| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1Institute of Zoology and 2Department of Life Science, National Taiwan University, Taipei, Taiwan
Submitted 21 March 2005; accepted in final form 19 May 2005
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
150 ms) and long-latency (151 600 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. |
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
; Coghill et al. 1994, 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 neurons that have a definite and restricted nociceptive receptive field and are somatotopically organized (Chudler et al. 1990; Kenshalo and Isensee 1983; Kenshalo et al. 2000; Lamour et al. 1983a,b). ACC nociceptive neurons tend to have rather large nociceptive receptive fields and may even include the entire body (Hutchison et al. 1999; Sikes and Vogt 1992; Yamamura et al. 1996). Thus neurons in the SI and ACC seem to exhibit different response properties.
Most of the electrophysiological studies have been carried out on anesthetized animal preparations. Because pain sensations are abolished by general anesthesia, the relevance of results from subjects in an anesthetized condition to pain function is unclear. In the studies performed in unanesthetized human subjects (Hutchison et al. 1999) or monkeys (Kenshalo et al. 1988), on the other hand, either ACC or SI units were respectively recorded, and very different sensory stimuli were tested. Thus quantitative comparisons cannot be made. It would be of interest to test the neuronal responses of the SI and ACC in the same subject with the same array of specific noxious stimuli. To address this critical issue, the first goal of this investigation was to simultaneously record SI and ACC neuronal responses to laser-heat stimulation applied to the mid-part of the tail of conscious rats.
Morphine has powerful analgesic effects. The amplitude of the laser-heat–evoked potential (LEP) is reduced by morphine in parallel with marked clinical pain relief (Kalliomaki et al. 1998; Lorenz et al. 1997). Moreover, Tsai et al. (2004) reported that morphine suppresses only the long-latency laser-evoked responses but not the short-latency laser-heat–evoked unit responses in the rat SI. With relatively denser concentrations of endogenous opiates and opiate receptors in the limbic cortex (Jones et al. 1991; Lewis et al. 1983; Mansour et al. 1986, 1987), it would be of interest to compare the effects of morphine on SI and ACC nociceptive responses such that sensory and affective aspects of the pain function may be explored pharmacologically (Merskey 1986). Our preliminary results were previously reported (Kuo and Yen 2003).
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
300 g at the time of electrode implantation. The care of the animals and the entire experimental procedure were in accordance with Codes for Experimental Use of Animals of the Council of Agriculture, Taiwan, based on the Animal Protection Law, Taiwan, and were approved by the Institutional Animal Care and Use Committee of National Taiwan University. Surgical procedures
The rat was anesthetized initially with pentobarbital sodium (50 mg/kg, ip). Ketamine hydrochloride (50 mg/kg, im) was administered as necessary to maintain a proper anesthetic depth so that the animal had no flexor reflex throughout the surgery period. The rat was mounted on a stereotaxic apparatus. A midline incision was made over the skull. After retraction of the skin and cleaning of the soft tissue, small craniotomies were made for the placement of intracortical microelectrodes in the primary sensorimotor cortex (SmI) and the ACC.
Two microwire array electrodes were implanted in each rat, one in the SmI and the other in the ACC. The eight-channel microwire array electrode was built in-house. Detailed procedures of the construction of the array electrode were previously published (Tsai et al. 2003). Briefly, this is a linear array of stainless-steel wires individually insulated with Teflon (50 µm OD). There are eight channels in an electrode, and the distance from the first channel to the last channel is about 2 mm. Two small longitudinal holes were opened in the right frontoparietal bone. One of the arrays was implanted in the tail region of the SmI (Chapin and Lin 1984). The coordinates of the SmI were 1–3 mm posterior to and 2–3 mm lateral to the bregma, and about 1 mm deep in the cortex. The receptive fields of the individual channels in the SmI were ascertained when the rat was still under anesthesia. The other microelectrode array set was implanted in the ACC 1–3 mm anterior to and 0.3–0.6 mm lateral to the bregma, and 1–2 mm ventral to the surface of the cortex. This region covers the most-responsive and -relevant zones of the ACC reported in the literature by unit recording (Hsu and Shyu 1997; Yamamura et al. 1996), brain imaging (Tuor et al. 2000), activation (Calejesan et al. 2000; Johansen and Fields 2004), and inactivation (Johansen et al. 2001; Kung et al. 2003).
