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The Journal of Neuroscience, September 7, 2005, 25(36):8150-8164; doi:10.1523/JNEUROSCI.2058-05.2005

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Behavioral/Systems/Cognitive
Multiple Object Response Normalization in Monkey Inferotemporal Cortex

Davide Zoccolan,^1,2,3 * David D. Cox,^1,2 * and James J. DiCarlo^1,2

¹McGovern Institute for Brain Research, ²Department of Brain and Cognitive Sciences, and ³Center for Biological and Computational Learning, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

The highest stages of the visual ventral pathway are commonly assumed to provide robust representation of object identity by disregarding confounding factors such as object position, size, illumination, and the presence of other objects (clutter). However, whereas neuronal responses in monkey inferotemporal cortex (IT) can show robust tolerance to position and size changes, previous work shows that responses to preferred objects are usually reduced by the presence of nonpreferred objects. More broadly, we do not yet understand multiple object representation in IT. In this study, we systematically examined IT responses to pairs and triplets of objects in three passively viewing monkeys across a broad range of object effectiveness. We found that, at least under these limited clutter conditions, a large fraction of the response of each IT neuron to multiple objects is reliably predicted as the average of its responses to the constituent objects in isolation. That is, multiple object responses depend primarily on the relative effectiveness of the constituent objects, regardless of object identity. This average effect becomes virtually perfect when populations of IT neurons are pooled. Furthermore, the average effect cannot simply be explained by attentional shifts but behaves as a primarily feedforward response property. Together, our observations are most consistent with mechanistic models in which IT neuronal outputs are normalized by summed synaptic drive into IT or spiking activity within IT and suggest that normalization mechanisms previously revealed at earlier visual areas are operating throughout the ventral visual stream.

Key words: inferotemporal cortex; monkey; object recognition; multiple objects; normalization; clutter tolerance

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Received May 20, 2005; revised July 22, 2005; accepted July 23, 2005.

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