of multi-site, multi-unit activity recorded previously in response to the conditional stimuli used for avoidance training; and (2) to document neuronal activity related to the onset of the behavioral avoidance response. Ninety-five units showed discriminative discharges: significantly different firing rates 90-700 ms after a foot shock-predictive conditional stimulus (CS+) than to a safety-predictive conditional stimulus (CS-). In accord with the multi-unit data, a majority of these units discharged at higher rates after the CS+ than after the CS-. The discharge rates of 87 units were greater during the 2-s period preceding the onset of avoidance responses than during comparable trial periods after CS-presentations followed by no response. Fifty-six of the 87 avoidance-related units exhibited a progressive ramp-like firing increase 2 s before the avoidance response, with the maximal discharge rate occurring 200 ms before the response. These dynamic pre-avoidance discharges occurred first in limbic thalamus then in cingulate cortex, suggesting that cortical pre-motor processing may confer temporal specificity upon a more generalized command volley relayed from thalamus. Unlike the multi-unit data, 24 neurons exhibited inverse discrimination, i.e., significantly greater discharges in response to the CS-than to the CS+. Also 27 neurons showed significantly more firing in the 2-s period before the end of CS-trials in which no behavioral response occurred, than in the 2-s pre-avoidance period on CS+ trials with responses. This "inverse' CS-related and pre-avoidance activity occurred at low incidence (< 15%) in all areas except the MD nucleus, wherein it was exhibited by 45% of the recorded units. The inverse activity may reflect the operation of local inhibitory neurons which suppress the discharges of other neurons in response to the CS-. The prevalence of inverse activity in the MD nucleus suggested an involvement of this area in behavioral inhibition.