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

ABSTRACT: Across sensory areas, neural microcircuits consolidate streams of information into unified representations of the external world. In the carnivore visual cortex, where eye-specific inputs first converge, it has been posited that a single, binocularly aligned modular orientation representation develops independent of sensory experience. In this study of ferret visual cortex using in vivo calcium imaging, we find evidence for a different developmental process. Early in development, contralateral, ipsilateral, or binocular stimulation each yield well-organized modular representations of orientation that display features of mature cortex. However, comparison of these representations reveals considerable misalignment that is evident at both modular and cellular scales. Experience-dependent processes drive reorganization of these three representations toward a single binocularly aligned representation resembling the early binocular representation through shifts in cellular orientation preference. Thus, while orderly modular networks of orientation preference initially arise independent of visual experience, experience is critical for the alignment of these early representations.

SUBMITTER: Chang JT

PROVIDER: S-EPMC7381370 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:To date, numerous mathematical models have been proposed on the basis of some types of Hebbian synaptic learning to account for the activity-dependent development of orientation maps as well as neuronal orientation selectivity. These models successfully reproduced orientation map-like spatial patterns. Nevertheless, we still have questions: (1) How does synaptic rewiring occur in the visual cortex during the formation of orderly orientation maps in early life? (2) How does visual experience contribute to the maturation of orientation selectivity of visual cortical neurons and reorganize orientation maps? (3) How does the sensitive period for orientation plasticity end? In this study, we performed animal experiments and mathematical modeling to understand the mechanisms underlying synaptic rewiring for experience-dependent formation and reorganization of orientation maps. At first, we visualized orientation maps from the intrinsic signal optical imaging in area 17 of kittens reared under single-orientation exposure through cylindrical-lens-fitted goggles. The experiments revealed that the degree of expansion of cortical domains representing the experienced orientation depends on the age at which the single-orientation exposure starts. As a result, we obtained the sensitive period profile for orientation plasticity. Next, we refined our previously proposed mathematical model for the activity-dependent self-organization of thalamo-cortical inputs on the assumption that rewiring is caused by the competitive interactions among transient synaptic contacts on the same dendritic spine. Although various kinds of molecules have been reported to be involved in such interactions, we attempt to build a mathematical model to describe synaptic rewiring focusing on brain-derived neurotrophic factor (BDNF) and its related molecules. Performing computer simulations based on the refined model, we successfully reproduced orientation maps reorganized in kittens reared under single-orientation exposure as well as normal visual experience. We also reproduced the experimentally obtained sensitive period profile for orientation plasticity. The excellent agreement between experimental observations and theoretical reproductions suggests that the BDNF-induced competitive interaction among synaptic contacts from different axons on the same spine is an important factor for the experience-dependent formation and reorganization of orientation selectivity and orientation maps.

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

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