When monkeys perform a delayed match-to-sample task, some neurons in the anterior inferotemporal cortex show sustained activity following the presentation of specific visual stimuli, typically only those that are shown repeatedly. When sample stimuli are shown in a fixed temporal order, the few images that evoke delay activity in a given neuron are often neighboring stimuli in the sequence, suggesting that this delay activity may be the neural correlate of associative long-term memory. Here we report that stimulus-selective sustained activity is also evident following the presentation of the test stimulus in the same task. We use a neural network model to demonstrate that persistent stimulus-selective activity across the intertrial interval can lead to similar mnemonic representations (distributions of delay activity across the neural population) for neighboring visual stimuli. Thus, inferotemporal cortex may contain neural machinery for generating long-term stimulus–stimulus associations.
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We thank Gadi Goelman for technical support in the MRI testing, Michail Dvorkin for development of some of the data analysis tools and Nicolas Brunel for help in reproducing his simulations. Robert Shapley pointed out the possible relevance of the connection between prosopagnosia and navigation problems in patients with temporal-lobe lesions. Daniel Amit and Shaul Hochstein commented on earlier versions of the manuscript. This work was supported by grants from the Israel Academy of Science and Israel National Institute of Psychobiology (V.Y.) and a McDonnel-Pew grant for cognitive neuroscience (E.Z).
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