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The Journal of Neuroscience, November 23, 2005, 25(47):10844-10856; doi:10.1523/JNEUROSCI.3562-05.2005

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Behavioral/Systems/Cognitive
The Suppressive Field of Neurons in Lateral Geniculate Nucleus

Vincent Bonin,^1,2 Valerio Mante,^1,2 and Matteo Carandini^1,2

¹Smith-Kettlewell Eye Research Institute, San Francisco, California 94115, and ²Institute of Neuroinformatics, University of Zurich and Swiss Federal Institute of Technology, CH-8057 Zurich, Switzerland

The responses of neurons in lateral geniculate nucleus (LGN) exhibit powerful suppressive phenomena such as contrast saturation, size tuning, and masking. These phenomena cannot be explained by the classical center-surround receptive field and have been ascribed to a variety of mechanisms, including feedback from cortex. We asked whether these phenomena might all be explained by a single mechanism, contrast gain control, which is inherited from retina and possibly strengthened in thalamus. We formalized an intuitive model of retinal contrast gain control that explicitly predicts gain as a function of local contrast. In the model, the output of the receptive field is divided by the output of a suppressive field, which computes the local root-mean-square contrast. The model provides good fits to LGN responses to a variety of stimuli; with a single set of parameters, it captures saturation, size tuning, and masking. It also correctly predicts that responses to small stimuli grow proportionally with contrast: were it not for the suppressive field, LGN responses would be linear. We characterized the suppressive field and found that it is similar in size to the surround of the classical receptive field (which is eight times larger than commonly estimated), it is not selective for stimulus orientation, and it responds to a wide range of frequencies, including very low spatial frequencies and high temporal frequencies. The latter property is hardly consistent with feedback from cortex. These measurements thoroughly describe the visual properties of contrast gain control in LGN and provide a parsimonious explanation for disparate suppressive phenomena.

Key words: cat; gain control; receptive field; masking; adaptation; inhibition

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Received May 6, 2005; revised September 30, 2005; accepted October 9, 2005.

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