Exact neural mass model for synaptic-based working memory

PLoS Comput Biol. 2020 Dec 15;16(12):e1008533. doi: 10.1371/journal.pcbi.1008533. eCollection 2020 Dec.

Abstract

A synaptic theory of Working Memory (WM) has been developed in the last decade as a possible alternative to the persistent spiking paradigm. In this context, we have developed a neural mass model able to reproduce exactly the dynamics of heterogeneous spiking neural networks encompassing realistic cellular mechanisms for short-term synaptic plasticity. This population model reproduces the macroscopic dynamics of the network in terms of the firing rate and the mean membrane potential. The latter quantity allows us to gain insight of the Local Field Potential and electroencephalographic signals measured during WM tasks to characterize the brain activity. More specifically synaptic facilitation and depression integrate each other to efficiently mimic WM operations via either synaptic reactivation or persistent activity. Memory access and loading are related to stimulus-locked transient oscillations followed by a steady-state activity in the β-γ band, thus resembling what is observed in the cortex during vibrotactile stimuli in humans and object recognition in monkeys. Memory juggling and competition emerge already by loading only two items. However more items can be stored in WM by considering neural architectures composed of multiple excitatory populations and a common inhibitory pool. Memory capacity depends strongly on the presentation rate of the items and it maximizes for an optimal frequency range. In particular we provide an analytic expression for the maximal memory capacity. Furthermore, the mean membrane potential turns out to be a suitable proxy to measure the memory load, analogously to event driven potentials in experiments on humans. Finally we show that the γ power increases with the number of loaded items, as reported in many experiments, while θ and β power reveal non monotonic behaviours. In particular, β and γ rhythms are crucially sustained by the inhibitory activity, while the θ rhythm is controlled by excitatory synapses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cerebral Cortex / cytology
  • Cerebral Cortex / physiology
  • Humans
  • Memory, Short-Term*
  • Models, Neurological*
  • Neuronal Plasticity
  • Neurons / physiology
  • Synapses / physiology*

Grants and funding

AT received financial support by the Excellence Initiative I-Site Paris Seine (Grant No ANR-16-IDEX-008), by the Labex MME-DII (Grant No ANR-11-LBX-0023-01) and by the ANR Project ERMUNDY (Grant No ANR-18-CE37-0014), all part of the French programme “Investissements d’Avenir”. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.