A stainless-steel screw (1 mm OD) for EEG recording was placed in the skull over the left SmI, 2.5 mm posterior and 2.5 mm lateral to the bregma. This was for the laser-heat–evoked potential recording, because in previous studies it was shown that the laser-heat–evoked potentials from the tail stimulation can be recorded bilaterally on both sides of the SmI (Shaw et al.1999, 2001). The ground electrode consisted of stainless-steel screws located over the top of the cerebellum (mid-occipital bone). Several stainless-steel screws were placed in the frontal and parietal bones for anchoring purposes. Two pairs of three-stranded stainless-steel wires (793400, A-M systems) were inserted into the neck muscle and in the tail-flick muscle, respectively, to record their respective EMGs. The holes in the skull and the implanted electrodes were sealed and secured with dental cement. The rats were allowed to recover for 
1 wk after surgery.
Experimental protocol
Before the experiment, the animal was transferred to a test chamber for >2 h/day for 5 days to habituate it to the experimental environment. On the day of the recording, a period of >30 min was allowed for the rat to become familiar with the chamber. The test chamber had an open top to facilitate the connection of the headset cable to the implanted electrodes. It was 36 x 24 x 30 cm in width, depth, and height, respectively. During the test trial, rats could move about in the chamber while tethered to the recording wire. The stimulus was generated by a CO2 laser (medical surgical laser, Tjing Ling 2, National Taiwan University; 10.6-µm wavelength), operating in the TEM00 mode (Gaussian distribution) (Yen et al. 1994). The radiant heat pulses were applied to the middle portion of the tail. The duration of the stimulation pulse was 15 ms. The output power was 8 W. The output energy was 120 mJ, which was about 1.5 times the maximal stimulus intensity for a tail flick response as determined in preliminary trials. The beam diameter was 3 mm (intentionally unfocused). To minimize tissue damage, sensitization, and habituation, stimuli were randomly applied to a local skin area 1 cm in length in the middle part of the tail. The interstimulus interval was longer than 10 s. 20 laser heat stimulations were made in each trial, and the jerky movements of the tail (tail flick) were noted. Each recording period lasted about 5 min.
Three doses (2.5, 5, and 10 mg/kg) of morphine were tested. The sequence of the dosages was random and different dosages were given intraperitoneally by a separation of 2 days. On each test day, laser irradiation trials were made before the morphine injection (to serve as a control) and every 60 min after the morphine injection for 4 h. After the completion of the three doses, the specificity of the morphine effect was assessed with the opiate antagonist, naloxone. Naloxone (8 mg/kg) was administered intraperitoneally 30 min before administration of 10 mg/kg morphine, and laser irradiation of the tail was performed every 60 min after morphine (naloxone + morphine). Naloxone hydrochloride was obtained from Research Biochemical International (Natik, MA), and the morphine sulfate was obtained from the Narcotics Bureau, Taipei, Taiwan.
Neuronal activity was recorded using a 32-channel Multi-channel Neuronal Acquisition Processor system (MNAP, Plexon, Dallas, TX). The electrical signals were passed from the headset to an amplifier and band-passed filtered (spike preamp filter: 0.5 8.8 kHz, gain: 10,000 20,000; EEG and EMG filters: 3 90 Hz, gain: 5,000; or 0.7 170 Hz, gain: 2,500). Real-time spike sorting was controlled by SortClient (Plexon), and the sampling rate of individual channels was 40 kHz.
Two controls were performed to ascertain that at least a part of the short- and long-latency SmI and ACC neuronal responses were sensory in origin. The first control experiment used the same laser stimuli on anesthetized and paralyzed rats that had completed all of the above protocols. Three rats implanted with SmI and ACC microwire arrays were used. After a control set of stimuli consisting of 40 50 single pulses of 15-ms, 8-W laser-heat stimuli given to the middle part of the tail, the rat was anesthetized initially with 4% halothane. The femoral vein was cannulated, and a warm solution of 80 mg/kg 
-chloralose (Sigma, St. Louis, MO) in saline was given intravenously. One to 2 ml of 2% gallamine triethiodide (Sigma) was given intravenously until the rat stopped breathing and artificial ventilation commenced. The ventilation volume and rate were regulated so that the maximal end-expiratory CO2 concentration was maintained between 3.5 and 4.5%. The rectal temperature of the rat was monitored and feedback-regulated at 37.5°C with a thermal blanket (Harvard). The same set of laser-heat stimuli was used to stimulate the mid-tail of the rat. Supplementary doses of gallamine and chloralose were given as necessary.
The second control was a reanalysis of data similar to the control in our previous report on SmI units (Tsai et al. 2004). We noted that, with the 5-mg/kg dose of morphine, the rat flicked its tail about half of the time. These trials were divided into flick and no-flick groups and the perievent (laser-heat stimuli) histograms of the SmI and ACC units were separately analyzed. In this way, the effect of movement (tail flick) on the SmI and ACC responses to laser heat irradiation of the tail could be identified if it existed.
