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J Neurophysiol 92: 3596-3600, 2004. First published July 28, 2004; doi:10.1152/jn.00310.2004
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REPORT

Effects of Chronic Dorsal Column Lesions on Pelvic Viscerosomatic Convergent Medullary Reticular Formation Neurons

Charles H. Hubscher1 and Richard D. Johnson2,3

1Department of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, Kentucky 40292; 2Department of Physiological Sciences, College of Veterinary Medicine and the 3Evelyn F. and William L. McKnight Brain Institute of the University of Florida, University of Florida, Gainesville, Florida 32610-0144

Submitted 26 May 2004; accepted in final form 23 July 2004


ABSTRACT
 
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Single medullary reticular formation (MRF) neurons receive multiple somatovisceral convergent inputs originating from many different spinal and cranial nerves, including the pelvic nerve (PN), dorsal nerve of the penis (DNP), and the abdominal branches of the vagus. In a previous study, the input to MRF from the male genitalia was shown to be eliminated with chronic 30-day dorsal hemisection at the T8 spinal level. In this study, the effect of a smaller chronic lesion [dorsal column lesion (DCx)] on MRF neuronal responses was examined. Responses to bilateral electrical stimulation of the DNP remained. MRF neuronal responses to non-noxious (touch/stroke) levels of penile stimulation, however, were eliminated; only responses to noxious pinch remained. No differences were found for the number of neurons responding to noxious distention of the colon between the DCx and control groups. Although no differences were found across these groups for the percent MRF responses to vagal stimulation, the mean response latency for the DCx group was twice the sham-DCx/intact control group. Taken together, these results indicate that the MRF receives at least some of its input from the male genitalia via pathways located within the dorsal columns at the mid-thoracic spinal level.


INTRODUCTION
 
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 ABSTRACT
 INTRODUCTION
METHODS
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 ACKNOWLEDGMENTS
 REFERENCES
 
The release of semen, urine, and feces is a complex process involving spinal reflexes that are under both conscious and unconscious control. Many brain regions along the entire neural axis are likely involved in the circuitry mediating ejaculation, micturition, and defecation. The focus of our studies is on the medullary reticular formation (MRF; includes the nucleus reticularis gigantocellularis and surrounding nuclei), which is part of a spino-bulbo-spinal loop mediating ejaculation (Marson and McKenna 1990Go; Yells et al. 1992Go). MRF neurons receive convergent inputs from multiple cutaneous, mucocutaneous, and visceral territories, which include regions innervated by spinal and cranial nerves (Hubscher and Johnson 1996Go; Hubscher et al. 2004Go). Using both acute (1 h) and chronic (30 day) lesions, the location of spino-bulbo-spinal pathways to/from the male urogenital tract and the type(s) of information being conveyed was previously shown, using electrophysiological techniques, to be located in the dorsal half of the cord at the T8 spinal level (Hubscher and Johnson 1999bGo, 2000Go). Acute lesions restricted to the dorsal columns revealed that low threshold penile input to MRF is conveyed in the dorsal columns. To address a number of issues surrounding the use of acute lesions, including spinal shock and the potential for reorganization of the neural circuitry, the location of the ascending projections within the mid-thoracic white matter was examined, in this study, with chronic lesions restricted to just the dorsal columns (DCx; recording of MRF neurons 30 days after injury).


METHODS
 
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Surgeries were performed on nine male Wistar rats (90 days of age) under aseptic conditions as previously described (Hubscher and Johnson 1999bGo). Each animal was anesthetized with a mixture of ketamine (80 mg/kg) and xylazine (10 mg/kg, ip). A long-acting antibiotic (Ambi-Pen: 0.5 ml sc; Butler, Columbus, OH) was administered before surgery. The spinal cord was exposed at the T8 level via removal of the overlying T7 vertebral lamina. DCx's were made through a longitudinal dural incision using a 21-gauge needle (7 animals). All surgical procedures (except the lesion) were done on two sham surgical controls. All animals recovered as previously described (Hubscher and Johnson 1999bGo). An analgesic (Ketoprofen; 2.5 mg/kg sc; Fort Dodge) was administered twice daily for the first 48 h and then as needed to alleviate postoperative discomfort.

