Hippocampal Neurogenesis Reduces the Dimensionality of Sparsely Coded Representations to Enhance Memory Encoding.

Anthony J Decostanzo,Tomoki Fukai,Chi Chung Alan Fung

doi:10.3389/fncom.2018.00099

Anthony J Decostanzo, Tomoki Fukai + Show 1 more

Open Access

https://doi.org/10.3389/fncom.2018.00099

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Abstract

Adult neurogenesis in the hippocampal dentate gyrus (DG) of mammals is known to contribute to memory encoding in many tasks. The DG also exhibits exceptionally sparse activity compared to other systems, however, whether sparseness and neurogenesis interact during memory encoding remains elusive. We implement a novel learning rule consistent with experimental findings of competition among adult-born neurons in a supervised multilayer feedforward network trained to discriminate between contexts. From this rule, the DG population partitions into neuronal ensembles each of which is biased to represent one of the contexts. This corresponds to a low dimensional representation of the contexts, whereby the fastest dimensionality reduction is achieved in sparse models. We then modify the rule, showing that equivalent representations and performance are achieved when neurons compete for synaptic stability rather than neuronal survival. Our results suggest that competition for stability in sparse models is well-suited to developing ensembles of what may be called memory engram cells.

Highlights

The model consists of a three-layer network including entorhinal cortical inputs (EC), dentate gyrus (DG), and a CA3 output (Figure 1A)
Our results suggest that the sparseness of the DG is exploited by adult neurogenesis to find lowdimensional contextual representations that enhance memory encoding (Figures 3C,D)
Our results suggest that neuronal or synaptic turnover in sparsely active regions of the brain may embody a novel learning rule that enhances the clustering of associated activity patterns, and thereby memory encoding and retrieval

Summary

Introduction

Since most adult-born neurons rapidly die, it has long been hypothesized that they must compete amongst themselves, and with mature neurons, for survival dependent upon their contribution to behavior (Bergami and Berninger, 2012) Consistent with this notion, newly adult-born cells integrate into the DG in an experience-dependent manner (Kempermann et al, 1997b; Gould et al, 1999; Bergami et al, 2015; Alvarez et al, 2016; Zhuo et al, 2016), and numerous studies have demonstrated that either ablation (Clelland et al, 2009; Sahay et al, 2011), or in vivo silencing of activity (Danielson et al, 2016; Zhuo et al, 2016) or synaptic output (Nakashiba et al, 2012) of these. Similar interventions that silence adult-born cells after learning have shown that retrieval of recent memories is impaired (Gu et al, 2012)

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