Single cell activity in the auditory cortex of the unanesthetized, behaving monkey: correlation with stimulus controlled behavior.

The neural activity of 60 cells in the auditory cortices of two rhesus monkeys was examined in relation to systematic variations in cued reinforcement conditions. Subjects were trained on a variant of the auditory reaction time (RT) task. In the final behavioral paradigm monkeys were rewarded for rapid key releases to all tonal stimuli in one reinforcement condition (frequency irrelevant = FI), while in the other stimulus-cued condition (frequency discrimination = FD) releases to certain tonal test frequencies were unrewarded. Upon completion of behavioral training, RTs to identical tonal test stimuli were longer and more variable when presented in the unrewarded (FD) condition. Following neurosurgery it was possible to observe the effects of reinforcement condition on auditory RT performance and the activity of single auditory cortical cells simultaneously. Of the auditory cortical cells sampled, 25% showed definite and repeatable alterations in evoked activity to the same tonal stimulus which were correlated with reinforcement condition. For nearly all cells examined the influence of reinforcement condition was much the same: on excitatory responses were increased in the FD condition. A few of the cells also showed alterations in latency and/or pattern of evoked discharge. Importantly, none of the units examined showed changes in their spontaneous discharge rates as a function of reinforcement condition. both peripheral mechanical and central neural theories were considered as a basis for the observed neural alterations. The specificity and latency of the alterations as well as the absence of tonic effects seemed to indicate that the neural changes observed were mediated by central mechanisms. Our results strongly suggest that the activity of a sample of auditory cortical neurons depends on the behavioral state of the preparation. We propose that 'behavioral state", appropriately defined, can be a useful concept for neurophysiologists.