Homeostasis of a representational map in the neocortex

Abstract

SummaryCortical function and the processing of sensory stimuli is remarkably robust against the continuous loss of neurons during aging, but also accelerated loss during prodromal stages of neurodegeneration1, 2. Population activity of neurons in sensory cortices builds a representation of the environment in form of a map that is structured in an informative way for guiding behavior. Here, we used the mouse auditory cortex as a model and probed the robustness of a representational map against the removal functionally characterized neurons. Specifically, we tested in how far the structure of the representational map is safeguarded by homeostatic network mechanisms. We combined longitudinal two-photon calcium imaging of population responses evoked by a diverse set of sound stimuli in the mouse auditory cortex with a targeted microablation of individual, functionally characterized neurons. Unilateral microablation of 30 - 40 selected sound-responsive layer 2/3 neurons led to a temporary collapse of the representational map that showed a subsequent recovery. At the level of individual neurons, we observed that the recovery was predominantly driven by neurons that were unresponsive to the sounds before microablation and gained responsiveness during the time course of several days. The remodeling of the spared network was mediated by a shift of the distribution of tuning curves towards the ablated neurons and was accompanied by a shift in the excitation/inhibition balance. Together, our findings provide a link between the plasticity of individual neurons and the population dynamics of sensory representations mediating robustness of cortical function. The dynamic reconstitution of the structure of activity patterns evoked by sensory stimuli despite a permanent loss of neurons in the network demonstrates a homeostatic maintenance of sensory representations in the neocortex.