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

Episodic Memory — Medial Temporal Lobe


Science 5 August 2011:  Vol. 333 no. 6043 pp. 773-776

Integrating ‘What’ and ‘When’ Across the Primate Medial Temporal Lobe

Yuji Naya1, Wendy A. Suzuki1

1Center for Neural Science, New York University, 4 Washington Place, New York, NY 10003, USA.


Episodic memory or memory for the detailed events in our lives is critically dependent on structures of the medial temporal lobe (MTL). A fundamental component of episodic memory is memory for the temporal order of items within an episode. To understand the contribution of individual MTL structures to temporal-order memory, we recorded single-unit activity and local field potential from three MTL areas (hippocampus and entorhinal and perirhinal cortex) and visual area TE as monkeys performed a temporal-order memory task. Hippocampus provided incremental timing signals from one item presentation to the next, whereas perirhinal cortex signaled the conjunction of items and their relative temporal order. Thus, perirhinal cortex appeared to integrate timing information from hippocampus with item information from visual sensory area TE.

Episodic memory, or the ability to mentally reexperience a previous event in one’s life, is formed when individual events or items become bound to the specific temporal context in which the event took place. The human medial temporal lobe (MTL) is critical for episodic memory presumably because of its role in binding individual stimuli or events to their temporal and spatial contexts. Computation models have proposed that cortical association areas signal information about items, parahippocampal regions signal information about items along with their temporal context, whereas hippocampus (HPC) supervises these item-context associations. Consistent with these model predictions, functional magnetic resonance imaging (fMRI) studies in humans report both HPC and parahippocampal activation during tasks of temporal-order memory. Recent neurophysiological studies in the rodent have highlighted the role of HPC in signaling either a particular time within a trial or incremental timing across the entire recording session. However, little is known about the neurophysiological basis of how item and timing information is integrated within MTL. We therefore recorded neural activity from MTL areas and a control visual area as nonhuman primates performed a temporal-order memory task that required encoding of two visual items and their temporal order.

A total of 644 neurons were recorded in the two macaques in entorhinal cortex (ERC) and perirhinal cortex (PRC).

To characterize the temporal dynamics of time cells observed throughout the MTL, we applied a population vector analysis.

These results indicated that, as a population, HPC time cells provide an incremental timing signal that gives an estimate of the relative time from the last cue presentation as well as an estimate of the relative time to the next cue presentation.

Principal component analysis of neuronal activity during the encoding phase also supported the idea of a strong incremental timing signal in HPC and a similar but weaker such signal in ERC.

The present study provides insight about how individual MTL structures may integrate item and timing information (i.e., “what” and “when”) in the service of episodic memory. HPC provides a robust incremental timing signal that may serve to anchor the timing to events within an episode. Consistent with predictions from previous computational models, our data show that PRC neurons integrate time and item information by modulating their stimulus-selective response properties across temporally distinct stimulus presentations. ERC neurons can signal incremental timing information as well as integrate item and time information, albeit at a lower magnitude than HPC or PRC, respectively. We hypothesize that the incremental timing signal in HPC is conveyed to PRC via ERC, where it is integrated with item information from TE and converted into a discrete item-based temporal order signal.

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