The Journal of Neurophysiology Vol. 78 No. 1 July 1997, pp. 521-527
Copyright ©1997 by the American Physiological Society

RAPID COMMUNICATION

Nucleus Gracilis: An Integrator for Visceral and Somatic Information

Elie D. Al-Chaer, Karin N. Westlund, and William D. Willis

Department of Anatomy and Neurosciences, University of Texas Medical Branch, Galveston, Texas 77555-1069

	ABSTRACT

Abstract Introduction Methods Results Discussion References

Al-Chaer, Elie D., Karin N. Westlund, and William D. Willis. Nucleus gracilis: an integrator for visceral and somatic information. J. Neurophysiol. 78: 521-527, 1997. The nucleus gracilis (NG) receives an abundance of visceral input from various abdominal organs and is proposed to play an important role in visceral pain processing. The purpose of this study was to investigate the necessity of the NG for colorectal input into the ventral posterolateral (VPL) nucleus of the thalamus. Single-cell recordings were made from nine VPL cells isolated in nine different male Sprague Dawley rats anesthetized with pentobarbital sodium. Responses of the VPL cells to colorectal distension (CRD) and to cutaneous stimuli were obtained before and after lesioning of the NG. Electrolytic (n = 5) and chemical (n = 4) lesions of the NG were made in different preparations. The chemical lesions were made by injecting a solution of kainic acid into the NG. Kainic acid presumably kills neuronal cell bodies and spares axons of passage. The results indicate that a lesion of the NG, regardless of its type, reduces dramatically the responses of VPL neurons to innocuous cutaneous stimuli, and, to a lesser extent, the responses to CRD. Attenuation of VPL neuronal responses to CRD as well as to innocuous cutaneous stimuli by the NG lesions emphasizes the role of the dorsal column in visceral nociception and suggests that the NG is an integration center for visceral and cutaneous information flowing into the VPL nucleus.

	INTRODUCTION

Abstract Introduction Methods Results Discussion References

The nucleus gracilis (NG) plays an important role in processing pelvic visceral input and relaying it to the ventral posterolateral (VPL) nucleus of the thalamus. Single cells in the NG that can be antidromically activated from the VPL nucleus or the medial lemniscus (ML) respond to mechanical and chemical stimulation of the descending colon and rectum as well as to cutaneous stimuli (Al-Chaer et al. 1996b). Although cutaneous input into the NG is mostly mediated by primary afferent projections, the visceral input is believed largely to involve a synaptic relay between primary afferents and postsynaptic dorsal column (DC) neurons (Al-Chaer et al. 1996b). Earlier studies have shown that field potentials and single-unit responses can be recorded from the DC nuclei (DCN), mainly the NG, in response to splanchnic nerve stimulation in the cat (Aidar et al. 1952; Rigamonti and Hancock 1974, 1978). Recently, Berkley and Hubscher (1995) reported that 50% of their sample of neurons in the NG that responded to gentle skin stimulation also responded to uterine and vaginal distension. Anatomically, the NG has been shown to receive primary afferents from the splanchnic nerve (Kuo and De Groat 1985) and nonprimary afferents from the lumbar and sacral cord (Cliffer and Giesler 1989; Hirshberg et al. 1996; Rustioni 1973). Input into the NG is carried mainly by fibers that ascend in the DC. Aidar et al. (1952) recorded fast responses to splanchnic nerve stimulation, "in logical time relationships," in the ipsilateral fasciculus gracilis of the spinal cord, the ipsilateral NG, and the region of decussation of the ML. Moreover, our group has shown that visceral as well as cutaneous input into the NG can be abolished by a lesion of the DC at the level of T₁₀ (Al-Chaer et al. 1996b). The T₁₀ DC lesion also dramatically reduced the responses of VPL cells to visceral and innocuous cutaneous stimuli (Al-Chaer et al. 1996a).