After the experiments were completed, electrical lesions (50 µA, 30 s) were made on selected electrodes of the microelectrode array. The animal was perfused intracardially with saline followed by 10% formalin. In several rats, the positions of the electrodes were marked by 30 s of a 5-µA positive current to deposit iron ions. The animals were perfused with 10% formalin containing 1% potassium ferrocyanide to display the iron deposition (Fig. 1A). Brains were removed and placed in the same perfusion fluid for 7 days. The frozen brain was serially sectioned at a 100-µm thickness with a sliding microtome. Sections were stained with crystal violet. The positions of the electrode tips were ascertained with camera lucida drawings under a stereomicroscope. Figure 1B shows the distribution of all electrode tips in the SmI and ACC.
|
The saved wavelet data were resorted using the software, Off-line Sorter, and analyzed using principal component analysis (PCA) and a template-matching algorithm (Plexon). Examples of SmI and ACC single units are shown in Figs. 2, 3, and 4. Spike activity was analyzed with the Neuroexplorer (Nex Technologies, Littleton, MA), Excel (Microsoft), and SigmaPlot (Jandel) programs. Peristimulation histograms were generated with a bin size of 10 ms. A "boxcar" filter (with a width of 3 bins) was used for postprocessing. Ensemble single-unit data (or single-unit data) were normalized as Z scores (Tsai et al. 2004). Briefly, the 0.5-s period before stimulation was used as the baseline period. The mean firing rate and SD of the 50 bins in this baseline period were calculated. All bin values were transformed to Z scores according to the mean and SD of the baseline period. A 99% confidence level (Z > 2.33 or Z < –2.33) was used for identifying the responsive single-unit activity (or ensemble single-unit activity). All of the units recorded from channels in the SmI tail region and responsive units in the ACC were summed to obtain the ensemble activities. The SmI tail region was identified by the brisk responses restricted to the tail when the rat was under anesthesia during the surgery for implantation and the day the animal was killed.
|
|
|
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
Supramaximal intensity of the CO2 laser (120 mJ; Yen et al. 1994) was used in this study to obtain consistent and reproducible behavioral responses. At this intensity, consistent with previous studies (Shaw et al. 1999, 2001; Tsai et al. 2004), short- (LEP1) and long-latency (LEP2) evoked potentials were recorded from the EEG skull electrode in the rostral parietal region. The average LEP1 and LEP2 values of the eight rats were 67 ± 3 and 356 ± 7 ms, respectively (Table 1).
|
), most of these SmI tail units (88%) responded to laser heat irradiation of the mid-tail (Table 2). The latencies of their laser heat responses were bimodally distributed as shown in Fig. 5. In the same population of rats, 125 single units were recorded in the ACC. There were also short- and long-latency responses of numerous ACC units after laser heat irradiation of the mid-tail (Table 2). Accordingly, 150 ms was used as a defining line for short- (
150 ms) and long-latency (>150 ms) cortical responses. Similar to units in the SmI, some units exhibited both short- and long-latency responses (6 units, 4.8%), whereas some had only a short-latency response (5 units, 4%), and more had only a long-latency response (32 units, 26%). Both short- and long-latency ACC unit responses peaked at longer latencies than did those of the SmI (Fig. 5). In addition, there were many ACC units that responded with initial latencies exceeding 600 ms. An example is shown in Fig. 4. The occurrence of different groups of units in the SmI and ACC as tested in the first control trial is summarized in Table 2. A 
2 test of this 2 x 6 contingency table showed that the distribution of the types of neurons in the SmI and ACC significantly differed (P < 0.001).
|
|
|
The effects of an intraperitoneal injection of morphine on the laser-heat–evoked cortical responses were studied with 2.5, 5, and 10 mg/kg doses in six rats. In each trial, 20–30 laser pulses were shone onto the mid-tail of the rat. Behaviorally, the laser-heat–evoked tail flick was affected (Fig. 7A). In control trials, tail flicks were elicited by 98 ± 1% of stimuli. The tail-flick behavior was inhibited most effectively 60 min after morphine administration at doses of 5 and 10 mg/kg (P < 0.01). The suppressive effect of 10 mg/kg morphine on the tail flick ratio lasted >120 min (P < 0.01). Tonic neck muscle EMG activity under the three morphine doses showed no significant difference during the 5-s periods before laser heat application, indicating no severe sedating effect by morphine.
|
). Similar results were obtained in this study. Figure 2 shows an example of morphine's effect on SmI unit responses. In trials performed 60 min after morphine administration (Fig. 2B), it can be seen that the short-latency responses in the SmI were not affected, whereas the long-latency ones were suppressed.
