Functional Specialization of eye-specific visual pathways into higher visual cortex

The brain is able to construct a visual representation of the world by parallel processing of cortical neurons that prefer increasingly complex stimuli. One way the visual cortex has accomplished parallel processing is by creating functionally organized modules that are tuned to unique features and linking them in multiple processing stages of cortex. For example, primary visual cortex (V1) sends functionally distinct information to higher visual areas (HVAs), which are more specialized in their processing of spatiotemporal information. Inherently coupled to this process is the convergence of eye-specific inputs in visual cortex. Shifting the eye-specific tuning of neurons in primary visual cortex by monocular deprivation in early life is known to disrupt tuning for spatial frequency in adulthood. Combining space and time better characterizes the segregation of HVAs. To begin to understand if eye-specific responses could be linked to tuning properties important for the segregation of HVAs, we characterized eye-specific spatiotemporal tuning of layer 2/3 excitatory cells within the binocular zone of V1 and two HVAs grouped into the putative ventral and dorsal streams, LM and PM, using two-photon GCaMP6s imaging of awake mice. An asymmetry was found at the level of V1, such that responses driven primarily by the contralateral eye were biased towards high spatial frequencies, low speeds, cardinal directions, and were more direction selective than binocular or ipsilateral eye-driven responses. Eye-specific inputs in V1 are tuned to different speeds and also have different degrees of speed tuning, where contralateral eye inputs are more speed tuned than ipsilateral eye inputs. The proportions of eye-specific neurons of LM and PM matched the expected preferences based on eye-specific spatial frequency tuning found at the level of V1. A similar contralateral bias for distinct features, most notably, spatiotemporal tuning, was found within LM and PM, linking neurons with similar eye-specific preferences to their tuning for early feature detectors important for stream specialization. To determine if V1 sends eye-specific functionally distinct information to HVAs, we injected AAV-Syn-GCaMP6s into the binocular zone of V1 and imaged the afferents that targeted either LM or PM. We found that V1 afferents to LM and PM were distinct in their distributions for ocular dominance, suggesting that eye-specific projections from V1 to HVAs contribute to their functional specificity. To determine if the functional specialization of HVAs depend upon eye-specific developmental mechanisms, we deprived mice of visual experience through the contralateral eye (CMD) during the ocular dominance critical period and assessed eye-specific spatiotemporal tuning of V1, LM and PM in adulthood. We found that CMD diminished the functional specificity of V1, LM and PM, resulting in areas without differentiated spatiotemporal preferences. Moreover, the eye-specific functional segregation was also disrupted with CMD. Altogether, our data demonstrates that the maturation of higher visual areas is dependent on proper binocular visual experience and suggests that the functional specialization of eye-specific responses could be an efficient routing mechanism to differentiate higher visual areas