Sensory experience steers representational drift in mouse visual cortex

• Published in: Nature communications Vol. 15; no. 1; pp. 9153 - 13
• Main Authors: Bauer, Joel, Lewin, Uwe, Herbert, Elizabeth, Gjorgjieva, Julijana, Schoonover, Carl E., Fink, Andrew J. P., Rose, Tobias, Bonhoeffer, Tobias, Hübener, Mark
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 23-10-2024; Nature Publishing Group; Nature Portfolio
• Subjects: 14; 14/69; 631/378/116/1925; 631/378/2591; 631/378/2613/1875; Animals; Behavior; Brain research; Calcium - metabolism; Calcium imaging; Confidence intervals; Drift; Female; Goggles; Hebbian plasticity; Humanities and Social Sciences; Information processing; Life sciences; Mice; Mice, Inbred C57BL; Models, Neurological; multidisciplinary; Neural plasticity; Neuroimaging; Neuronal Plasticity - physiology; Neurons; Neurons - physiology; Neurosciences; Orientation - physiology; Orientation behavior; Photic Stimulation; Plasticity; Preferred orientation; Primary Visual Cortex - physiology; Science; Science (multidisciplinary); Sensory evaluation; Somatosensory cortex; Statistics; Synapses; Synapses - physiology; Synaptic plasticity; Visual cortex; Visual Cortex - physiology; Visual observation; Visual Perception - physiology; Visual plasticity; Visual stimuli; Volatility
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-53326-x

Representational drift—the gradual continuous change of neuronal representations—has been observed across many brain areas. It is unclear whether drift is caused by synaptic plasticity elicited by sensory experience, or by the intrinsic volatility of synapses. Here, using chronic two-photon calcium imaging in primary visual cortex of female mice, we find that the preferred stimulus orientation of individual neurons slowly drifts over the course of weeks. By using cylinder lens goggles to limit visual experience to a narrow range of orientations, we show that the direction of drift, but not its magnitude, is biased by the statistics of visual input. A network model suggests that drift of preferred orientation largely results from synaptic volatility, which under normal visual conditions is counteracted by experience-driven Hebbian mechanisms, stabilizing preferred orientation. Under deprivation conditions these Hebbian mechanisms enable adaptation. Thus, Hebbian synaptic plasticity steers drift to match the statistics of the environment.
Neural mechanisms underlying representational drift are not fully understood. Here authors report that the preferred orientation of mouse visual cortex neurons drifts over time. Altering visual experience does not change drift magnitude, but rather its direction, such that neurons’ tuning matches the statistics of the environment.