Laser-heat stimulation of the mid-tail also elicited fast and slow responses in the ACC (Figs. 3, 5, 6, and 8). In contrast to the differential effects on fast and slow responses of the SmI, morphine treatment suppressed both fast and slow responses of the ACC. A single-unit example is shown in Fig. 3. Fast and slow laser-heat–evoked responses of both units a and b in the ACC disappeared after an intraperitoneal injection of 10 mg/kg morphine. Ensemble SmI and ACC unit responses were statistically compared. Figure 8 shows results in one rat before and after treatment with 5 mg/kg morphine. Activities of a total of eight SmI units and seven ACC units were linearly summed and normalized to Z scores in this rat. In the control period, both SmI and ACC showed fast and slow ensemble responses. After a single dose of morphine, both fast and slow ACC responses drastically decreased, whereas in the SmI only the slow response was suppressed. The peak Z score values of the ensemble unit responses of the six rats are analyzed in Fig. 7, B and C. The SmI fast response did not significantly change with the three morphine doses (Fig. 7B), but the SmI slow response was significantly suppressed 60 min after the 5 mg/kg dose and for a longer duration after the 10 mg/kg dose (Fig. 7B). In sharp contrast, both the ACC fast and slow responses were very sensitive to morphine treatment. Both were significantly suppressed for 120 min by the 5 and 10 mg/kg doses of morphine (Fig. 7C). The fast ACC response was significantly suppressed for 240 min under the higher dose of 10 mg/kg (Fig. 7C).
|
2 test). In turn, SmI A0C+ units were significantly less affected than were the ACC A0C+ units (P < 0.05, 2 test).
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
In a recent paper (Tsai et al. 2004), we studied the responses of SmI units to laser-heat stimulation of the tail. As confirmed in this study, SmI units in the tail representation area respond to laser-heat pulses with either a short- and/or a long-latency response. When responses of many SmI units are summed, the ensemble activity consistently shows two peaks. These short- and the long-latency peaks match the LEP1-and LEP2-evoked potentials recorded by a screw over the skull of a rat, respectively. Single units were simultaneously recorded in the SmI and ACC in this study. About one-half of the ACC units also responded to laser stimulation of the tail. The most-prevalent types of responses observed in the ACC were also short- and long-latency responses (Table 2; Fig. 5). A new type of response pattern was found in the ACC, i.e., one with a very long-latency and long-lasting response (Figs. 4, 6, and 8; Table 2).
Outwardly they appeared similar, but when examined quantitatively, the short- and long-latency laser-heat–evoked responses in the ACC differed from those in the SmI. The percentage of ACC units that showed a short-latency response (defined as a latency <150 ms) was only 8.8% (A+C0 and A+C+ combined in Table 2), in contrast to the 43% in the SmI. The latency distribution of the short-latency response in the ACC ranged from 35 to 150 ms, with a median value of 125 ms, whereas the range in the SmI was from 30 to 100 ms, with a median value of 51 ms. The third difference in the short-latency response between the two areas was their sensitivity to morphine treatment. The SmI short-latency laser-heat–evoked response was not affected by morphine, even under a very large dose of 10 mg/kg. In contrast, the ACC short-latency response was very sensitive to morphine, and the inhibition was the strongest and the longest (cf. Fig. 7, B and C).
Percentage-wise, the ACC had far fewer units that responded in the long-latency range (defined as a latency exceeding 150 ms) to laser stimulation of the tail (38 of 125, 30%) than did the SmI (57 of 74, 77%). In other aspects, laser-heat–evoked long-latency responses in the SmI and ACC were more alike. Long-latency responses in both places had the highest peak, in the range of 300 350 ms, although the average latency in the SmI was consistently shorter than that in the ACC (Figs. 5 and 6). SmI and ACC long-latency responses were suppressed to a comparable degree by 5 and 10 mg/kg of morphine treatment for 120 min (Fig. 7, B and C).