Although it is clear that visceral responses can be recorded from neurons of the NG that project to the VPL nucleus, this does not define the NG as a relay for visceral information carried in the DC into the VPL nucleus, nor does it rule out relays for visceral information in nuclei other than the NG. For instance, visceral information carried by DC axons could be relayed via DC collaterals onto spinothalamic tract neurons located in the upper cervical spinal cord (Burstein et al. 1990; Kemplay and Webster 1989). Axons of cervical spinothalamic tract neurons could then convey the visceral information to the VPL nucleus. The purpose of this study was to investigate how essential the NG is for colorectal input into the VPL nucleus of the thalamus. Therefore recordings were made from single cells in the VPL nucleus in response to graded colorectal distension (CRD) and to cutaneous stimuli before and after a lesion of the NG. The hypothesis was that lesioning of the NG would reduce the responses of VPL cells to CRD and innocuous cutaneous stimuli as effectively as a DC lesion, indicating that visceral input carried by DC axons into the VPL nucleus is largely relayed in the NG. The lesions were made either by passing current through an electrode inserted into the NG or by an injection of kainic acid into the NG. A preliminary report of this work has been made (Westlund et al. 1996).

	METHODS

Abstract Introduction Methods Results Discussion References

Experiments were performed on nine male Sprague-Dawley rats weighing between 280 and 350 g. The rats were initially anesthetized with an intraperitoneal injection of pentobarbital sodium (40 mg/kg). The trachea was intubated and a catheter was inserted into one of the jugular veins to allow a continuous infusion of the anesthetic (5 mg·kg¹·h¹). Body temperature was monitored and kept around 37°C by a servo-controlled heated blanket. The head of the rat was fixed in a stereotaxic instrument. An incision was made in the skin over the head and the cervical vertebral column. The underlying muscles were retracted. A craniotomy was made to expose the area of cortex above the thalamus. Part of the occipital bone above the cerebellum was removed and a small laminectomy was made to expose C₁. The procedure allowed easy access to the NG while enabling recordings from the thalamus. The dura mater was cut and exposed brain tissues were covered with warm mineral oil.

Stimulation

The visceral stimulus used was CRD. CRD was applied with the use of an inflatable balloon inserted rectally into the descending colon to 7 cm from the anus (for details on the setup and the balloon preparation, see Al-Chaer et al. 1996a; Gebhart and Sengupta 1996). The CRD consisted of consecutive inflations of the balloon to pressures ranging between 20 and 80 mmHg, applied in increments of 20 mm for 20 s every 4 min. CRD stimuli having an intensity >40 mmHg are considered noxious (Ness and Gebhart 1988; Ness et al. 1990). Cutaneous stimuli consisted of brushing the receptive field with the use of a camel hair brush (BR), applying pressure to a fold of skin with the use of an arterial clip with a weak grip (PR), and pinching a fold of skin with the use of an arterial clip with a strong grip (PI). BR and PR are considered innocuous, whereas PI is considered noxious (for more details on the characteristics of the cutaneous stimuli and properties of the neurons, see Al-Chaer et al. 1996a,b).

View larger version (124K): [in this window] [in a new window]   FIG. 1. Photomicrograph of section through rat brain stem. Arrow: site of electrolytic lesion in nucleus gracilis (NG).

Recordings

Recordings from individual neurons of the VPL nucleus were performed with the use of tungsten microelectrodes (125 µm, shank; 12 M). The electrode was inserted stereotaxically into the brain, aiming for the VPL area. The electrode was lowered slowly while brief taps were applied to the contralateral hindlimb or the perineal area. When multiunit activity became distinctly audible, the site coordinates were recorded and the electrode was moved in small increments until a VPL unit was well isolated. The cutaneous receptive field was mapped and the unit's response to CRD was determined. Extracellular action potentials were fed into a window discriminator and displayed on an oscilloscope screen. The output of the window discriminator and amplifier were led into a data collection system (CED 1401 +) and a personal computer to compile rate histograms or wavemark files. Responses of a VPL cell to consecutive applications of cutaneous stimuli (BR, PR, and PI) were recorded. The responses are expressed as the average rate of firing of the cell during a particular stimulus minus the average baseline rate. The responses to CRD, on the other hand, were stored separately. Twenty seconds of baseline activity preceded the application of a distension stimulus. Each stimulus lasted 20 s. Four minutes were allowed to elapse between two consecutive stimuli. The responses were calculated as the difference between the rate of firing during the response and that during the baseline recording. The responses obtained before the NG lesion were considered as controls. Those obtained after the lesion were calculated as a percentage of the controls.

