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The Journal of Neuroscience, July 21, 2004, 24(29):6540-6544; doi:10.1523/JNEUROSCI.1630-04.2004

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BRIEF COMMUNICATION
Pain Encoding in the Human Forebrain: Binary and Analog Exteroceptive Channels

Fred A. Lenz,¹ Shinji Ohara,¹ Rick H. Gracely,² Patrick M. Dougherty,³ and Salil H. Patel¹

¹Department of Neurosurgery, Johns Hopkins Hospital, Baltimore, Maryland 21278-7713, ²Departments of Internal Medicine and Rheumatology and Neurology, University of Michigan Health System and Ann Arbor Veterans Affairs Medical Center, Ann Arbor, Michigan 48109, and ³Department of Anesthesiology, M.D. Anderson Cancer Center, Houston, Texas 77030

The neuronal system signaling pain has often been characterized as a labeled line consisting of neurons in the pain-signaling pathway to the brain [spinothalamic tract (STT)] that respond only to painful stimuli. It has been proposed recently that the STT contains a series of analog labeled lines, each signaling a different aspect of the internal state of the body (interoception) (e.g., visceral-cold-itch sensations). In this view, pain is the unpleasant emotion produced by disequilibrium of the internal state. We now show that stimulation of an STT receiving zone in awake humans (66 patients) produces two different responses. The first is a binary response signaling the presence of painful stimuli. The second is an analog response in which nonpainful and painful sensations are graded with intensity of the stimulus. Compared with the second pathway, the first was characterized by higher pain ratings and stimulus-evoked sensations covering more of the body surface (projected fields). Both painful responses to stimulation were described in terms usually applied to external stimuli (exteroception) rather than to internal or emotional phenomena, which were infrequently evoked by stimulation of either pathway. These results are consistent with those of functional imaging studies that have identified brain regions activated in a binary manner by the application of a specific, painful stimulus while increases in stimulus intensity do not produce increased activation. Such binary pain functions could be involved in pain-related alarm-alerting functions, which are independent of stimulus amplitude.

Key words: principal sensory nucleus of thalamus; human; microstimulation; pain; spinothalamic; thalamus

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Received April 28, 2004; revised May 30, 2004; accepted June 7, 2004.

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