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The Journal of Neuroscience, October 11, 2006, 26(41):10548-10557; doi:10.1523/JNEUROSCI.1746-06.2006

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Behavioral/Systems/Cognitive
Angular Tuning Bias of Vibrissa-Responsive Cells in the Paralemniscal Pathway

Takahiro Furuta,1,2 Kouichi Nakamura,2,3 and Martin Deschenes1

1Centre de Recherche Université Laval Robert-Giffard, Québec G1J 2G3, Canada, 2Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan, and 3Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Kawaguchi 332-0012, Japan

Correspondence should be addressed to Dr. Martin Deschenes, Centre de Recherche Université Laval Robert-Giffard, 2601 de la Canardiere, Québec G1J 2G3, Canada. Email: martin.deschenes{at}crulrg.ulaval.ca

One of the most salient features of primary vibrissal afferents is their sensitivity to the direction in which the vibrissae move. Directional sensitivity is also well conserved in brainstem, thalamic, and cortical neurons of the lemniscal pathway, indicating that this property plays a key role in the organization of the vibrissal system. Here, we show that directional tuning is also a fundamental feature of second-order interpolaris neurons that give rise to the paralemniscal pathway. Quantitative assessment of responses to vibrissa deflection revealed an anisotropic organization of receptive fields with regard to topography, response magnitude, and the degree of angular tuning. Responses evoked by all vibrissae within the receptive field of each cell exhibited a high consistency of direction preference, but a striking difference in angular tuning preference was found among cells that reside in the rostral and caudal divisions of the interpolaris nucleus. Although in caudal interpolaris vectors of angular preference pointed in all directions, in rostral interpolaris virtually all vectors pointed upward, revealing a strong preference for this direction. Control experiments showed that the upward bias did not rely on a preferential innervation of rostral cells by upwardly tuned primary vibrissa afferents, nor did it rely on a direction-selective recruitment of feedforward inhibition. We thus propose that the upward preference bias of rostral cells, which project to the posterior group of the thalamus, emerges from use-dependent synaptic processes that relate to the kinematics of whisking.

Key words: vibrissa; trigeminal nuclei; paralemniscal pathway; interpolaris nucleus; whisking; vibrissal receptive field


Received April 24, 2006; revised Sept. 7, 2006; accepted Sept. 8, 2006.

Correspondence should be addressed to Dr. Martin Deschenes, Centre de Recherche Université Laval Robert-Giffard, 2601 de la Canardiere, Québec G1J 2G3, Canada. Email: martin.deschenes{at}crulrg.ulaval.ca




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