Lesions of the NG

Electrolytic (n = 5) or chemical (n = 4) lesions of the NG were made. For an electrolytic lesion (n = 5), an extra fine microelectrode (125-µm tip) was inserted into the nucleus at the level of the obex, 0.5-1 mm from the midline and under view through a surgical microscope. The electrode was advanced 100-300 µm beneath the surface. The lesion was made by passing a continuous current (250 µA for 30 s) through the electrode.

Chemical lesions were made by injecting a solution of kainic acid into the NG (Coyle et al. 1978). The kainic acid solution was prepared by diluting kainic acid (Sigma Chemical) in 0.14 M NaCl (5 mg/ml) and titrating to pH 7.4 with NaOH. Ten microliters of the solution were obtained in a Hamilton microsyringe. A micropipette tip was glued to the tip of the Hamilton syringe and filled with the solution. The syringe was the mounted on a micromanipulator and its tip was slowly advanced into the NG. The desired target was similar to that described for the electrolytic lesion. The solution of kainic acid was slowly injected into the NG over a period of 1 min.

Histology

At the end of each experiment the recording site in the VPL nucleus was marked by passing a continuous current (250 µA for 20 s). The animal was then transcardially perfused with 4% paraformaldehyde. The rostralmost spinal cord and the brain were removed and incubated in 20% sucrose before frozen sectioning at 50 µm. The sections were stained with cresyl violet. The VPL recording sites were identified and the extent of each NG lesion was reconstructed.

View larger version (14K): [in this window] [in a new window]   View larger version (16K): [in this window] [in a new window]   FIG. 2. A and B: responses of a ventral posterolateral (VPL) neuron to colorectal distension (CRD) 80 mmHg in intensity before (A) and after (B) an electrolytic lesion of NG. C and D: responses of same VPL neuron to cutaneous stimulation [brush (BR), pressure (PR), and pinch (PI)] before (C) and after (D) NG lesion.

Statistical analysis

The responses of VPL cells to visceral and cutaneous stimuli obtained before and after the NG lesions were analyzed for statistical significance with the use of a repeated-measures analysis of variance. Significant effects were evaluated with the use of Bonferroni's multiple comparison method versus a control group. Differences were considered significant if a Bonferroni corrected value of P < 0.05 was obtained.

	RESULTS

Abstract Introduction Methods Results Discussion References

Recordings were made from nine VPL cells isolated in nine different preparations. Five VPL cells were tested before and after an electrolytic lesion of the NG was made contralateral to the recording site. Four other VPL cells were tested before and after an injection of kainic acid into the NG. The cells responded to CRD of 20, 40, 60, and 80 mmHg in intensity and also to cutaneous stimuli. The responses to 80-mmHg CRD ranged between 7.2 and 48.8 spikes/s, with an average of 16.6 ± 4.3 (SE) spikes/s. The cells also responded to cutaneous stimuli. The responses to BR ranged between 4 and 66 spikes/s, with an average of 18.3 ± 6.4 spikes/s. The cutaneous receptive fields of these cells were located in the perineal and hindlimb areas.

Effect of the electrolytic lesions

Electrolytic lesions of the NG reduced dramatically the responses of these cells to CRD. The responses to 80-mmHg distension, for instance, ranged after the lesion between 3.0 and 16.5 spikes/s, with an average of 6.5 ± 2.6 spikes/s, a reduction of 66.3% from the average response before the lesion. The responses to cutaneous stimuli, on the other hand, were differentially affected by the lesion of the NG. Responses to BR were dramatically reduced and ranged between 1.4 and 8.3 spikes/s, with an average of 3.7 ± 1.2 spikes/s, a reduction of 84.4% from their initial average response. Responses to PI, however, did not change significantly.

View larger version (123K): [in this window] [in a new window]   FIG. 3. Photomicrograph of section through rat brain stem. Arrow: site of injection of kainic acid.