Laser irradiation has been used as a specific noxious stimulus since the mid-1970s (Carmon et al. 1976, 1978). The 10.6-µm wavelength infrared radiation of the CO2 laser selectively activates nociceptive receptors and generates a pure pain sensation, which is conveyed through both myelinated A-
and unmyelinated C fibers to the cerebral cortex in humans (Bromm and Treede 1984, 1987). Two cortical laser-evoked potentials (LEP1 and LEP2) have been recorded from the cerebral cortex of the rat (Shaw et al. 1999, 2001). The conduction velocities of the peripheral fibers responsible for the activation of these LEPs have been estimated. Kalliomaki et al. (1993) stimulated different proximo-distal locations of the hindpaw of halothane-anesthetized rats. A single long-latency cortical evoked potential was observed, and its peripheral conduction velocity was estimated to be 0.7 m/s. Shaw et al. (1999) stimulated different proximo-distal locations of the tail of conscious rats. LEP1 and LEP2 were observed, and their peripheral conduction velocities were estimated to be 22 and 0.7 m/s, respectively. Sun et al. (2003) analyzed the current source density of laser-evoked field potentials in the SmI of lightly anesthetized rats. Two major components were identified intracortically after laser stimulation of different proximo-distal locations of the hindpaw. Their conduction velocities from that research corresponded to the A- and C fiber ranges, respectively.
In this study, two consistent components of the ensemble unit responses to laser-heat irradiation of the tail were identified in both the SI and ACC (Figs. 2, 3, 5, 6, and 8). Although a direct study has yet to be performed for the ACC, our working hypothesis is that the two components in both regions arise primarily from A- and C fiber inputs, respectively. We showed here, in addition, that the response latencies in the ACC were longer than those in the SI. This is most likely due to the nature of synaptic transfer along the afferent pathways going to the two regions. The SI receives its major afferent input from the ventroposteriolateral nucleus of the lateral thalamic pathway, in contrast to the ACC, which receives inputs from the medial thalamic pathway. The results in this brought forth a direct comparison of nociceptive signal transferring in the lateral and the medial thalamic pathways both in their synaptic efficacy and their modulation by morphine.
The emphasis of this study was on single units and regional ensemble unit study of cortical processing of nociceptive information. There have been many SI and ACC single-unit studies of their nociceptive information processing. Except for a very limited number of studies (Iwata et al. 1998; Kenshalo et al. 1988; Tsai et al. 2004; Wang et al. 2003), most studies were performed on the SI in anesthetized animals (Chudler et al. 1990; Iwata et al. 1990; Kalliomaki et al. 1993; Kenshalo and Isensee 1983; Kenshalo et al. 2000; Lamour et al. 1982, 1983a,b; Matsumoto et al. 1989) and in the ACC (Sikes and Vogt 1992; Vogt and Sikes 2000; Yamamura et al. 1996; Zhang et al. 2004). SI nociceptive neurons have relatively smaller receptive fields. The activities of these neurons show good coding ability for stimulation intensity. In contrast, the receptive fields of nociceptive neurons in the ACC are larger and usually bilateral. Using the ensemble unit-recording technique, this study adds quantitative information about the nociceptive processing of SI and ACC neurons. In addition, by simultaneously recording as many as 20 single units in the SI and ACC in the same animal, populations of SI and ACC neuronal activities could be compared. Although individual single units showed variable response patterns, collectively, fairly robust responses to noxious laser-heat were observed in both the SI and ACC. Ensemble activity of the SI showed consistently faster and stronger short- and long-latency responses than those of the ACC. An unexpected finding revealed by this analysis was a long-duration response of the ACC ensemble activity (Figs. 4 and 6), which could last for more than a few seconds. This is a pattern similar to the result obtained in the ACC with magnetoencephalograms of human subjects in response to single shots of laser-heat applied to the dorsum of the hand (Ploner et al. 2002). How this slower-onset, longer-duration response in the ACC contributes to affective, attentional, or cognitive aspects of pain function awaits further experimentation.
Another set of data of this study relates to the effect of morphine (ip) on the laser-heat–evoked cortical responses. Interestingly, the ACC showed higher sensitivity to morphine treatment than did the SI (Fig. 7; Table 3). This is consistent with the biochemical findings of a higher density of opiate receptors in the limbic cortex, including the ACC (Jones et al. 1991; Lewis et al. 1983; Mansour et al. 1986, 1987). It has been shown that morphine at lower doses is effective in reducing pain emotion and that a higher dose is required to decrease the pain sensation (Price et al. 1985). Thus it may be possible to dissect different components of pain pharmacologically by the use of morphine. By showing that the ACC ensemble unit response to noxious heat stimuli is more sensitive to morphine treatment, our data added cellular evidence in support of the important role of the ACC in the emotional function of pain (Hamner et al. 1999; Johansen et al. 2001; Kung et al. 2003).
