Abstract
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.
Highlights
In the visual cortices of cats and macaques, there are representations of specific visual features, such as orientation preference, direction of motion preference, ocular dominance, and retinotopy (Hubel and Wiesel, 1962, 1968, 1974, 1977; Hubel et al, 1977; Tusa et al, 1978, 1979; Swindale et al, 1987; Swindale, 1988)
If the single-orientation exposure affected orientation selectivity formation from postnatal day 10 (P10) to P24, the histogram should have a single peak at 90◦
Orientation Map Development First of all, we attempted to reproduce the development of a regular orientation map in the visual cortex of cats reared under normal visual conditions
Summary
In the visual cortices of cats and macaques, there are representations of specific visual features, such as orientation preference, direction of motion preference, ocular dominance, and retinotopy (Hubel and Wiesel, 1962, 1968, 1974, 1977; Hubel et al, 1977; Tusa et al, 1978, 1979; Swindale et al, 1987; Swindale, 1988) These feature representations emerge as columns in the 3D visual cortex, because neuronal response properties are similar in the depth direction from the pia mater to white matter. Blakemore and Cooper (1970) exposed kittens to a vertical or horizontal orientation for several hours a day, keeping the kittens inside a drum where vertical or horizontal lines were painted on the inner wall At other times, they reared the animals in a dark room with their mother cats to prevent visual experience other than vertical or horizontal lines. Stryker and Sherk (1975) repeated similar experiments but they were not able to reproduce Blakemore and Cooper’s results with statistical significance
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