Homeostasis of a representational map in the neocortex

Abstract

Cortical function in general and the processing of sensory stimuli in particular are remarkably robust against the continuous loss of neurons during aging, and even the accelerated loss during prodromal stages of neurodegeneration1,2. Population activity of neurons in sensory cortices represents the environment in form of a map, which is structured in an informative way for guiding behavior. Here, we used the mouse auditory cortex as a model and tested in how far the structure of the representational map is protected by homeostatic network mechanisms against the removal of neurons. We combined longitudinal two-photon calcium imaging of population responses evoked by a diverse set of sound stimuli with a targeted microablation of functionally characterized neurons. Unilateral microablation of 30 - 40 selected highly sound-responsive neurons in layer 2/3 led to a temporary disturbance of the representational map in the spared population that, however, recovered in subsequent days. At the level of individual neurons, we observed that the recovery of the spared network was predominantly driven by neurons unresponsive to the sounds before microablation which strengthened the correlation structure of the local network after gaining responsiveness. In contrast, selective microablation of inhibitory neurons induced a prolonged disturbance of the representational map that was primarily characterized by a destabilization of sound responses across trials. Together, our findings provide a link between the tuning and plasticity of individual neurons and the structure of a representational map at the population level which reveals homeostatic network mechanisms safeguarding sensory processing in neocortical circuits.