In summary, by using a modified tail-flick model in conscious rats, this study showed many interesting differences in laser-heat–evoked responses in the SmI and ACC. Differential sensitivities of these nociceptive responses to morphine treatment were also quantified. These data may be useful in dissecting the mechanisms of different aspects of pain function.
|
GRANTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
|
ACKNOWLEDGMENTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
|
FOOTNOTES |
|---|
Address for reprint requests and other correspondence: C.-T. Yen, Inst. of Zoology, National Taiwan Univ., No.1 Roosevelt Rd., Section 4, Taipei 106, Taiwan (E-mail: ctyen{at}ntu.edu.tw)
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
Bromm B and Treede RD. Human cerebral potentials evoked by CO2 laser stimuli causing pain. Exp Brain Res 67: 153–162, 1987.[CrossRef][Web of Science][Medline]
Calejesan AA, Kim SJ, and Zhuo M. Descending facilitatory modulation of a behavioral nociceptive response by stimulation in the adult rat anterior cingulate cortex. Eur J Pain 4: 83–96, 2000.[CrossRef][Web of Science][Medline]
Carmon A, Dotan Y, and Sarne Y. Correlation of subjective pain experience with cerebral evoked responses to noxious thermal stimulations. Exp Brain Res 33: 445–453, 1978.[Web of Science][Medline]
Carmon A, Mor J, and Goldberg J. Evoked cerebral responses to noxious thermal stimuli in humans. Exp Brain Res 25: 103–107, 1976.[Web of Science][Medline]
Casey KL, Minoshima S, Berger KL, Koeppe RA, Morrow TJ, and Frey KA. Positron emission tomographic analysis of cerebral structures activated specifically by repetitive noxious heat stimuli. J Neurophysiol 71: 802–807, 1994.
Chapin JK and Lin CS. Mapping the body representation in the SI cortex of anesthetized and awake rats. J Comp Neurol 229: 199–213, 1984.[CrossRef][Web of Science][Medline]
Chudler EH, Anton F, Dubner R, and Kenshalo DR Jr. Responses of nociceptive SI neurons in monkeys and pain sensation in humans elicited by noxious thermal stimulation: effect of interstimulus interval. J Neurophysiol 63: 559–569, 1990.
Coghill RC, Sang CN, Maisog JM, and Iadarola MJ. Pain intensity processing within the human brain: a bilateral, distributed mechanism. J Neurophysiol 82: 1934–1943, 1999.
Coghill RC, Talbot JD, Evans AC, Meyer E, Gjedde A, Bushnell MC, and Duncan GH. Distributed processing of pain and vibration by the human brain. J Neurosci 14: 4095–4108, 1994.[Abstract]
Craig AD. Pain mechanisms: labeled lines versus convergence in central processing. Annu Rev Neurosci 26: 1–30, 2003.[Medline]
Craig AD, Reiman EM, Evans A, and Bushnell MC. Functional imaging of an illusion of pain. Nature 384: 258–260, 1996.[CrossRef][Medline]
Davis KD, Wood ML, Crawley AP, and Mikulis DJ. fMRI of human somatosensory and cingulate cortex during painful electrical stimulation. Neuroreport 7: 321–325, 1995.[Web of Science][Medline]
Dorbyshire SW, Jones AK, Gyulai F, Clark S, Townsend D, and Firestone LL. Pain processing during three levels of noxious stimulation produces differential patterns of central activity. Pain 73: 431–445, 1997.[CrossRef][Web of Science][Medline]
Hamner MB, Lorberbaum JP, and George MS. Potential role of the anterior cingulate cortex in PTSD: review and hypothesis. Depress Anxiety 9: 1–14, 1999.[CrossRef][Medline]
Hofbauer RK, Rainville P, Duncan GH, and Bushnell MC. Cortical representation of the sensory dimension of pain. J Neurophysiol 86: 402–411, 2001.
Hsieh JC, Belfrage M, Stone-Elander S, Hansson P, and Ingvar M. Central representation of chronic ongoing neuropathic pain studied by positron emission tomography. Pain 63: 225–236, 1995.[CrossRef][Web of Science][Medline]
Hsu MM and Shyu BC. Electrophysiological study of the connection between medial thalamus and anterior cingulate cortex in the rat. Neuroreport 8: 2701–2707, 1997.[Web of Science][Medline]
Hutchison WD, Davis KD, Lozano AM, Tasker RR, and Dostrovsky JO. Pain-related neurons in the human cingulate cortex. Nat Neurosci 2: 403–405, 1999.[CrossRef][Web of Science][Medline]
Iwata K, Tsuboi Y, Muramatsu H, and Sumino R. Distribution and response properties of cat SI neurons responsive to changes in tooth temperature. J Neurophysiol 64: 822–834, 1990.
Iwata K, Tsuboi Y, and Sumino R. Primary somatosensory cortical neuronal activity during monkey's detection of perceived change in tooth-pulp stimulus intensity. J Neurophysiol 79: 1717–1725, 1998.
