Forward processing of long-term associative memory in monkey inferotemporal cortex.

Abstract

The macaque inferotemporal (IT) cortex, which serves as the storehouse of visual long-term memory, consists of two distinct but mutually interconnected areas: area TE (TE) and area 36 (A36). In the present study, we tested whether memory encoding is put forward at this stage, i.e., whether association between the representations of different but semantically linked objects proceeds forward from TE to A36. To address this question, we trained monkeys in a pair-association (PA) memory task, after which single-unit activities were recorded from TE and A36 during PA trials. Neurons in both areas showed stimulus-selective cue responses (347 in TE, 76 in A36; "cue-selective neurons") that provided, at the population level, mnemonic linkage between the paired associates. The percentage of neurons in which responses to the paired associates were significantly (p < 0.01) correlated at the single-neuron level ("pair-coding neuron") dramatically increased from TE (4.9% of the cue-selective neurons) to A36 (33%). The pair-coding neurons in A36 were further separable into Type1 (68%) and Type2 (32%) on the basis of their initial transient responses after cue stimulus presentation. Type1 neurons, but not Type2 neurons, began to encode association between paired stimuli as soon as they exhibited stimulus selectivity. Thus, the representation of long-term memory encoded by Type1 neurons in A36 is likely substantiated without feedback input from other higher centers. Therefore, we conclude that association between the representations of the paired associates proceeds forward at this critical step within IT cortex, suggesting selective convergence onto a single A36 neuron from two TE neurons that encode separate visual objects.