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The Journal of Neuroscience, June 22, 2005, 25(25):5926-5934; doi:10.1523/JNEUROSCI.1360-05.2005

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Behavioral/Systems/Cognitive
The Role of Thalamic Inputs in Surround Receptive Fields of Barrel Neurons

Ernest E. Kwegyir-Afful,¹ Randy M. Bruno,^2,3 Daniel J. Simons,² and Asaf Keller¹

¹Program in Neuroscience and Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, Maryland 21201, ²Department of Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15261, and ³Max Planck Institute, Department of Cellular Physiology, Heidelberg 69120, Germany

Controversy exists regarding the relative roles of thalamic versus intracortical inputs in shaping the response properties of cortical neurons. In the whisker-barrel system, this controversy centers on the mechanisms determining the receptive fields of layer IV (barrel) neurons. Whereas principal whisker-evoked responses are determined by thalamic inputs, the mechanisms responsible for adjacent whisker (AW) responses are in dispute. Here, we took advantage of the fact that lesions of the spinal trigeminal nucleus interpolaris (SpVi) significantly reduce the receptive field size of neurons in the ventroposterior thalamus. We reasoned that if AW responses are established by these thalamic inputs, brainstem lesions would significantly reduce the receptive field sizes of barrel neurons. We obtained extracellular single unit recordings from barrel neurons in response to whisker deflections from control rats and from rats that sustained SpVi lesions. After SpVi lesions, the receptive field of both excitatory and inhibitory barrel neurons decreased significantly in size, whereas offset/onset response ratios increased. Response magnitude decreased only for inhibitory neurons. All of these findings are consistent with the hypothesis that AW responses are determined primarily by direct thalamic inputs and not by intracortical interactions.

Key words: thalamus; trigeminal; vibrissa (whisker); rat; thalamocortical and corticofugal projections; somatosensory cortex

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Received April 7, 2005; revised May 10, 2005; accepted May 11, 2005.

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