Neuronal activity related to visual recognition memory: long-term memory and the encoding of recency and familiarity information in the primate anterior and medial inferior temporal and rhinal cortex.

Recordings of the activity of 2705 single neurones were made in entorhinal and perirhinal cortex, area TG of the temporal lobe, and the inferior temporal cortex both during monkeys' performance of a serial recognition memory task using complex pictures and when monkeys were shown objects. Responses of 120 (9.7%) of the visually responsive neurons recorded were significantly smaller to the second than to the first presentations of unfamiliar stimuli. The incidence of such responses was highest in perirhinal cortex plus areas TE1 and TE2 of the temporal lobe, intermediate in lateral entorhinal cortex and areas TE3 and TG, and lowest in other parts of entorhinal and inferior temporal cortex. Response decrements were maintained across 20 or more intervening presentations of other stimuli for the majority of the neurones tested. Responses of 43 (14.4%) of the visually responsive neurones tested were significantly greater to unfamiliar than to highly familiar stimuli. Such differential responses were found only in lateral entorhinal and perirhinal cortex plus areas TG, TE1, TE2 and TE3. For 6 neurones the response difference was significant even when the familiar stimuli had not been seen for more than 24 h: such neurones demonstrate access to information stored in long-term memory for more than 24 h. Seven familiarity neurones signalled information concerning the relative familiarity of stimuli but not information concerning how recently they were last seen; 58 recency neurones signalled information concerning the recency of presentation of stimuli, but not their relative familiarity. Thus certain neurones demonstrate the separable encoding of recency and familiarity information. Neurones signalling information of use for recognition memory are found in cortex close to the rhinal sulcus where lesions result in major deficits in the performance of recognition memory tasks. The conjunction of these findings provides strong evidence for the importance of these neurones and this cortex for processes (recency and familiarity discrimination) necessary for recognition and working memory. The possible relation of the neuronal responses to priming memory is also discussed.

The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gyrus and inferior temporal cortex of the primate.

The activity of 736 single neurons was recorded from the hippocampal formation (HF), the rhinal cortex (RH), the medial and anterior inferior temporal cortex (TE), or areas TF and TH of the parahippocampal gyrus (PHG) of monkeys during the performance of a delayed matching to sample task. The results indicate differences between the areas in their contributions to sensory processing and memory. Of the neurons, 55% responded to either the first (S1) and/or the second (S2) of the two successively presented visual stimuli. The proportion of responsive neurons and the proportion of neurons that responded selectively on the basis of shape or color (but not size) were significantly higher in areas TE + RH than in HF + PHG. The responses to S1 differed from those to S2 for 18% of the total sample: of these differentially responsive neurons, 66% of the TE + RH neurons responded more strongly to S1 (the sample presentation, allowing stimulus acquisition), whereas 71% of the HF + PHG neurons responded more strongly to S2 (the match/nonmatch comparison, when the behavioral decision could be made). Of 239 TE + RH neurons recorded during the delayed matching task or when objects were shown, 12% displayed evidence of memory for the previous occurrence of stimuli by responding strongly to the first, but significantly less strongly to subsequent presentations of visual stimuli that were novel or had not been seen recently. In contrast, none (0%) of 328 neurons so tested in HF and PHG had a response that declined significantly on stimulus repetition. For six (86%) of seven TE + RH neurons tested, the decrement in response persisted even after distraction by intervening presentations of other stimuli. Further evidence of information storage was found for 7 (33%) of 21 neurons for which responses to the first presentations of unfamiliar objects were significantly greater than to the first presentations of very familiar objects, even though the familiar objects had not been seen for greater than 15 min.

Hippocampus and medial temporal cortex: neuronal activity related to behavioural responses during the performance of memory tasks by primates.

Neuronal activity was recorded in the hippocampal formation, the parahippocampal gyrus and medial inferotemporal cortex of monkeys performing memory tasks. In a modified delayed matching to sample task in which 2 sequentially presented stimuli were compared on each trial, a match condition required a right panel press, whereas a non-match condition required a left panel press. The activity of 336/736 (45.7%) neurons was related to the behavioural responses (left or right panel presses) in this task. The incidence of response-related activity was 57.4% in cortical areas adjacent to the rhinal sulcus plus medial inferotemporal cortex, and 40.2% for the hippocampal formation. For 58.9% of these response-related neurons, the activity change associated with the behavioural response was greater than that during presentation of the sensory stimuli, though neurons commonly responded (33.2% of all recorded neurons) to both sensory and motor events. The activity of 198 neurons (26.9%) differed between go-left and go-right trials; such neurons were found in all areas but were nearly twice as common in the posterior as in the anterior hippocampal formation. The importance of visual stimuli for the response-related neuronal activity was examined during the performance of a delayed alternation task without visual cues indicating direction of response. The response-related activity of 8 neurons recorded during the delayed alternation and the delayed matching tasks was similar in both tasks, indicating that memory for the behavioural responses influences the activity of the response-related neurons. In order to test the effects of stimulus familiarity and non-spatial responses on medial temporal neurons, recognition memory and visual discrimination tasks requiring lick responses were performed. The activity of 2/375 (0.5%) neurons was related to the lick responses; 3/68 neurons in the inferomedial temporal cortex responded on the basis of stimulus novelty and none reflected their reinforcement value. It is concluded that the hippocampal formation, the parahippocampal gyrus and medial inferotemporal cortex all have a role in the utilisation of sensory, mnemonic and motor information underlying the selection of spatially-directed behavioural responses.

Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory.

Amnesia has been reported to result from combined damage to the amygdala, hippocampus and inferomedial temporal cortex in man and monkey. Evidence is presented that neuronal activity in the monkey inferomedial temporal cortex reflects memory for the previous occurrence of visual stimuli: 26 (15%) of 173 single units responded more strongly to first than to subsequent presentations of unfamiliar stimuli. No such responses were found for neurones recorded in the hippocampus and subicular cortex. The findings suggest that the inferomedial temporal cortex plays a central role in processes necessary for recognition memory.