Rapid Encoding of New Memories by Individual Neurons in the Human Brain

Matias J Ison,Rodrigo Quian Quiroga,Itzhak Fried

doi:10.1016/j.neuron.2015.06.016

Matias J Ison, Rodrigo Quian Quiroga + Show 1 more

Open Access

https://doi.org/10.1016/j.neuron.2015.06.016

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Abstract

SummaryThe creation of memories about real-life episodes requires rapid neuronal changes that may appear after a single occurrence of an event. How is such demand met by neurons in the medial temporal lobe (MTL), which plays a fundamental role in episodic memory formation? We recorded the activity of MTL neurons in neurosurgical patients while they learned new associations. Pairs of unrelated pictures, one of a person and another of a place, were used to construct a meaningful association modeling the episodic memory of meeting a person in a particular place. We found that a large proportion of responsive MTL neurons expanded their selectivity to encode these specific associations within a few trials: cells initially responsive to one picture started firing to the associated one but not to others. Our results provide a plausible neural substrate for the inception of associations, which are crucial for the formation of episodic memories.

Highlights

Neuroimaging investigations in humans and behavioral studies of neurological patients have substantiated the importance of the medial temporal lobe (MTL) for episodic memories (Davachi, 2006; Eichenbaum, 2004; Eichenbaum et al, 2007; Moscovitch, 1994; Squire et al, 2004; Tulving, 2002)
Neurophysiological and lesion studies in animals have shown that the MTL is involved in the encoding of associations (Bunsey and Eichenbaum, 1996; Day et al, 2003; Kahana et al, 2008; Sakai and Miyashita, 1991; Wirth et al, 2003), which is a key mechanism for episodic memory formation
Firing Patterns of Single Cells during Learning In 14 patients, who participated in 25 experimental sessions, we recorded the activity of multiple single neurons using electrodes implanted in the MTL for clinical reasons

Summary

Introduction

Neuroimaging investigations in humans and behavioral studies of neurological patients have substantiated the importance of the medial temporal lobe (MTL) for episodic memories (Davachi, 2006; Eichenbaum, 2004; Eichenbaum et al, 2007; Moscovitch, 1994; Squire et al, 2004; Tulving, 2002). Neurophysiological and lesion studies in animals have shown that the MTL is involved in the encoding of associations (Bunsey and Eichenbaum, 1996; Day et al, 2003; Kahana et al, 2008; Sakai and Miyashita, 1991; Wirth et al, 2003), which is a key mechanism for episodic memory formation. Human studies have not addressed episodic memory formation at the single neuron level. On the other hand, have relied on extensive reward-driven training with numerous repetitions of non-natural stimuli, offering a limited account on how single exposures to natural stimuli can give rise to the rapid encoding of new episodic memories. In order to gain such evidence, we combined the ability to analyze trial-by-trial changes in the robust firing of highly selective MTL neurons (Quian Quiroga et al, 2005, 2008, 2009), with the rapid facility that humans have for learning complex associations and consciously declare them

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