Two kinds of memory signals in neurons of the human hippocampus - PubMed (original) (raw)

Two kinds of memory signals in neurons of the human hippocampus

Zhisen J Urgolites et al. Proc Natl Acad Sci U S A. 2022.

Abstract

Prior studies of the neural representation of episodic memory in the human hippocampus have identified generic memory signals representing the categorical status of test items (novel vs. repeated), whereas other studies have identified item specific memory signals representing individual test items. Here, we report that both kinds of memory signals can be detected in hippocampal neurons in the same experiment. We recorded single-unit activity from four brain regions (hippocampus, amygdala, anterior cingulate, and prefrontal cortex) of epilepsy patients as they completed a continuous recognition task. The generic signal was found in all four brain regions, whereas the item-specific memory signal was detected only in the hippocampus and reflected sparse coding. That is, for the item-specific signal, each hippocampal neuron responded strongly to a small fraction of repeated words, and each repeated word elicited strong responding in a small fraction of neurons. The neural code was sparse, pattern-separated, and limited to the hippocampus, consistent with longstanding computational models. We suggest that the item-specific episodic memory signal in the hippocampus is fundamental, whereas the more widespread generic memory signal is derivative and is likely used by different areas of the brain to perform memory-related functions that do not require item-specific information.

Keywords: episodic memory; human hippocampus; single-unit activity; sparsely coded memory.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.

Fig. 1.

Number of neurons that exhibited generic memory signals (repeated vs. novel) in the hippocampus, amygdala, prefrontal cortex, and anterior cingulate. In each of the four regions, the total number of neurons exhibiting a generic memory signal exceeded the number expected by chance, using an alpha level of 0.05 (the dotted line) based on the total number of neurons recorded per region. For example, 38 neurons in the hippocampus exhibited a generic memory signal, which was significantly above the 19.9 expected by chance.

Fig. 2.

Fig. 2.

QQ plots of the normalized spike counts in response to novel words (_x_-axis) and repeated words (_y_-axis) for the hippocampus (A and B), amygdala (C and D), prefrontal cortex (E and F), and anterior cingulate (G and H). Top panels plot 100% of the data for each region (hippocampus: 77,431 recordings; amygdala: 65,219 recordings; prefrontal: 47,399 recordings; anterior cingulate: 62,205 recordings). The dark symbols indicate high-density data points, representing thousands of recordings; the light symbols indicate low-density data points, representing a very small percentage of recordings. Bottom panels show the same data after removing the 0.25% recordings with the highest spike counts from both the novel-word and repeated-word distributions. For the hippocampus, the points fell mostly along the diagonal line but exhibited a sharp upward deflection (A), indicating that some neurons responded strongly to some repeated words. After removing the top 0.25% of the data, the upward deflection for the hippocampus disappeared (B), indicating that only a very small percentage of neurons spiked more in response to repeated words than novel words. By contrast, the plots for the other three regions did not exhibit similar upward deflections. Thus, the activity pattern signaling episodic memory was identified only in the hippocampus.

References

    1. Squire L. R., Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195–231 (1992). -PubMed
    1. Eichenbaum H., Cohen N. J., From Conditioning to Conscious Recollection: Memory Systems of the Brain (Oxford University Press, 2004).
    1. Tulving E., “Episodic and semantic memory” in Organization of Memory, Tulving E., Donaldson W., Eds. (Academic Press, New York, 1972), pp. 381–403.
    1. Shepard R. N., Teghtsoonian M., Retention of information under conditions approaching a steady state. J. Exp. Psychol. 62, 302–309 (1961). -PubMed
    1. Squire L. R., Wixted J. T., Clark R. E., Recognition memory and the medial temporal lobe: a new perspective. Nat. Rev. Neurosci. 8, 872–883 (2007). -PMC -PubMed

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