Environmental novelty modulates rapid cortical plasticity during navigation

Abstract

We enter a new room and can orient ourselves in a matter of seconds. Similarly, when mice enter a new environment, they learn the location of behaviorally relevant objects and places in just a few trials. In the brain, spatial representations in the form of position-correlated neural activity emerge on a similar timescale in multiple regions. This phenomenon has been most intensively studied in the hippocampus, and the medial entorhinal cortex (MEC), traditionally seen as key brain regions for spatial learning and navigation in mammals. However, recent evidence shows that activity throughout cortical areas, including primary visual cortex (V1), higher visual areas, and retrosplenial cortex (RSC) is influenced by spatial location, and is critical for visually-guided spatial navigation.

However, the role of plasticity in building spatial representations in cortex, and how experience modulates this process, are not well understood.

To investigate the role of plasticity in the formation of spatial representations in cortex, we combined two-photon calcium imaging with two-photon holographic stimulation to perturb neural activity in behaving animals with single cell precision. We show that targeted activation of individual layer 2/3 neurons rapidly biased neural activity towards stimulation-paired locations in novel, but not familiar, environments. In contrast, RSC layer 5 neurons exhibited stimulation-induced plasticity regardless of environmental familiarity. These findings reveal a layer-specific, experience-dependent modulation of plasticity and offer a framework for how neocortical spatial representations strike a balance between stability of familiar environments with flexibility for continuous updates of relevant context information.

Alex Attinger 

Stanford, Department of Neurobiology 

Alex Attinger is a postdoc in the lab of Prof. Lisa Giocomo at Stanford University. He is interested in how the brain constructs internal models of the world and uses those to make sense of sensory input and guide behavior. He is currently investigating the plasticity of cortical circuits during spatial learning and memory formation by using large-scale neural recordings and optogenetics. His PhD research at FMI Basel revealed how the coupling of sensory and motor experience during development fundamentally shapes visual perception by tuning a cortical circuit that compares feedforward visual input with top-down predictions.

(Giocomo Lab: Visit Lab Website)

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