Experience-dependent development and maintenance of binocular neurons in the mouse visual cortex

Abstract

The normal development of neuronal circuits requires both hard-wired gene expression and experience. Sensory processing, such as vision, is especially sensitive to perturbations in experience. However, the exact contribution of experience to neuronal visual response properties and binocular vision remains unknown. To determine how visual response properties develop in vivo, we used single cell resolution two-photon calcium imaging of mouse binocular visual cortex at multiple time-points after eye opening. Few neurons are binocularly responsive immediately after eye opening and respond solely to either the contralateral or ipsilateral eye. Binocular neurons emerge during development, which requires visual experience, and show specific tuning of visual response properties. As binocular neurons emerge, activity between the two eyes becomes more correlated in the neuropil. Since experience-dependent plasticity requires the expression of activity-dependent genes, we determined whether the plasticity gene Arc mediates the development of normal visual response properties. Surprisingly, rather than mirroring the effects of visual deprivation, mice that lack Arc show increased numbers of binocular neurons during development. Strikingly, removing Arc in adult binocular visual cortex increases the numbers of binocular neurons and recapitulates the developmental phenotype, suggesting cortical circuits that mediate visual processing require ongoing experience-dependent plasticity. Thus, experience is critical for the normal development and maintenance of circuits required to process binocular vision.

Vision is required for the formation of binocular neurons prior to the classical critical period

“…By contrast, we demonstrate here that early vision is required for the formation of normal numbers of binocular neurons and to improve binocular cell receptive field tuning and matching. In agreement with previous studies, our measures show that few binocular neurons are present at eye opening [20][21][22]41 . Within the first four days thereafter, a near-adult number of binocular neurons is established.…”

“…At eye opening, visually evoked responses were almost entirely driven by contralateral eye stimulation (Figure 1F). This low level of innate binocularity is consistent with previous reports [20][21][22][23] . Moreover, our measures of contralateral eye evoked receptive field tuning at eye opening are consistent with electrophysiological measures 24 , indicating that GCaMP6s signals at this early age accurately reflect the underlying neurophysiology 25 .…”

Development of natural scene representation in primary visual cortex requires early postnatal experience

“…The initial formation of cortical receptive field properties [58][59][60][61], such as orientation selectivity to grating stimuli [60], as well as retinal response properties [62] do not require visual experience. Innate properties are subsequently shaped by experience as well as by development itself.…”

Retinal waves but not visual experience are required for development of retinal direction selectivity maps

“…However, not all directions of motion are equally represented in the visual system. Several studies support the idea that the presence of directional visual stimulation instructs development of direction selectivity in visual cortex: horizontal motion detection develops after eye opening when animals become mobile (Jenks and Shepherd, 2020), visual deprivation leads to fewer direction-selective cells (Li et al, 2006), and training for particular directional motion at particular ages increases the proportion of direction-selective cells (Li et al, 2008; Roy et al, 2020).…”