Mnemonic Responses of Single Units Recorded from Monkey Inferotemporal Cortex, Accessed via Transcommissural Versus Direct Pathways: A Dissociation between Unit Activity and Behavior

Abstract

Three macaques were trained on a task in which a sequence of single visual images was presented serially, and the monkeys signaled whether the image was a new or a repeated one. The optic chiasm and splenium of the corpus callosum were transected, leaving the anterior commissure as the only path for cortical interhemispheric transfer. Images were presented to only one eye at a time. Re-presentations of images to the same eye were recognized correctly in Ͼ95% of trials. A robust stimulus-specific adaptation (i.e., a reduced response to a repeated image) was seen in the population of single units recorded from inferotemporal cortex during these same trials. When an interhemispheric transfer was demanded of the animals (i.e., the re-presentation was made to the other eye), recognition performance was somewhat reduced, to 86% correct. Interestingly, in this situation the stimulus-specific adaptation disappeared completely. The disappearance occurred regardless of whether the transfer direction was from the hemisphere ipsilateral to the recording site to the hemisphere contralateral to the recording site, or vice versa. Thus, stimulusspecific adaptation in inferotemporal cortex units is not required for recognition. Key words: visual memory; extrastriate cortex; inferotemporal cortex; macaque; memory; vision; interhemispheric relationsInferotemporal cortex (IT) of the monkey appears to play an important role in visual memory processes. Severe memory disturbances were found when IT was damaged either permanently (Mishkin, 1966(Mishkin, , 1982Wilson et al., 1972;Dean, 1974;Delacour, 1977;Horel et al., 1987) or reversibly (Fuster et al., 1981;Horel et al., 1987). Memory processes are reflected in the single-unit activity recorded in IT (Brown et al., 1987;Miyashita and Chang, 1988;Miller and Desimone, 1994). One of the most evident and widely studied is stimulus-specific adaptation (SSA). This has also been termed "decremental response" (Brown et al., 1987) and "adaptive mnemonic filtering" (Miller and Desimone, 1994). In this phenomenon, the first presentation of an unfamiliar visual stimulus to a monkey generates a stronger response than the same stimulus when it is re-presented (Baylis and Rolls, 1987;Brown et al., 1987;Rolls et al., 1989;Miller et al., 1991;Riches et al., 1991;Fahy et al., 1993;Li et al., 1993; Ringo, 1993, 1994).SSA has recently been reviewed (Ringo, 1996). We were interested in experimental manipulation, which would transform this single-unit memory effect. Such a transformation, with a simultaneous measure of behavioral memory performance, would allow an experimental (rather than a correlational) investigation of the neural basis of a mnemonic behavior. To this end, we took advantage of the partially "split-brain" preparation to channel the sensory information coming into IT via two widely separated routes. The partial split-brain was created by transecting the optic chiasm and corpus callosum, leaving an intact anterior commissure (AC). In monkeys, the AC is fully capable of transferring visual ...

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