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The Journal of Neuroscience, November 11, 2009, 29(45):14236-14246; doi:10.1523/JNEUROSCI.2341-09.2009

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Behavioral/Systems/Cognitive
Cerebral and Cerebrospinal Processes Underlying Counterirritation Analgesia

Mathieu Piché,^1,2,3,4,7 Marianne Arsenault,^3,4,5 and Pierre Rainville^2,3,4,6

¹Département de Physiologie, ²Groupe de recherche sur le système nerveux central, ³Centre de recherche en neuropsychologie et cognition, ⁴Centre de recherche de l'Institut universitaire de gériatrie de Montréal, and ⁵Départements de Psychologie and ⁶Stomatologie, Université de Montréal, Montréal, Quebec H3T 1J4, Canada, and ⁷Département de chiropratique, Université du Québec à Trois-Rivières, Trois-Rivières, Quebec G9A 5H7, Canada

Correspondence should be addressed to Dr. Pierre Rainville, Département de Stomatologie, Faculté de Médecine Dentaire, Université de Montréal, CP 6128 Succursale Centre-ville, Montréal, QC H3C 3J7, Canada. Email: pierre.rainville{at}umontreal.ca

Pain is a complex experience involving extensive interactions between brain and spinal cord processes. Various interventions that modulate pain, such as the application of a competing noxious stimulus (counterirritation), are thought to involve cerebrospinal regulation through diffuse noxious inhibitory controls (DNICs). However, no study has yet examined the relation between brain and spinal cord activity during counterirritation analgesia in humans. This fMRI study investigates brain responses to phasic painful electrical stimulation administered to the sural nerve to evoke a spinal nociceptive response (RIII reflex) before, during and after counterirritation induced by the immersion of the left contralateral foot in cold water. Responses are compared with a control condition without counterirritation. As expected, counterirritation produced robust pain inhibition with residual analgesia persisting during the recovery period. In contrast, RIII reflex amplitude was significantly decreased by counterirritation only in a subset of subjects. Modulatory effects of counterirritation on pain perception and spinal nociception were paralleled by decreased shock-evoked activity in pain-related areas. Individual changes in shock-evoked brain activity were specifically related to analgesia in primary somatosensory cortex (SI), anterior cingulate cortex and amygdala, and to RIII modulation in supplementary motor area and orbitofrontal cortex (OFC). Moreover, sustained activation induced by the counterirritation stimulus in the OFC predicted shock-pain decrease while sustained activity in SI and the periaqueductal gray matter predicted RIII modulation. These results provide evidence for the implication of at least two partly separable neural mechanisms underlying the effects of counterirritation on pain and spinal nociception in humans.

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Received May 19, 2009; revised Sept. 7, 2009; accepted Sept. 28, 2009.

Correspondence should be addressed to Dr. Pierre Rainville, Département de Stomatologie, Faculté de Médecine Dentaire, Université de Montréal, CP 6128 Succursale Centre-ville, Montréal, QC H3C 3J7, Canada. Email: pierre.rainville{at}umontreal.ca

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