Electrophysiological recordings were made 30 days after injury using previously described protocols (Hubscher and Johnson 1996Go, 1999bGo). Each animal was anesthetized with urethane (1.2 g/kg, ip) and intravenous supplements of 5% urethane were given as needed. The common carotid artery, jugular vein, and trachea were intubated for the purposes of blood pressure monitoring, intravenous infusion route, and end expired pCO2 monitoring. Body temperature was maintained at 37°C and mean blood pressure 75 mmHg or above throughout the experiment. The head was clamped in a stereotaxic holder, and the brain stem exposed as previously described (Hubscher and Johnson 1996Go, 1999bGo). The pelvic nerve (PN) and dorsal nerve of the penis (DNP) were exposed bilaterally and specially fabricated bipolar silicon-cuff microelectrodes were implanted around each of the exposed nerves (Hubscher and Johnson 1996Go). The stimulus consisted of trains of 14 pulses at 70 pps (100-ms train duration, 1 train/s), with a pulse strength set at approximately five times pudendal reflex threshold (i.e.,30–50 µA, 0.1-ms duration). This stimulus intensity level is supramaximal for the myelinated PN/DNP nerve fibers in the A{beta} and A{delta} range (Johnson and Murray 1992Go). For the abdominal branch of the vagus nerve, a bipolar ring electrode was threaded down the esophagus and positioned in the abdominal cavity just caudal to the esophageal hiatus (Hubscher et al. 2004Go; Khasar et al. 1998Go). Stainless steel microelectrodes (FHC; impedance, 6–8 MOhms) attached to a hydraulic probe were used as previously described (Hubscher and Berkley 1994Go; Hubscher and Johnson 1996Go). The MRF region containing the highest percentage of DNP/PN responsive neurons (Hubscher and Johnson 1999aGo) was searched for neurons responsive bilateral stimulation of the PN. Single identified neurons (somato-dendritic) were recorded extracellularly and the spikes stored on videotape and replayed off-line using a computer based software package.

Latency of the response, bilaterality of the response, and the degree of excitation or inhibition was determined. As previously described (Hubscher and Johnson 1996Go, 2002Go), a neuronal response was counted if the number of spikes firing was at least two times (excitation) or one-half (inhibition) of background firing levels that occur immediately prior to stimulus onset. The doubling/halving criteria was chosen because the increase/decrease was clearly audible through the audiomonitor and is clearly distinguishable as a response in comparison to the random and slight increases/decreases in firing frequencies that were not associated with a stimulus. In units that did not have a spontaneous discharge, a minimum of three spikes was required for it to count as an excitatory response. Convergent cutaneous receptive fields were tested over the entire body, using hand-held probes. Colonic distention was made using a 10-mm-long latex balloon (Berkley et al. 1993Go; Hubscher et al. 2004Go). At the end of the experiment, the animal was killed with an anesthetic overdose and perfused transcardially with 0.9% saline followed by 10% formalin. The block of brain stem tissue containing the recording sites was removed and stored overnight in a 10% formalin/30% sucrose solution. Recording sites were visualized in 50-µm vibratome sections stained with cresyl violet and reconstructed under light and dark field illumination (Paxinos and Watson 1998Go). All animal procedures were reviewed and approved by the Institutional Animal Use and Care Committee at the University of Louisville and the University of Florida.


RESULTS
 
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DISCUSSION
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 REFERENCES
 
In the MRF, a total of 109 neurons responsive to bPN were found in nine animals along 30 electrode tracks. All of these neurons also responded to bDNP stimulation. A summary of the response properties of these neurons is presented in Table 1. Since there were no significant differences (t-test; P > 0.05) found between neurons in the sham-DCx and intact control (Hubscher et al. 2004Go) groups, the data were combined (Table 1). Note that 47% of the PN/DNP-responsive MRF neurons in the DCx group and 59% of the neurons in the controls had no background activity. No significant differences (t-test, P > 0.05) in response latencies were found between DCx and sham-DCx or with intact controls (Hubscher et al. 2004Go). In addition, no significant differences were found in response latency between neurons with excitatory and inhibitory responses (so data were combined). The mean response latency to bPN and bDNP stimulation was 149.4 ± 11.0 and 132.1 ± 11.0 (SE) ms, respectively.


