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The Journal of Neuroscience, August 16, 2006, 26(33):8441-8450; doi:10.1523/JNEUROSCI.1293-06.2006
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Behavioral/Systems/Cognitive
Corticofugal Output from the Primary Somatosensory Cortex Selectively Modulates Innocuous and Noxious Inputs in the Rat Spinothalamic System
Lénaïc Monconduit, Alberto Lopez-Avila, Jean-Louis Molat, Maryse Chalus, andLuis Villanueva Institut National de la Santé et de la Recherche Médicale, E-216, Université de Clermont-1, 63000 Clermont-Ferrand, France
Correspondence should be addressed to Luis Villanueva, Institut National de la Santé et de la Recherche Médicale, E-216, Université de Clermont-1, 11 Boulevard Charles de Gaulle, 63000 Clermont-Ferrand, France. Email: luis.villanueva{at}u-clermont1.fr
Sensory maps for pain can be modified by deafferentation or injury, and such plasticity has been attributed mainly to changes in the convergence of projections in "bottom-up" mechanisms. We addressed the possible contribution of "top-down" mechanisms by investigating the functional significance of corticofugal influences from the primary somatosensory cortex (S1) to the ventroposterolateral thalamic nucleus (VPL). The strong convergence of spinal and lemniscal afferents to the VPL and the close correspondence between afferents and efferents within the VPL–S1 network suggest the existence of functionally related thalamocortical circuits that are implicated in the detection of innocuous and noxious inputs. Functional characterization of single nociceptive, wide dynamic range, and non-nociceptive VPL neurons and labeling the axons and terminal fields with the juxtacellular technique showed that all three types of cells project to a restricted area, within S1. The convergence of the terminal trees of axons from VPL neurons activated by innocuous, noxious, or both inputs suggests that their inputs are not segregated into anatomically distinct regions. Microinjections within S1 were performed for pharmacological manipulation of corticofugal modulation. Glutamatergic activation of corticofugal output enhanced noxious-evoked responses and affected in a biphasic way tactile-evoked responses of VPL cells. GABAA-mediated depression of corticofugal output concomitantly depressed noxious and enhanced innocuous-evoked responses of VPL neurons. Microinjections of a GABAA antagonist on corticofugal cells enhanced noxious-evoked responses of VPL cells. Our findings demonstrate that corticofugal influences from S1 contribute to selectively modulate somatosensory submodalities at the thalamic level.
Key words: ventrobasal thalamus; pain; allodynia; GABA; deafferentation; nociception
Received Oct. 20, 2005; revised June 21, 2006; accepted July 1, 2006.
Correspondence should be addressed to Luis Villanueva, Institut National de la Santé et de la Recherche Médicale, E-216, Université de Clermont-1, 11 Boulevard Charles de Gaulle, 63000 Clermont-Ferrand, France. Email: luis.villanueva{at}u-clermont1.fr
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