Figure 1 shows photomicrographs of the site of the smallest electrolytic NG lesion that had an effect on VPL neuronal responses, in low- (×2, Fig. 1A) and high-power magnification (×20, Fig. 1B). The responses of the VPL cell in this experiment, recorded before and after the NG lesion, are shown in Fig. 2. Figure 2A shows the response of the VPL cell to CRD 80 mmHg in intensity before the NG lesion. The mean frequency of the response was 20.8 spikes/s before the NG lesion and 3.5 spikes/s after the lesion. Figure 2, C and D, shows the responses of the same VPL cell to cutaneous stimuli before and after the NG lesion, respectively. The response to BR decreased from 6.6 spikes/s before the lesion to 0.4 spikes/s after the lesion. On the other hand, the response to PI increased from 1.7 spikes/s before the NG lesion to 3.0 spikes/s after the lesion.

Effect of the chemical lesions

The effects of the chemical lesions of the NG were also potent and significant. The responses of four VPL cells tested to 80 mmHg CRD were reduced by 50.7% after the injection of kainic acid. The average response to BR was reduced by 80.7%. Responses to PI, on the other hand, did not change significantly after the injection of kainic acid.

Figure 3 shows photomicrographs of the injection site in one experiment at low- (×2, Fig. 3A) and high-power magnification (×40, Fig. 3B). The responses of the VPL cell tested before and after the lesion in Fig. 3 are shown in Fig. 4. The response of the VPL cell to CRD of an intensity of 80 mmHg was 13.4 spikes/s before the NG lesion (Fig. 4A) and 3.5 spikes/s after the NG lesion (Fig. 4B). The response to BR decreased from 23.4 spikes/s before the NG lesion (Fig. 4C) to 7.4 spikes/s after the NG lesion (Fig. 4D). The cell did not respond initially to PI; however, after the NG lesion the response to PI was 2.4 spike/s.

View larger version (21K): [in this window] [in a new window]   View larger version (16K): [in this window] [in a new window]   FIG. 4. A and B: responses of a VPL neuron to CRD 80 mmHg in intensity before (A) and after (B) an injection of kainic acid into NG. C and D: responses of same VPL neuron to cutaneous stimulation (BR, PR, and PI) before (C) and after (D) chemical lesion of NG.

Cumulative effect of both electrolytic and chemical lesions

No significant difference between the effect of the electrolytic lesion of the NG and that of the chemical lesion on the responses of the VPL cells to either visceral or cutaneous stimuli was observed (Fig. 5). Therefore the two populations were pooled together and the data are presented as the mean effect of both lesions. Figure 6 shows the cumulative effect of both the electrolytic and the chemical lesions of the NG on the responses of VPL cells to CRD (A) and cutaneous stimuli (B). Responses to 80-mmHg CRD show a significant reduction of 59.8 ± 3.4%. Responses to BR were also significantly reduced by 80.6 ± 3.3%. The responses to PR were significantly reduced by 46.2 ± 11.6%. The responses to PI did not significantly change, although there was a tendency for them to be increased in some cells.

View larger version (18K): [in this window] [in a new window]   FIG. 5. Line graphs illustrating average responses (means ± SE) of 9 VPL neurons to graded CRD (20, 40, 60, and 80 mmHg) before lesion of NG, after an electrolytic lesion of NG (n = 5), and after a chemical lesion of NG (n = 4). Asterisks: P  0.05.

View larger version (19K): [in this window] [in a new window]   FIG. 6. Bar graphs illustrating % change (mean ± SE) of the responses of 9 VPL neurons to CRD (A) and to cutaneous stimuli (B) induced by electrolytic and chemical lesions of NG. Negative changes: % reduction of responses obtained after lesion as compared with those obtained before lesion. Positive change: % increase.

	DISCUSSION

Abstract Introduction Methods Results Discussion References

The results obtained indicate that lesions of the NG reduce the responses of VPL cells to CRD and also to innocuous mechanical cutaneous stimuli. The NG lesions did not have a significant effect on the responses to noxious mechanical cutaneous stimuli. The findings imply that the NG is involved in mediating noxious visceral and innocuous cutaneous inputs into the VPL nucleus of the thalamus.

