Sensory experience modifies feature map relationships in visual cortex.

Shaun L Cloherty,Michael R Ibbotson,Partha S Bhagavatula,Markus A Hietanen,Geoffrey J Goodhill,Nicholas J Hughes

doi:10.7554/elife.13911

Abstract

The extent to which brain structure is influenced by sensory input during development is a critical but controversial question. A paradigmatic system for studying this is the mammalian visual cortex. Maps of orientation preference (OP) and ocular dominance (OD) in the primary visual cortex of ferrets, cats and monkeys can be individually changed by altered visual input. However, the spatial relationship between OP and OD maps has appeared immutable. Using a computational model we predicted that biasing the visual input to orthogonal orientation in the two eyes should cause a shift of OP pinwheels towards the border of OD columns. We then confirmed this prediction by rearing cats wearing orthogonally oriented cylindrical lenses over each eye. Thus, the spatial relationship between OP and OD maps can be modified by visual experience, revealing a previously unknown degree of brain plasticity in response to sensory input.

Highlights

In cats and monkeys neurons in the primary visual cortices are selective for both the orientation of the visual input and its eye of origin (Hubel and Wiesel, 1977)
While some aspects of the structure of ocular dominance (OD) and orientation preference (OP) maps individually are plastic in response to altered visual input, such as monocular deprivation (Hubel et al, 1977; Shatz and Stryker, 1978; Farley et al, 2007) or stripe rearing (Sengpiel et al, 1999; Tanaka et al, 2006), none of these manipulations has succeeded in modifying the overall spatial relationships between OD and OP maps, which have appeared immune from environmental influence
The elastic net algorithm (Durbin and Mitchison, 1990) uses Hebbian learning to optimize a tradeoff between coverage and continuity constraints, and can explain many aspects of visual map formation (Swindale, 1996; Goodhill, 2007)

Summary

Introduction

In cats and monkeys neurons in the primary visual cortices are selective for both the orientation of the visual input (orientation preference, OP) and its eye of origin (ocular dominance, OD) (Hubel and Wiesel, 1977) These feature preferences are arranged spatially in the form of OP and OD maps, with stereotypical structure within each map, and strong spatial relationships between them (Blasdel and Salama, 1986; Bonhoeffer and Grinvald, 1991; Bartfeld and Grinvald, 1992; Obermayer and Blasdel, 1993; Hubener et al, 1997; Nauhaus et al, 2012). In particular OP map pinwheels, where domains representing all orientations meet at a point, always tend to lie close to the center of OD regions This is true even after manipulations of the visual input such as rearing animals with artificially induced strabismus (Hubel and Wiesel, 1965; Lowel, 1994; Lowel et al, 1998) or monocular deprivation (Crair et al, 1997). Whether this relationship is a fundamental aspect of map structure that is determined by innate mechanisms (Godecke and Bonhoeffer, 1996; Crair et al, 1998; Kaschube et al, 2002; Katz and Crowley, 2002; Tomita et al, 2013), and beyond the limits of brain plasticity, is unclear

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Conclusion