Johansen JP and Fields HL. Glutamatergic activation of anterior cingulate cortex produces an aversive teaching signal. Nat Neurosci 7: 398–403, 2004.[CrossRef][Web of Science][Medline]
Johansen JP, Fields HL, and Manning BH. The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex. Proc Natl Acad Sci USA 98: 8077–8082, 2001.
Jones AK, Qi LY, Fujirawa T, Luthra SK, Ashburner J, Bloomfield P, Cunningham VJ, Itoh M, Fukuda H, and Jones T. In vivo distribution of opioid receptors in man in relation to the cortical projections of the medial and lateral pain systems measured with positron emission tomography. Neurosci Lett 126: 25–28, 1991.[CrossRef][Web of Science][Medline]
Kalliomaki J, Luo XL, Yu YB, and Schouenborg J. Intrathecally applied morphine inhibits nociceptive C fiber input to the primary somatosensory cortex of the rat. Pain 77: 323–329, 1998.[CrossRef][Web of Science][Medline]
Kalliomaki J, Weng HR, Nilsson HJ, and Schouenborg J. Nociceptive C fibre input to the primary somatosensory cortex (SI). A field potential study in the rat. Brain Res 622: 262–270, 1993.[CrossRef][Web of Science][Medline]
Kenshalo DR Jr., Chudler EH, Anton F, and Dubner R. SI nociceptive neurons participate in the encoding process by which monkeys perceive the intensity of noxious thermal stimulation. Brain Res 454: 378–382, 1988.[CrossRef][Web of Science][Medline]
Kenshalo DR Jr. and Isensee O. Responses of primate SI cortical neurons to noxious stimuli. J Neurophysiol 50: 1479–1496, 1983.
Kenshalo DR, Iwata K, Sholas M, and Thomas DA. Response properties and organization of nociceptive neurons in area 1 of monkey primary somatosensory cortex. J Neurophysiol 84: 719–729, 2000.
Kung JC, Su NM, Fan RJ, Chai SC, and Shyu BC. Contribution of the anterior cingulate cortex to laser-pain conditioning in rats. Brain Res 970: 58–72, 2003.[CrossRef][Web of Science][Medline]
Kuo CC and Yen CT. Comparison of responses to noxious laser stimuli of neurons in the primary somatosensory cortex and anterior cingulate cortex of the rat. 33rd Annual Meeting of the Society for Neuroscience, New Orleans, LA, 2003.
Lamour Y, Guilbaud G, and Willer JC. Rat somatosensory (SmI) cortex: II. Laminar and columnar organization of noxious and non-noxious inputs. Exp Brain Res 49: 46–54, 1983a.[Web of Science][Medline]
Lamour Y, Willer JC, and Guilbaud G. Neuronal responses to noxious stimulation in rat somatosensory cortex. Neurosci Lett 29: 35–40, 1982.[CrossRef][Web of Science][Medline]
Lamour Y, Willer JC, and Guilbaud G. Rat somatosensory (SmI) cortex: I. Characteristics of neuronal responses to noxious stimulation and comparison with responses to non-noxious stimulation. Exp Brain Res 49: 35–45, 1983b.[Web of Science][Medline]
Lewis ME, Pert A, Pert CB, and Herkenham M. Opiate receptor localization in rat cerebral cortex. J Comp Neurol 216: 339–358, 1983.[CrossRef][Web of Science][Medline]
Lorenz J, Beck H, and Bromm B. Cognitive performance, mood and experimental pain before and during morphine-induced analgesia in patients with chronic non-malignant pain. Pain 73: 369–375, 1997.[CrossRef][Web of Science][Medline]
Mansour A, Khachaturian H, Lewis ME, Akil H, and Watson SJ. Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain. J Neurosci 7: 2445–2464, 1987.[Abstract]
Mansour A, Lewis ME, Khachaturian H, Akil H, and Watson SJ. Pharmacological and anatomical evidence of selective mu, delta, and kappa opioid receptor binding in rat brain. Brain Res 399: 69–79, 1986.[CrossRef][Web of Science][Medline]
Matsumoto N, Sato T, and Suzuki TA. Characteristics of the tooth pulp-driven neurons in a functional column of the cat's somatosensory cortex (SI). Exp Brain Res 74: 263–271, 1989.[Web of Science][Medline]
Merskey H. Classification of chronic pain. Descriptions of chronic pain syndromes and definition of pain terms. Pain Suppl 3: S1–S225, 1986.[Medline]
Paxinos G and Watson C. The Rat Brain in Stereotaxic Coordinates (4th ed.). San Diego, CA: Academic Press, 1998.
