Predicting synchronous firing of large neural populations from sequential recordings

PLoS Comput Biol. 2021 Jan 28;17(1):e1008501. doi: 10.1371/journal.pcbi.1008501. eCollection 2021 Jan.

Abstract

A major goal in neuroscience is to understand how populations of neurons code for stimuli or actions. While the number of neurons that can be recorded simultaneously is increasing at a fast pace, in most cases these recordings cannot access a complete population: some neurons that carry relevant information remain unrecorded. In particular, it is hard to simultaneously record all the neurons of the same type in a given area. Recent progress have made possible to profile each recorded neuron in a given area thanks to genetic and physiological tools, and to pool together recordings from neurons of the same type across different experimental sessions. However, it is unclear how to infer the activity of a full population of neurons of the same type from these sequential recordings. Neural networks exhibit collective behaviour, e.g. noise correlations and synchronous activity, that are not directly captured by a conditionally-independent model that would just put together the spike trains from sequential recordings. Here we show that we can infer the activity of a full population of retina ganglion cells from sequential recordings, using a novel method based on copula distributions and maximum entropy modeling. From just the spiking response of each ganglion cell to a repeated stimulus, and a few pairwise recordings, we could predict the noise correlations using copulas, and then the full activity of a large population of ganglion cells of the same type using maximum entropy modeling. Remarkably, we could generalize to predict the population responses to different stimuli with similar light conditions and even to different experiments. We could therefore use our method to construct a very large population merging cells' responses from different experiments. We predicted that synchronous activity in ganglion cell populations saturates only for patches larger than 1.5mm in radius, beyond what is today experimentally accessible.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • Computational Biology
  • Models, Neurological*
  • Nerve Net* / cytology
  • Nerve Net* / physiology
  • Neurons / physiology*
  • Rats
  • Retinal Ganglion Cells / physiology

Grants and funding

This work was supported by ANR TRAJECTORY (to OM), by the European Union’s Horizon 2020 research and innovation programme (Human Brain Project SGA2) under grant agreement No. 785907 (to OM), a grant from AVIESAN-UNADEV (to OM). This work was completed with the support of the Programme Investissements d’Avenir IHU FOReSIGHT (ANR-18-IAHU-01, to OM and UF), by the French State program Investissements d’Avenir managed by the Agence Nationale de la Recherche [LIFESENSES: ANR-10-LABX-65] (to OM). and by the program ‘`DIM cerveau et pensée" from the region Ile-de-France (to SD). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.