Unitized representation of paired objects in area 35 of the macaque perirhinal cortex.

The perirhinal cortex, which is critical for long-term stimulus-stimulus associative memory, consists of two cytoarchitectonically distinct subdivisions: area 35 (A35) and area 36 (A36). Previous electrophysiological studies suggested that macaque A36 is involved in both association and retrieval processes during a visual pair-association task. However, the neuronal properties of macaque A35 have never been examined because A35 is located in a very narrow region, which makes it difficult to systematically record single-unit activity from there. In the present study, we overcame this technical difficulty for targeting A35 by combining magnetic resonance imaging-guided in-vivo localization with postmortem histological localization. This two-track approach enabled us to record from 181 A35 neurons in two macaque monkeys while they performed a pair-association task. Among these neurons, 64 showed stimulus-selective responses during the cue period (cue-selective neurons), whereas 18 did during the delay period (delay-selective neurons). As in A36, the responses of cue-selective neurons in A35 to paired associates were correlated. In both areas, these correlations were stronger in neurons showing delay selectivity than in those without delay selectivity. Notably, delay-selective neurons in A35 responded similarly to the optimal stimulus and its paired associate, whereas delay-selective neurons in A36 discriminated between them. However, these neurons in both areas discriminated the primary pair, consisting of the optimal stimulus and its paired associate, from other pairs, indicating that selectivity across pairs was maintained between the two areas. These results suggest that delay-selective neurons in A35 represent these paired stimuli as a single unitized item rather than two associated items.