Functional Differentiation of Mouse Visual Cortical Areas Depends upon Early Binocular Experience

Abstract

The mammalian visual cortex contains multiple retinotopically defined areas that process distinct features of the visual scene.Little is known about what guides the functional differentiation of visual cortical areas during development. Recent studies in mice have revealed that visual input from the two eyes provides spatiotemporally distinct signals to primary visual cortex (V1), such that contralateral eye-dominated V1 neurons respond to higher spatial frequencies than ipsilateral eye-dominated neurons. To test whether binocular visual input drives the differentiation of visual cortical areas, we used two-photon calcium imaging to characterize the effects of juvenile monocular deprivation (MD) on the responses of neurons in V1 and two higher visual areas, LM (lateromedial) and PM (posteromedial). In adult mice of either sex, we find that MD prevents the emergence of distinct spatiotemporal tuning in V1, LM, and PM. We also find that, within each of these areas, MD reorganizes the distinct spatiotemporal tuning properties driven by the two eyes. Moreover, we find a relationship between speed tuning and ocular dominance in all three areas that MD preferentially disrupts in V1, but not in LM or PM. Together, these results reveal that balanced binocular vision during development is essential for driving the functional differentiation of visual cortical areas. The higher visual areas of mouse visual cortex may provide a useful platform for investigating the experience-dependent mechanisms that set up the specialized processing within neocortical areas during postnatal development.

The role of early visual experience in the development of spatial‐frequency preference in the primary visual cortex

“…The values of optimal SFs at PW3 obtained by intrinsic imaging and two-photon Ca 2+ imaging in the present study are similar to those just after eye-opening previously reported via electrophysiological recordings in mice (Hoy & Niell, 2015). In addition, the optimal SF values after PW3 are similar to those reported in some previous studies on adult mice (Hoy & Niell, 2015;Durand et al 2016) but lower than in others (Salinas et al 2017(Salinas et al , 2021. This difference may be ascribed to the differences in the recording sites in the visual cortex.…”

“…We further show that this developmental shift requires visual experience during a particular period in postnatal development. A recent study employing two-photon Ca 2+ imaging demonstrated that 2-week monocular deprivation of juvenile mice causes a decrease in optimal SFs in the adult visual cortex (Salinas et al 2021). Thus, normal visual experience seems to be required for a developmental increase in optimal SFs.…”

Chronic Monocular Deprivation Reveals MMP9-Dependent and -Independent Aspects of Murine Visual System Plasticity

“…Changes in visual response strength induced by cMD were limited to deprived eye responses, and therefore differed from the response to MD at the peak of the critical period, in which deprived eye depression is followed by an increase in the strength and selectivity of non-deprived eye responses [ 2 , 35 , 50 , 51 ]. The decrease in the strength of visual responses following cMD was observed across a range of spatial frequencies and contrasts.…”

“…The characterization of neuronal responses in mouse V1b as binocular has recently come under scrutiny [ 37 , 59 , 60 , 61 , 62 ]. Central to this debate is the role of inclusion criteria in the definition of visually-evoked GCaMP activity, as the adaptation of high-threshold inclusion criteria excludes contributions from the non-dominant eye [ 51 ]. However, in our hands, increasing the threshold for the inclusion of visually-evoked activity from the non-dominant eye did not reduce the number of neurons categorized as binocular in any experimental populations of adult mice.…”

Focusing on cognitive potential as the bright side of mental atypicality

“…Third, ocular dominance has been shown to result from the competition between neurons and neural networks to represent and process environmental and internal information 44 – 46 . For instance, the dominance of one eye over the other was a direct function of the amount of light stimulating the dominant eye in birds 44 .…”