Retracted: Enhanced responses of the anterior cingulate cortex neurones to colonic distension in viscerally hypersensitive rats

Abstract

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 neuronal activities in response to colorectal distension (CRD) were recorded in control, sham-treated rats and viscerally hypersensitive (EA) rats (induced by chicken egg albumin injection, I.P). The ACC neurones of controls failed to respond to 10 or 30 mmHg CRD; only 22% were activated by 50 mmHg CRD. Among the latter, 16.4% exhibited an excitatory response to CRD and were labelled 'CRD-excited' neurones. In contrast, CRD (10, 30 and 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 with controls. Splanchnicectomy combined with pelvic nerve section abolished ACC responses to CRD in EA rats. Spontaneous activity in CRD-excited ACC neurones was significantly higher in EA rats than in controls. CRD-excited ACC neurones 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 neurones 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 neurones, decreased CRD pressure threshold, and increased response magnitude. Enhanced ACC nociceptive transmission in viscerally hypersensitive rats is restricted to visceral afferent input.

Distribution and properties of visceral nociceptive neurons in rabbit cingulate cortex

“…Although the source of viscerocutaneous afferents likely arises in the MITN, the problem of cutaneous-only and visceral-only responses originate from present findings and those of Gao et al (2006) showing visceral hypersensitization with increased baseline activity and lowered threshold for visceral activation in ACC that were not associated with changes in noxious cutaneous responses. Although it is not known how independent channels process cutaneousonly and visceral-only pain in cingulate cortex, the following possibilities are relevant.…”

“…This assures that neuron responses under anesthesia reflect nociceptive activity. There is only one study of ACC neuron responses during colorectal distension (Gao et al, 2006). These neurons were not activated by innocuous distension and only 22% were nociceptive.…”

Regional brain activation in conscious, nonrestrained rats in response to noxious visceral stimulation

“…Thus, it is not surprising that no consensus has emerged that allows comparison between rat c-fos data and human neuroimaging findings. Other region-specific analysis of neuronal responses to CRD has been carried out using in vivo electrophysiological recording technique [1,22]. Lazovic et al conducted the only reported fMRI study in the rat CRD model [38].…”

Topological Alterations of the Intrinsic Brain Network in Patients with Functional Dyspepsia

“…The ACG is a multifunctional region that participates in information processing of visceral sensory data, cognitive control and emotional arousal. [35][36][37][38] It is one of the most commonly activated areas during visceral distension. 39,40 Intriguingly, the nodal centralities in the ACG were found to be positively related to DSS of patients in the current results, which reflected the correlation between information flow through the ACG and symptom severity.…”