Topographic maps are common throughout the nervous system, yet their functional role is still unclear. In particular, whether they are necessary for decoding sensory stimuli is unknown. Here we examined this question by recording population activity at the cellular level from the larval zebrafish tectum in response to visual stimuli at three closely spaced locations in the visual field. Due to map imprecision, nearby stimulus locations produced intermingled tectal responses, and decoding based on map topography yielded an accuracy of only 64%. In contrast, maximum likelihood decoding of stimulus location based on the statistics of the evoked activity, while ignoring any information about the locations of neurons in the map, yielded an accuracy close to 100%. A simple computational model of the zebrafish visual system reproduced these results. Although topography is a useful initial decoding strategy, we suggest it may be replaced by better methods following visual experience.

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.DOI: http://dx.doi.org/10.7554/eLife.13911.001

An important example of brain plasticity is the change in the structure of the orientation map in mammalian primary visual cortex in response to a visual environment consisting of stripes of one orientation. In principle there are many different ways in which the structure of a normal map could change to accommodate increased preference for one orientation. However, until now these changes have been characterised only by the relative sizes of the areas of primary visual cortex representing different orientations. Here we extend to the stripe-reared case a recently proposed Bayesian method for reconstructing orientation maps from intrinsic signal optical imaging data. We first formulated a suitable prior for the stripe-reared case, and developed an efficient method for maximising the marginal likelihood of the model in order to determine the optimal parameters. We then applied this to a set of orientation maps from normal and stripe-reared cats. This analysis revealed that several parameters of overall map structure, specifically the difference between wavelength, scaling and mean of the two vector components of maps, changed in response to stripe-rearing, which together give a more nuanced assessment of the effect of rearing condition on map structure than previous measures. Overall this work expands our understanding of the effects of the environment on brain structure.

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A striking example of brain organisation is the stereotyped arrangement of cell preferences in the visual cortex for edges of particular orientations in the visual image. These "orientation preference maps" appear to have remarkably consistent statistical properties across many species. However fine scale analysis of these properties requires the accurate reconstruction of maps from imaging data which is highly noisy. A new approach for solving this reconstruction problem is to use Bayesian Gaussian process methods, which produce more accurate results than classical techniques. However, so far this work has not considered the fact that maps for several other features of visual input coexist with the orientation preference map and that these maps have mutually dependent spatial arrangements. Here we extend the Gaussian process framework to the multiple output case, so that we can consider multiple maps simultaneously. We demonstrate that this improves reconstruction of multiple maps compared to both classical techniques and the single output approach, can encode the empirically observed relationships, and is easily extendible. This provides the first principled approach for studying the spatial relationships between feature maps in visual cortex.