Ploner M, Gross J, Timmermann L, and Schnitzler A. Cortical representation of first and second pain sensation in humans. Proc Natl Acad Sci USA 99: 12444–12448, 2002.
Price DD, Von der Gruen A, Miller J, Rafii A, and Price C. A psychophysical analysis of morphine analgesia. Pain 22: 261–269, 1985.[CrossRef][Web of Science][Medline]
Rainville P, Duncan GH, Price DD, Carrier B, and Bushnell MC. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277: 968–971, 1997.
Shaw FZ, Chen RF, Tsao HW, and Yen CT. Comparison of touch- and laser heat-evoked cortical field potentials in conscious rats. Brain Res 824: 183–196, 1999.[CrossRef][Web of Science][Medline]
Shaw FZ, Chen RF, and Yen CT. Dynamic changes of touch- and laser heat-evoked field potentials of primary somatosensory cortex in awake and pentobarbital-anesthetized rats. Brain Res 911: 105–115, 2001.[CrossRef][Web of Science][Medline]
Sikes RW and Vogt BA. Nociceptive neurons in area 24 of rabbit cingulate cortex. J Neurophysiol 68: 1720–1732, 1992.
Sun JJ, Yang JW, Chang MH, Chou PH, and Shyu BC. The current source density analysis of laser-evoked potentials using multichannel recordings in the somatosensory cortex of rats. 33rd Annual Meeting of the Society for Neuroscience, New Orleans, LA, 2003.
Talbot JD, Marrett S, Evans AC, Meyer E, Bushnell MC, and Duncan GH. Multiple representations of pain in human cerebral cortex. Science 251: 1355–1358, 1991.
Tsai ML, Kuo CC, Sun WZ, and Yen CT. Differential morphine effects on short- and long-latency laser-evoked cortical responses in the rat. Pain 110: 665–674, 2004.[CrossRef][Web of Science][Medline]
Tsai ML and Yen CT. A simple method for fabricating horizontal and vertical microwire arrays. J Neurosci Methods 131: 107–110, 2003.[CrossRef][Web of Science][Medline]
Tuor UI, Malisza K, Foniok T, Papadimitropoulos R, Jarmasz M, Somorjai R, and Kozlowski P. Functional magnetic resonance imaging in rats subjected to intense electrical and noxious chemical stimulation of the forepaw. Pain 87: 315–324, 2000.[CrossRef][Web of Science][Medline]
Vogt BA, Derbyshire S, and Jones AK. Pain processing in four regions of human cingulate cortex localized with co-registered PET and MR imaging. Eur J Neurosci 8: 1461–1473, 1996.[CrossRef][Web of Science][Medline]
Vogt BA and Sikes RW. The medial pain system, cingulate cortex, and parallel processing of nociceptive information. Prog Brain Res 122: 223–235, 2000.[Web of Science][Medline]
Wang JY, Luo F, Chang JY, Woodward DJ, and Han JS. Parallel pain processing in freely moving rats revealed by distributed neuron recording. Brain Res 992: 263–271, 2003.[CrossRef][Web of Science][Medline]
Willis WD. The Pain System. The Neural Basis of Nociceptive Transmission in the Mammalian Nervous System. Basel: Karger, 1985.
Yamamura H, Iwata K, Tsuboi Y, Toda K, Kitajima K, Shimizu N, Nomura H, Hibiya J, Fujita S, and Sumino R. Morphological and electrophysiological properties of ACCx nociceptive neurons in rats. Brain Res 735: 83–92, 1996.[Web of Science][Medline]
Yen CT, Huang CH, and Fu SE. Surface temperature change, cortical evoked potential and pain behavior elicited by CO2 lasers. Chin J Physiol 37: 193–199, 1994.[Medline]
Zhang R, Tomida Y, Katayama Y, and Kawakami Y. Response durations encode nociceptive stimulus intensity in the rat medial prefrontal cortex. Neuroscience 125: 777–785, 2004.[CrossRef][Web of Science][Medline]
This article has been cited by other articles:
|
|
 |
|
  C.-C. Kuo, R.-J. Chiou, K.-C. Liang, and C.-T. Yen Differential Involvement of the Anterior Cingulate and Primary Sensorimotor Cortices in Sensory and Affective Functions of Pain J Neurophysiol, March 1, 2009; 101(3): 1201 - 1210. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-W. Yang, H.-C. Shih, and B.-C. Shyu Intracortical Circuits in Rat Anterior Cingulate Cortex Are Activated by Nociceptive Inputs Mediated by Medial Thalamus J Neurophysiol, December 1, 2006; 96(6): 3409 - 3422. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
