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The Journal of Neuroscience, January 21, 2004, 24(3):752-761; doi:10.1523/JNEUROSCI.3272-03.2004

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Behavioral/Systems/Cognitive
Posterior Triangular Thalamic Neurons Convey Nociceptive Messages to the Secondary Somatosensory and Insular Cortices in the Rat

Caroline Gauriau and Jean-François Bernard

Institut National de la Santé et de la Recherche Médicale, U-288, 75634 Paris, France

This study investigated the responses of posterior triangular (PoT) thalamic neurons to tactile and noxious calibrated stimuli in anesthetized rats. We report here that 41% of PoT units responded to cutaneous stimulation, in most cases, by increasing strongly their firing. Forty-five percent of the responding units were nociceptive specific (NS), 19% were nociceptive nonspecific (NNS), and 36% were tactile. The NS units responded only to frankly noxious stimuli applied to relatively large receptive fields (several parts of the body). They encoded nociceptive temperatures chiefly in 46-50°C ranges. The NNS units resembled NS units but also responded to innocuous stimuli. Tactile units responded chiefly to repeated innocuous stimuli applied to very small receptive fields (one to two fingers or vibrissae).

A representative sample of PoT somatosensory neurons, characterized first by their response to innocuous and noxious cutaneous stimuli, were filled with juxtacellular injection of biotin-dextran that made it possible to label adequately the soma, the dendrites, and the entire axon of PoT neurons. We observed that the axons of NS neurons terminated only in secondary somatosensory (S2) cortex, whereas the axons of NNS and tactile neurons projected chiefly to the insular cortex and the amygdala.

In conclusion, our results demonstrate a spinal-PoT-S2/insular cortices nociceptive pathway that conveys nociceptive messages arising from lamina I and spinal neurons of deep laminas. Furthermore, our results demonstrate for the first time that projections of PoT neurons are correlated to their physiological properties.

Key words: lamina I; dorsal horn; thalamus; S2; insular; cortex; nociception

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Received July 10, 2003; revised November 21, 2003; accepted November 24, 2003.

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