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Received August 5, 2005
Revised September 7, 2005
Accepted after revision October 19, 2005
1 University of MIchigan
2 University of Michigan
3 University of Michigan, 6510 Medical Sci Research Bldg 1
* To whom correspondence should be addressed. E-mail: yli{at}umich.edu.
The anterior cingulate cortex (ACC) is critically involved in processing the affective component of pain sensation. Visceral hypersensitivity is a characteristic of irritable bowel syndrome. Electrophysiological activity of the ACC with regard to visceral sensitization has not been characterized. Single ACC activities in response to colorectal distension (CRD) were recorded in sham-treated rats and viscerally hypersensitive (EA) rats (induced by chicken egg albumin (EA) injection, I.P.). The ACC neurons of controls failed to respond to 10 or 30 mmHg CRD; only 22% were activated by 50 mmHg CRD. Among the latter, 12% were labelled CRD-excited neurons. In contrast, CRD (10, 30, 50 mmHg) markedly increased ACC neuronal responses of EA rats (10%, 28%, and 47%, respectively). CRD produced greater pressure-dependent increases in ACC spike firing rates in EA rats compared to controls. Splanchnicectomy combined with pelvic nerve sections abolished ACC responses to CRD in EA rats. Spontaneous activity in CRD-excited ACC neurons was significantly higher in EA rats than in controls. CRD-excited ACC neurons in control and EA rats (7 of 16 [42%] and 8 of 20 [40%], respectively) were activated by transcutaneous electrical and thermal stimuli. However, ACC neuronal activity evoked by noxious cutaneous stimuli did not change significantly in EA rats. This study identifies CRD-responsive neurons in the ACC and establishes for the first time that persistence of a heightened visceral afferent nociceptive input to the ACC induces ACC sensitization, characterized by increased spontaneous activity of CRD-excited neurons, decreased CRD pressure threshold, and increased response magnitude. Enhanced ACC nociceptive transmission in viscerally hypersensitive rats is restricted to visceral afferent input.
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