The quality and complexity of pairwise maximum entropy models for large cortical populations

PLoS Comput Biol. 2024 May 2;20(5):e1012074. doi: 10.1371/journal.pcbi.1012074. eCollection 2024 May.

Abstract

We investigate the ability of the pairwise maximum entropy (PME) model to describe the spiking activity of large populations of neurons recorded from the visual, auditory, motor, and somatosensory cortices. To quantify this performance, we use (1) Kullback-Leibler (KL) divergences, (2) the extent to which the pairwise model predicts third-order correlations, and (3) its ability to predict the probability that multiple neurons are simultaneously active. We compare these with the performance of a model with independent neurons and study the relationship between the different performance measures, while varying the population size, mean firing rate of the chosen population, and the bin size used for binarizing the data. We confirm the previously reported excellent performance of the PME model for small population sizes N < 20. But we also find that larger mean firing rates and bin sizes generally decreases performance. The performance for larger populations were generally not as good. For large populations, pairwise models may be good in terms of predicting third-order correlations and the probability of multiple neurons being active, but still significantly worse than small populations in terms of their improvement over the independent model in KL-divergence. We show that these results are independent of the cortical area and of whether approximate methods or Boltzmann learning are used for inferring the pairwise couplings. We compared the scaling of the inferred couplings with N and find it to be well explained by the Sherrington-Kirkpatrick (SK) model, whose strong coupling regime shows a complex phase with many metastable states. We find that, up to the maximum population size studied here, the fitted PME model remains outside its complex phase. However, the standard deviation of the couplings compared to their mean increases, and the model gets closer to the boundary of the complex phase as the population size grows.

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Cerebral Cortex / physiology
  • Computational Biology
  • Computer Simulation
  • Entropy*
  • Models, Neurological*
  • Neurons* / physiology

Grants and funding

Research Council of Norway Centre of Neural Computation, grant number 223262; Research Council of Norway NORBRAIN, grant number 295721; The Kavli Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.