PREY CAPTURE LEARNING DRIVES CRITICAL PERIOD-SPECIFIC PLASTICITY IN MOUSE BINOCULAR VISUAL CORTEX

To thrive in their environment, animal must constantly adapt and learn. This fundamental ability relies on the brain’s capacity to adjust its circuitry and function to ensure optimal behavioral outcomes, and the underlying processes have been intensively studied. While brain plasticity persists through life, it is especially high during development and decreases with age. Despite extensive research on adult learning-induced plasticity and developmental plasticity, how they interact remains comparatively poorly known: i.e., how learning reshapes circuitry and function during development, when neuronal networks are particularly dynamic, and how this remodeling may differ from the more stable adult brain.
Here, we started addressing this fundamental question using prey capture learning, a rich, ethologically relevant and vision-dependent paradigm, combined with chronic in vivo two-photon imaging, chemogenetics and pharmacology. We show that prey capture learning depends on the primary visual cortex (V1) in critical-period mice, and drives an enhancement of visual function and a profound rewiring of the circuitry of binocular V1, leading to improved discrimination of moving visual stimuli and increased excitatory connectivity and dynamics. This structural and functional remodeling is stabilized through stabilized through non-Hebbian, tumor necrosis factor (TNF) α-dependent mechanisms. Strikingly, and in contrast to a large literature on adult learning, we saw no morphological changes in adult hunters, strongly suggesting that prey capture learning-induced plasticity is mediated by mechanisms specific to the critical period.
Our findings emphasize the particularity of critical-period plasticity and demonstrate that learning during critical periods can remodel brain circuitry and function through distinct mechanisms.