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  		TABLE 1. Summary of MRF recordings

 
A summary showing the location of the PN-responsive neurons for three animals with DCx lesions at one anterior-posterior level within the restricted search area is shown in Fig. 1A. The results from intact control animals (Hubscher et al. 2004Go) are also shown (for comparison). As shown in Fig. 1, these neurons were located throughout the MRF search area (in Gi, GiA, DPGi, LPGi; Paxinos and Watson 1998)Go.



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  		FIG. 1. Example showing the location of pelvic nerve (PN)-responsive medullary reticular formation (MRF) neurons in 6 animals [3 intact male rats, 8 electrode tracks total; 3 rats with a chronic dorsal column lesion (DCx), 8 electrode tracks in total]. All of these neurons also responded to bilateral electrical stimulation of the dorsal nerve of the penis (DNP). Location of responses to low (stroke) and high (pinch) threshold levels of mechanical stimulation of the penis are shown in A. Responses to stroking the penis were only found in intact controls and sham-DCx (data not shown) animals. Some of the neurons shown in A also responded to colon distention (B). Note that although more PN-responsive neurons are shown post-DCx, there were no significant differences overall between the groups in the number of PN-responsive neurons per electrode track. Cross-section is adapted from Fig. 65 of Paxinos and Watson (1998)Go. Intact data have been published elsewhere (Hubscher et al. 2004Go). 4V, 4th ventricle; 7, facial nucleus; DPGi, dorsal paragigantocellular nucleus; Gi, gigantocellular reticular nucleus; GiA, Gi pars alpha; IRt, intermediate reticular nucleus; LPGi, lateral paragigantocellular nucleus; py, pyramidal tract; RMg, raphe magnus nucleus.

 
For the DCx group of animals, 100% of the neurons responded to noxious levels of penile stimulation (pinch) compared with 0% responding to non-noxious levels (i.e., touch/stroke). Examples showing typical excitatory responses of single MRF neurons to PN/DNP stimulation following a chronic DCx lesion is provided in Fig. 2. As shown in Table 1, only MRF neurons in the control groups responded to touch/stroke of the penis.



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  		FIG. 2. Typical responses of 2 pelvic nerve (PN) responsive single neurons (same animal) located in the right n. reticularis gigantocellularis (unit 1) and dorsal paragigantocellular nucleus (unit 2; PN response not shown). Both neurons responded to dorsal nerve of the penis (bDNP) as well as distention of the colon (shown for unit 1 only) and mechanical stimulation of the penis (stroke, pinch). Note that the response shown for colon distention had an afterdischarge (duration of >30 s; complete record not shown). Both units responded to pinching of the entire body (not all responses shown). The lesion epicenter reconstruction is shown. Horizontal bar symbols on the raw records indicate onset and duration of a natural stimulus. Arrows (and often the stimulus artifacts) indicate onset of an electrical stimulus train to the respective nerve. l., left; r., right.

 
A small subpopulation of the neurons, not previously described in the intact control group (Hubscher et al. 2004Go), had "complex" response patterns; i.e., MRF neurons with excitatory or inhibitory responses to PN/DNP stimulation occasionally had opposite responses (inhibitory or excitatory, respectively) from stimulation of one of the convergent territories, particularly the face. These neuronal response patterns, found on occasion in both controls and DCx lesioned animals, were located in all MRF subdivisions within the search territory (see outlined areas in Fig. 1). Two examples obtained from recordings in the MRF of an intact control animal are provided in Fig. 3 (see also data in Table 1).



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  		FIG. 3. Examples showing "complex" response patterns in an intact control animal. Responses of the single neuron in A, located in the left GiA, were inhibitory for bilateral stimulation of the PN and DNP but excitatory for pinching the face. This neuron also had inhibitory responses to pinching of the rest of the body (including the ear; responses not shown), but did not respond to vagal stimulation or colon distention. Responses of the single neuron in B, located in the left Gi, were excitatory for stimulation of the PN, as well as the DNP and entire body (data not shown), except the face. Pinching the face inhibited all of the excitatory responses (effect on response to PN shown). This neuron also did not respond to stimulation of either the vagus or colon. Symbols as indicated in Fig. 2 legend. Each of the 4 raw records represents a 7-s time frame.

