Neuronal responses related to visual recognition.

To analyse the neural basis of long-term memory, recordings were made from single neurons in monkeys performing a visual recognition task of the type impaired in anterograde amnesia in man. Each visual stimulus was shown twice per day, once as novel, and after 0 to 17 other intervening items in the recognition task, on a second trial, as familiar, when the monkey could lick to obtain fruit juice if he recognized the stimulus correctly. At the anterior border of the thalamus, a population of neurons was found which responded to the stimuli only when they were familiar. The activity of these neurons was not related to lick responses. Further, in a different, visual discrimination, task, a number of these neurons were found to respond both to the familiar rewarded stimulus to which the monkey always licked, and to the familiar aversive stimulus to which he did not lick. This shows that in a reward association task these neurons respond on the basis of familiarity, providing evidence for a dissociation of recognition and associative memories. Analysis of the responses of these neurons in the continuous visual recognition task showed that the responses to familiar stimuli were time-locked to the onset and duration of the visual stimulation (brief exposures producing brief responses). The response latencies were in the range 100 to 200 ms. A 100 ms exposure of the stimulus was sufficient for the stimulus to be encoded, and a 100 ms exposure was also sufficient for a recognition related response. The magnitude of the neuronal response on trials with familiar stimuli decreased as the number of trials between the first (novel) and second (familiar) presentation of the same stimulus increased. The rate of this decay or 'forgetting' varied from cell to cell and was best described by an exponential function. Repeated exposure tended to slow the rate of forgetting, and two or three repeated presentations prolonged some cell 'memories' for more than 100 intervening trials. Although the majority of the neurons did not have such long 'memories', in that they responded as novel to stimuli seen on a preceding day, so that their responses could be related to recency but not to absolute recognition of ever having seen a stimulus before, 2 neurons did respond to stimuli which had not been seen for 24 h. The neurons showed some ability to respond to stimuli as familiar despite changes in viewing conditions and transformations such as 90 deg rotation. These findings indicate that the responses of these neurons at the anterior border of the thalamus are activated during recency or longer term recognition processing, both of which are impaired in anterograde amnesia in man. Measurement of the responses of these neurons, which appear to have access to memory mechanisms, has allowed parameters affecting such memory mechanisms to be investigated.