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Patterns of spike activity were measured in the pericruciate cortex of conscious cats before and after development of a Pavlovian conditioned eye blink response. Unit activity was tested with presentations of a click conditioned stimulus (CS) and a hiss discriminative stimulus (DS) of similar intensity to the click. Unit discharge in response to the CS increased after conditioning, but not after backward conditioning when conditioned reflexes (CRs) were not performed. Rates of spontaneous, baseline discharge were not increased after conditioning with respect to rates of discharge measured in the naive state. It appeared that an increase in the ratio of CS-elicited discharge to background activity, together with an increase in the number of units responding to the CS after conditioning, supported discrimination of the CS from the DS and performance of the conditioned blink response. This is the first detailed characterization of patterns of a rapidly conditioned Pavlovian response. Activation of units by the CS preceded the onset of the CR, supporting the hypothesis that the activity played a role in initiating the conditioned eye blink movement. Extinction with retention of performance of the CR was associated with perseverance of the increased unit discharge in response to the CS. Extinction with substantially reduced performance of the CR was associated with diminution of the unit response to the CS below levels found with conditioning. Averages of patterns of spike activity elicited by the CS after conditioning showed components of discharge with onsets of 8–40 msec (alpha 1), 40–72 msec (alpha 2), 72–112 msec (beta), and greater than 112 msec (gamma), corresponding to each of four separate excitatory EMG components of the compound blink CR. Each component increased in magnitude after conditioning, relative to levels found in the naive state. The finding that long- as well as short-latency components of unit activation increased after conditioning supported the hypothesis that generation of both long- and short-latency blink CRs in normal animals may depend significantly on neural circuitry and mechanisms within the motor cortex.

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Measurements were made of resting potentials, input resistance, and excitability to intracellularly applied, depolarizing current pulses in neurons of the pericruciate cortex of conscious cats before and after acquisition of a rapidly conditioned eye blink reflex (CR). Neuronal excitability increased after conditioning, and an increased input resistance was found to be correlated with the increased level of excitability. No associated changes were found in resting potentials as a consequence of conditioning. When cells were divided into groups according to the latency of spike activity elicited by a click conditioned stimulus (CS) in relation to four separate excitatory EMG components of the compound blink CR, excitability increases were found in cells with increased spike activity at alpha 1 (8–40 msec), alpha 2 (40–72 msec), beta (72–112 msec), and gamma (112–160 msec) latencies after delivery of the CS. Also, the proportion of cells with high excitability (less than 0.7 nA required for spike elicitation) was increased at each latency period after conditioning. Increases in later components of spike discharge could also be found in the cells with increases in earlier components of discharge and increased excitability. The findings suggested that excitability increases facilitated a responsiveness to the CS that supported production of long- as well as short-latency components of the blink CR. Many of the changes in neuronal properties found after rapid eye blink conditioning, such as the increases in excitability and resistance and in the proportion of CS-excitable cells, resembled changes found earlier after acquisition of a slowly developing Pavlovian blink CR, using the same click CS and tap unconditioned stimulus without addition of a hypothalamic stimulus. The possibility should be considered that the (10–100 times) more rapidly acquired form of eye blink conditioning does not represent a different form of conditioning, but instead a change in the rate of conditioning supported by the more rapid production of increases in neural excitability.