Experience-dependent reorganization drives development of a binocularly unified cortical representation of orientation

Abstract

Across sensory areas, neural microcircuits consolidate diverse streams of sensory information into unified, representations of the external world, but the developmental process underlying alignment of sensory representations remains poorly understood. Using two-photon and widefield epifluorescence calcium imaging in developing ferret visual cortex, we find an early developmental period in which monocular stimulation reveals two divergent representations of orientation at the network and cellular-scales. During the period of monocular network misalignment, binocular stimulation drives a third orientation representation, distinct from the constituent monocular representations. Alignment towards a single, binocularly unified representation requires binocular visual experience shortly after eye-opening. Chronic imaging demonstrates that the monocular and binocular orientation representations functionally reorganize towards a single representation resembling the early binocular representation through concerted shifts in preferred orientation across the cellular-scale and network-scale representations. Thus, we propose that an experience-dependent learning process drives the emergence of a unified binocular representation of orientation.

Synaptic and intrinsic mechanisms underlying development of cortical direction selectivity

“…In the developing visual system, molecular cues and spontaneous activity ( Katz and Shatz, 1996 ) shape the formation of initial circuitry and the emergence of initial cortical receptive field properties, including retinotopic organization ( Cang et al, 2008 ) and orientation selectivity ( Chapman and Stryker, 1993 ; Crair et al, 1998 ; Li et al, 2006 ; Smith et al, 2018 ) (although not its alignment across the two eyes, which requires experience Wang et al, 2010 ; Gu and Cang, 2016 ; Whitney et al, 2019 ). In cortex of ferrets ( Li et al, 2006 ) and primates ( Hatta et al, 1998 ) (but not mice: Rochefort et al, 2011 ), selectivity for direction of motion is not present at eye opening – neurons respond about equally to stimulation in two opposite directions – but develops over a period of about 2 weeks in ferrets and about 4 weeks in macaques.…”