Characterizing the nonlinear structure of shared variability in cortical neuron populations using latent variable models

TL;DR

This paper introduces nonlinear latent variable models to analyze shared variability in neural populations, revealing different structures in anesthetized V1 and awake prefrontal cortex, advancing understanding of neural response variability.

Contribution

The paper develops two nonlinear latent variable models, including a general model and the Generalized Affine Model, to characterize shared neural variability without restrictive assumptions.

Findings

V1 activity is best described by an affine model with additive and multiplicative latent variables.

Prefrontal cortex activity exhibits more complex nonlinearities.

Models effectively capture population response variability across different brain regions.

Abstract

Sensory neurons often have variable responses to repeated presentations of the same stimulus, which can significantly degrade the stimulus information contained in those responses. This information can in principle be preserved if variability is shared across many neurons, but depends on the structure of the shared variability and its relationship to sensory encoding at the population level. The structure of this shared variability in neural activity can be characterized by latent variable models, although they have thus far typically been used under restrictive mathematical assumptions. Here we introduce two nonlinear latent variable models for analyzing large-scale neural recordings. We first present a general nonlinear latent variable model that is agnostic to the stimulus tuning properties of the individual neurons, and is hence well suited for exploring neural populations whose tuning properties are not well characterized. This motivates a second class of model, the Generalized Affine Model, which simultaneously determines each neuron's stimulus selectivity and a set of latent variables that modulate these stimulus-driven responses both additively and multiplicatively. While these approaches can detect very general nonlinear relationships in shared neural variability, we find that neural activity recorded in anesthetized primary visual cortex (V1) is best described by a single additive and single multiplicative latent variable, i.e. an `affine model'. In contrast, application of the same models to recordings in awake macaque prefrontal cortex discover more general nonlinearities to compactly describe the population response variability. These results thus demonstrate how nonlinear latent variable models can be used to describe population response variability, and suggest that a range of methods is necessary to study different brain regions under different experimental conditions.