Abstract

Auditory recognition memory in non-human primates differs from recognition memory in other sensory systems. Monkeys learn the rule for visual and tactile delayed matching-to-sample within a few sessions, and then show one-trial recognition memory lasting 10–20 min. In contrast, monkeys require hundreds of sessions to master the rule for auditory recognition, and then show retention lasting no longer than 30–40 s. Moreover, unlike the severe effects of rhinal lesions on visual memory, such lesions have no effect on the monkeys' auditory memory performance. The anatomical pathways for auditory memory may differ from those in vision. Long-term visual recognition memory requires anatomical connections from the visual association area TE with areas 35 and 36 of the perirhinal cortex (PRC). We examined whether there is a similar anatomical route for auditory processing, or that poor auditory recognition memory may reflect the lack of such a pathway. Our hypothesis is that an auditory pathway for recognition memory originates in the higher order processing areas of the rostral superior temporal gyrus (rSTG), and then connects via the dorsolateral temporal pole to access the rhinal cortex of the medial temporal lobe. To test this, we placed retrograde (3% FB and 2% DY) and anterograde (10% BDA 10,000 mW) tracer injections in rSTG and the dorsolateral area 38DL of the temporal pole. Results showed that area 38DL receives dense projections from auditory association areas Ts1, TAa, TPO of the rSTG, from the rostral parabelt and, to a lesser extent, from areas Ts2-3 and PGa. In turn, area 38DL projects densely to area 35 of PRC, entorhinal cortex (EC), and to areas TH/TF of the posterior parahippocampal cortex. Significantly, this projection avoids most of area 36r/c of PRC. This anatomical arrangement may contribute to our understanding of the poor auditory memory of rhesus monkeys.

Highlights

  • Primates have a surprisingly poor ability to store auditory sensory information into long-term memory (Fritz et al, 2005; Scott et al, 2012)

  • That about 70% of the total temporal input to area 38 into dorsolateral (38DL) of the dorsolateral temporal pole originated in the auditory processing areas of area Ts1 (Ts1) and area area Tpt (Tpt) (TAa) of the rostral superior temporal gyrus (STG) and area RTL of the rostral superior temporal plane (STP)

  • Our results show that the areas that form the rostral STG project mainly to area 38DL, which in turn projects to entorhinal cortex (EC), area 35 of perirhinal cortex (PRC), and areas area TH (TH) and area TF (TF) of Parahippocampal Cortex (PHC)

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Summary

Introduction

Primates have a surprisingly poor ability to store auditory sensory information into long-term memory (Fritz et al, 2005; Scott et al, 2012). This contrasts with their remarkable capability to form long-term visual and tactile memories (Murray and Mishkin, 1984; Goulet and Murray, 2001). As tested with the delayed nonmatching to sample (DNMS) task, visual recognition memory is learned quickly and displays a high level performance at long delays or with many items to remember. As noted in our earlier paper of this series (Muñoz-López et al, 2010), comparison of the visual, tactile, and auditory anatomical pathways might provide us with an explanation as to the difference in recognition memory ability

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