Experience with moving visual stimuli drives the early development of cortical direction selectivity

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Abstract
Neural circuits in the visual cortex are immature at birth, and require exposure to visual stimuli to form the connections and selectivity of the mature visual system. To date, just how stimulus driven neural activity guides the emergence of properties such as direction selectivity has been unclear. Li et al. now track this process with a combination of intrinsic and two-photon calcium imaging in visually naive ferrets. After exposing the animals to stimuli moving along one single axis of motion, they find that selectivity for those directions emerges rapidly as well as the local organization of direction preference between neighbouring cells. Neural circuits in the visual cortex are immature at birth, and require exposure to visual stimuli to form the connections and selectivity of the mature visual system. It has been unclear how stimulus-driven neural activity guides the emergence of properties such as direction selectivity. This paper tracks this process with a combination of intrinsic and two-photon calcium imaging in visually naive ferrets. After exposing the animals to stimuli moving along one single axis of motion, it is found that selectivity for those directions emerges rapidly as well as the local organization of direction preference between neighbouring cells. The onset of vision occurs when neural circuits in the visual cortex are immature, lacking both the full complement of connections1,2 and the response selectivity that defines functional maturity3,4. Direction-selective responses are particularly vulnerable to the effects of early visual deprivation, but it remains unclear how stimulus-driven neural activity guides the emergence of cortical direction selectivity. Here we report observations from a motion training protocol that allowed us to monitor the impact of experience on the development of direction-selective responses in visually naive ferrets. Using intrinsic signal imaging techniques, we found that training with a single axis of motion induced the rapid emergence of direction columns that were confined to cortical regions preferentially activated by the training stimulus. Using two-photon calcium imaging techniques, we found that single neurons in visually naive animals exhibited weak directional biases and lacked the strong local coherence in the spatial organization of direction preference that was evident in mature animals. Training with a moving stimulus, but not with a flashed stimulus, strengthened the direction-selective responses of individual neurons and preferentially reversed the direction biases of neurons that deviated from their neighbours. Both effects contributed to an increase in local coherence. We conclude that early experience with moving visual stimuli drives the rapid emergence of direction-selective responses in the visual cortex.

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