The results also indicate that transmission of visceral information flow through the DC into the VPL nucleus of the thalamus most likely involves a synaptic connection at the level of the NG. This is evident from the effects of the chemical lesions. Kainic acid injection would presumably kill neuronal cell bodies in the NG while sparing axons of passage (Coyle et al. 1978). The effect of the electrolytic lesion, on the other hand, was not significantly different from that of the chemical lesion, indicating that axons of passage across the NG play a minor role, if any, in relaying visceral information to the VPL nucleus. The lack of any significant effect on the responses to noxious mechanical cutaneous stimuli substantiates earlier findings (Al-Chaer et al. 1996a) that the DC plays a minor role in relaying excitatory noxious cutaneous input to the VPL nucleus. This input is largely carried by pathways in the ventrolateral column of the spinal cord, such as the spinothalamic tract. However, the tendency for the responses to noxious PI to increase seen after the NG lesion might be due to the removal of a masking effect of the DC input on these responses.

These results were anticipated on the basis of earlier studies that have demonstrated that the NG receives an important input from the pelvic viscera (Al-Chaer et al. 1996b; Berkley and Hubscher 1995). This input is projected in the DC and is largely mediated by postsynaptic DC fibers (Al-Chaer et al. 1996b). Severing these fibers at the level of T₁₀ interrupts pelvic visceral input into the NG as well as into the VPL nucleus of the thalamus. It is likely that a similar relationship of the nucleus cuneatus to upper abdominal and thoracic viscera exists (Chandler et al. 1996).

Several studies (Al-Chaer et al. 1996b; Berkley and Hubscher 1995; Cliffer et al. 1992; Dostrovsky and Millar 1977) have shown that cells in the DCN have access to converging sources of information about innocuous and noxious events taking place in the pelvic viscera as well as in the skin. This situation was regarded as similar to that in the spinal cord (Berkley and Hubscher 1995) in that the DC-DCN resemble the spinal dorsal horn-spinothalamic tract in the access to convergent input from viscera and skin, which led to the conclusion that the DC might as well be involved in visceral pain. Apkarian et al. (1995) suggested that the DC may be more important for visceral pain than is the spinothalamic tract. Our group found that the DC carries the majority of the excitatory visceral input from the colon into the VPL nucleus of the thalamus.

In addition to pelvic visceral and cutaneous information, the DCN also receive descending input from a variety of brain stem centers involved in sensory processing (Jundi et al. 1982; see also Willis and Coggeshall 1991). Earlier studies have described changes in transmission through the DCN as a result of polysensory stimulation (Atweh et al. 1974; Jundi et al. 1982; Saadé et al. 1985). Convergence of multiple sensory inputs onto neurons in the dorsolateral medulla, including the DCN, was also recently described (Blair and Thompson 1995). Moreover, the DCN have access to information on muscular and proprioceptive activities, in addition possibly to motor and autonomic functions (Doyle and Maxwell 1993; Masson et al. 1991; Schrimsher and Reier 1993; Wall 1970). Interaction between these inputs at the level of the DCN (see Saadé and Jabbur 1984) would presumably filter out irrelevant information ascending in the spinal cord or descending from higher brain centers and relay a meaningful message to the VPL nucleus or other brain stem sites where it can be amplified or modulated by inputs from other spinal tracts projecting to the thalamus, such as the spinothalamic tract. Although the functional significance of the various control pathways to the DCN is conjectural, the interaction between them at the level of DCN cells and their effect on the ultimate output of the DCN is evident. Therefore it is tempting to suggest that the DCN play an interactive role in the integration of various sensory inputs, including those of visceral origin. Confirmation of this suggested function awaits further studies.

	ACKNOWLEDGEMENTS

  We thank G. Gonzales for assistance with the artwork.

  This work was supported by National Institute of Neurological Disorders and Stroke Grants NS-09743, NS-11255, and NS-32778.

	FOOTNOTES

  Address reprint requests to W. D. Willis.

  Received 28 January 1997; accepted in final form 13 March 1997.

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