Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Sensory and Memory Processing in Temporal Cortex



Science 18 March 2011:  Vol. 331 no. 6023 pp. 1443-1447

Reversal of Interlaminar Signal Between Sensory and Memory Processing in Monkey Temporal Cortex

Daigo Takeuchi,  Toshiyuki Hirabayashi,  Keita Tamura, and  Yasushi Miyashita

Department of Physiology, University of Tokyo School of Medicine, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.


The primate temporal cortex implements visual long-term memory. However, how its interlaminar circuitry executes cognitive computations is poorly understood. Using linear-array multicontact electrodes, we simultaneously recorded unit activities across cortical layers in the perirhinal cortex of macaques performing a pair-association memory task. Cortical layers were estimated on the basis of current source density profiles with histological verifications, and the interlaminar signal flow was determined with cross-correlation analysis between spike trains. During the cue period, canonical “feed-forward” signals flowed from granular to supragranular layers and from supragranular to infragranular layers. During the delay period, however, the signal flow reversed to the “feed-back” direction: from infragranular to supragranular layers. This reversal of signal flow highlights how the temporal cortex differentially recruits its laminar circuits for sensory and mnemonic processing.

The primate inferotemporal cortex locates at the final stage of the ventral visual pathway and serves as a storehouse for visual long-term memory. Previous studies have demonstrated neuronal activity related to presented visual objects and retrieved images at the single-neuron level, but the underlying network dynamics remain to be understood. Evidence from the primary sensory cortices suggests that local circuits extending across cortical layers are crucially involved in sensory processing. This raises questions about how the interlaminar circuitry in the inferotemporal cortex is differentially recruited to process presented objects and to retrieve visual long-term memory.

We used two strategies to investigate interlaminar signal flow in awake behaving monkeys. First, we used current source density (CSD) analysis as a tool for layer estimation in each electrode penetration; CSD reflects the gross transmembrane currents in the local neuronal ensemble and is used to estimate the cortical layers that receive afferent inputs. Second, we used cross-correlation analysis of spike trains to infer the functional interactions across cortical layers; asymmetry or peak lag of the cross-correlogram (CCG) reflects the direction of functional connectivity between neurons.

Two monkeys were trained to perform a pair-association task, in which they had to retrieve the learned paired associate in response to the presented cue stimulus. We recorded single- and multi-unit activities and local field potentials (LFPs) by inserting linear-array multicontact electrodes (16 or 24 contacts with spacing of 150 or 100 μm, respectively) vertically. Postmortem histological analyses confirmed that the earliest current sink evoked by cue stimuli consistently corresponded to the granular layer.

The present study demonstrated that canonical feed-forward signal flow across cortical layers during sensory coding reverse to the feed-back direction during memory retrieval phase, which suggests flexible recruitment of interlaminar connectivity depending on the cognitive demands in the monkey association cortices. We used CSD analysis to estimate cortical layers, and the observed stimulus-evoked CSD profiles were quite similar to those in the primary sensory cortices.

A recent study in the rat primary auditory cortex demonstrated that the direction of interlaminar signal flow depends on the cortical “state”: Sensory-evoked responses were initiated in the thalamorecipient layers and then propagated to the superficial and deep layers, whereas in spontaneously active “up-states,” neuronal activity was initiated in the deep layers and then propagated to the superficial layers. These state-dependent changes in the interlaminar signal flows in rats are consistent with our results obtained in monkeys performing a memory task. Together, these findings highlight the flexibility of cortical laminar circuits. Further experiments will be needed to determine whether such flexible interlaminar connectivity is also implemented and used in other cortical areas for other cognitive demands.

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