Experience-Dependent Reorganization Drives Development of a Binocularly Unified Cortical Representation of Orientation

Abstract

Across sensory areas, neural microcircuits consolidate diverse streams of information into unified, representations of the external world. In the carnivore visual cortex, where eye-specific inputs converge, it has been posited that a single, shared columnar representation of orientation develops independent of sensory experience. In this study, in vivo calcium imaging with columnar and cellular resolution reveals a strikingly different developmental process in ferret visual cortex, starting with an early developmental period in which contralateral, ipsilateral or binocular stimulation each yield distinct well-organized representations of orientation that are misaligned at the columnar and cellular scale. Experience-dependent processes drive the reorganization of these three representations towards a single binocularly-aligned representation resembling the early binocular representation through concerted shifts in the preferred orientation of individual neurons. Thus, contrary to previous findings, a unified binocular representation of orientation results from an experience-dependent process that aligns the activity patterns of three distinct neural representations..

Development of Visual Response Selectivity in Cortical GABAergic Interneurons

“…We wondered how these changes in the responses of GABA-INs related to the modular organization of orientation preferences. Modular organization has been observed in both mature excitatory and inhibitory networks, as well as naive excitatory networks in the ferret 4,6,8 . To assess the state of the modular organization across development, we used widefield 3A-B).…”

“…The visual cortex of carnivores and primates has a modular arrangement of excitatory neurons, which is characterized by both the local clustering and long-range patterning of neuronal responses and functional properties such as orientation preference. Modular network organization is evident in excitatory networks before visual experience for both spontaneous activity and visually evoked responses to orientation, suggesting it develops in an experience-independent manner 4,6,7 .…”

“…The onset of visual experience coincides with a period during which cortical circuits are highly plastic. This enables visual experience to drive maturation of the functional properties and network organization of excitatory neurons in the visual cortex, improving orientation and direction selectivity and establishing binocular alignment of response preferences [1][2][3][4][5] . The visual cortex of carnivores and primates has a modular arrangement of excitatory neurons, which is characterized by both the local clustering and long-range patterning of neuronal responses and functional properties such as orientation preference.…”

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

“…The above-mentioned process was done separately for recordings to the contralateral or ipsilateral eye. Cells were considered monocular if the trial-averaged response to any stimulus direction was greater than two standard deviations above the noise mean for the contralateral or the ipsilateral eye (Chang et al, 2020). Cells were considered binocular if the trial-averaged response to any stimulus direction was greater than two standard deviations above the noise mean for each eye.…”

A binocular synaptic network supports interocular response alignment in visual cortical neurons

“…In carnivores and primates, binocular convergence first occurs in the primary visual cortex (V1) where individual cortical neurons respond selectively to sensory stimulation of one or both eyes Wiesel, 1962, 1965;Ohzawa and Freeman, 1986a;Priebe, 2008). Cortical neurons are also selective for edge orientation (Hubel and Wiesel, 1962;Priebe and Ferster, 2012), and in all mammals investigated, most binocular neurons exhibit matched orientation preferences for stimuli viewed through each eye (Bridge and Cumming, 2001;Chang et al, 2020;Ferster, 1981;Hubel and Wiesel, 1962;Nelson et al, 1977;Skottun and Freeman, 1984;Wang et al, 2010). While interocular alignment of response properties is considered to be a prerequisite for binocular vision (Marr and Poggio, 1979), the synaptic basis of this phenomenon is poorly understood.…”