Comparison of Anterior Cingulate and Primary Somatosensory Neuronal Responses to Noxious Laser-Heat Stimuli in Conscious, Behaving Rats

Abstract

Kuo, Chung-Chih and Chen-Tung Yen. Comparison of anterior cingulate and primary somatosensory neuronal responses to noxious laser-heat stimuli in conscious, behaving rats. J Neurophysiol 94: 1825-1836, 2005; 10.1152/jn.00294.2005. In this study, we investigated single-unit responses of the primary sensorimotor cortex (SmI) and anterior cingulate cortex (ACC) to noxious stimulation of the tail of the rat. The influences of morphine on these nociceptive responses were also compared. Multiple single-unit activities were recorded from two eight-channel microwire arrays chronically implanted in the tail region of the SmI and ACC, respectively. CO 2 laser-heat irradiation of the middle part of the tail at an intensity slightly higher than that causing a maximal tail flick response was used as a specific noxious stimulus. Examined individually, ACC neurons were less responsive than SmI neurons to laser-heat stimulus, in that only 51% of the ACC units (n ϭ 125) responded compared with 88% of the SmI units (n ϭ 74). Among these responsive ACC units, many had a very long latency and long-lasting excitatory type of response that was seldom found in the SmI. When ensemble activities were examined, laser heat evoked both short-(60 ϳ 150 ms) and long-latency (151 ϳ 600 ms) responses in the SmI and ACC. Latencies of both responses were longer in the ACC. Furthermore, a single dose of 2.5-10 mg/kg morphine intraperitoneally suppressed only the long latency response in the SmI, but significantly attenuated both responses in the ACC. These effects of morphine were completely blocked by prior treatment with the opiate receptor blocker, naloxone. These results provide further evidence suggesting that the SmI and ACC may play different roles in processing noxious information. I N T R O D U C T I O NRecent neuroimaging studies in human subjects have revealed several key forebrain areas most often activated by noxious stimulations. Among these areas are the primary somatosensory cortex (SI) and anterior cingulate cortex (ACC) (Casey et al. 1994; Coghill et al. 1994 Coghill et al. , 1999 Craig et al. 1996; Davis et al. 1995; Dorbyshire et al. 1997; Hsieh et al. 1995; Talbot et al. 1991; Vogt et al. 1996). Furthermore, studies by Rainville et al. (1997) and Hofbauer et al. (2001) showed that functional MRI (fMRI) intensities in the SI were correlated with the intensity of the noxious heat, whereas those in the ACC were better correlated with subjective unpleasantness, suggesting a differential functional role between SI and ACC.In contrast, the processing of nociceptive information in the forebrain at the cellular level is largely unclear. Neuroanatomical and neurophysiological studies have shown that pain information is processed through a complicated serial and parallel network in the forebrain (Craig 2003; Willis 1985). Electrophysiological studies of the SI have revealed nociceptive neu-

Dynamic Processing of Nociception in Cortical Network in Conscious Rats: A Laser-evoked Field Potential Study

“…Although the role of SI in pain processing is still in debate, there is converging evidence suggesting that SI participates in the pain perception (Bushnell et al 1999). Recently, evidence from multiple single-unit recording in conscious rats showed that SI neurons exhibited excitatory type responses to noxious laser stimulation applied to the tail (Kuo and Yen 2005). Previous work in our laboratory also supported the role of SI in processing of noxious radiate heat stimulation delivered to the hind paw of the rat (Wang et al , 2004.…”

Predicting Aversive Events and Terminating Fear in the Mouse Anterior Cingulate Cortex during Trace Fear Conditioning

“…All bin values were transformed to z-scores according to the mean and SD of the baseline period. A 99% confidence level (z Ͼ 2.33 or z Ͻ Ϫ2.33) was used for identifying whether a single extracellular unit responded (Kuo and Yen, 2005).…”

Temporal and spatial temperature distribution in the glabrous skin of rats induced by short-pulse CO2 laser

“…6,7 In addition, radiant heat stimulation is essential for wakeful, freely moving behavioral animal studies. [8][9][10] Short-pulse lasers of tens of milliseconds offer several advantages over a long-pulse laser, including completing noxious stimuli before escape behaviors, [8][9][10] reducing tissue damage, and increasing synchronization of neuronal activities.…”

“…3 Since then, the CO 2 laser has been widely used in human and animal pain studies. [8][9][10][21][22][23] We investigated six intensities of short-pulse (25 and 35 ms) CO 2 laser, which ranged from innocuous to noxious indicated by paw lifting. We applied laser pulses on the hind paw of the rat under anesthesia, and detected surface temperature distribution by a fast speed infrared camera.…”