 
A summary showing the location of neurons responding to colon distention in three DCx animals is also presented in Fig. 1B. No significant differences (P > 0.05) were found between groups for convergent input from the distal colon. Although no significant differences (P > 0.05; see Table 1) were found across groups for responses to vagal stimulation (P > 0.05), the mean vagal response latency for the DCx group (305.1 ± 33.4 ms) was significantly different (t-test; P < 0.01) from the sham-DCx group (166.9 ± 31.4 ms) and intact controls (166.8 ± 21.3 ms).


DISCUSSION
 
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
One result of this study is the finding that the dorsal columns convey low-threshold input from the glans penis to the MRF. The MRF has been shown in the rat to be interconnected with the dorsal column nuclei (Odutola 1977Go; Tomasulo and Emmers 1972Go). Previous studies using female rats have shown that the nucleus gracilis receives pelvic-visceral inputs from the reproductive organs (Berkley and Hubscher 1995Go; Hubscher 1994Go). Given that responses to bDNP and noxious mechanical stimulation of the penis are lost following both acute and chronic dorsal hemisection of the cord at the T8 spinal level (Hubscher and Johnson 1999bGo) but not following a DCx lesion, the dorsal portion of the lateral funiculus is most likely the location of these ascending projections to MRF. These findings are consistent with Li et al. (1998)Go, who showed the loss of responses of GiA neurons to noxious heat applied to cutaneous regions following transection of the contralateral dorsolateral funiculus.

A second finding is that pathways other than the dorsal columns convey noxious input from the distal colon to MRF. Possibilities include the spinoreticular pathway (Chaouch et al. 1983Go; Menetrey et al. 1980Go), in addition to collaterals from the spinomesencephalic pathway (McMahon and Wall 1983Go; Zemlan et al. 1978Go) and the spinohypothalamic pathway (Kostarczyk et al. 1997Go). Others, however, have shown that responses to colorectal distention in one subset of thalamic neurons [ventroposterolateral nucleus (VPL)] are reduced, but not eliminated, following an acute lesion of either the dorsal column (Al-Chaer et al. 1996Go) or nucleus gracilis (Al-Chaer et al. 1997Go). In addition, ascending projections from neurons in the area around the spinal central canal has been implicated in the transmission of second-order afferent information for visceral nociception to the nucleus gracilis (Wang et al. 1999Go). A lack of reduced responses to colon distension in this experiment may be explained by the different area of the brain stem being examined or by the fact that chronic and not acute lesions were used for this study (i.e., some reorganization of the circuitry with time postinjury may have occurred). A further possibility is that the responses of VPL neurons in the thalamus to colorectal distention may be due to stimulation of the rectum and not the descending colon (as tested in this study). In recent recordings in the thalamus of male rats (Hubscher and Johnson 2003Go), neurons responsive to distention of just the descending colon were found in multiple thalamic subregions (medial-dorsal central, ventrolateral, lateral-dorsal/posterior, submedius), but not within the VPL (although bDNP and not bPN was used as the search stimulus).

The MRF has also been shown in the rat to be interconnected with the solitary nucleus in the caudal brain stem (Jean 1991Go; Mtui et al. 1995Go). In female rats, the solitary nucleus has been shown to relay input (potentially noxious) from pelvic-visceral sources centrally (cervix, vagina, and uterus) via both a spino-solitary and vagal-solitary pathway (Hubscher and Berkley 1994Go 1995). Furthermore, anatomical tracing experiments show vagal innervation of all colon regions above the rectum (Altschuler et al. 1989Go, 1993Go) as well as the entire uterus and cervix in the female rat (Collins et al. 1999Go; Ortega-Villalobos et al. 1990Go). The responses to colon distention could therefore be due to the intact projection via the abdominal branch of the vagus.

A third finding in this study is the change in response latency of MRF neurons to electrical stimulation of the abdominal branches of the vagus following DCx. The effect of DCx on the vagal input to MRF may reflect the possibility of reorganization of the inputs from the colon. Vagal afferents do not normally respond in the noxious range (Ozaki et al. 1999Go). Perhaps the C-fibers in the vagus became mechanosensitive to colon distention in the noxious range, which might account for the doubling of the response latency.


GRANTS
 
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 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
ACKNOWLEDGMENTS
 REFERENCES
 
This study was supported by National Institute of Neurological Disorders and Stroke Grant NS-40919.


ACKNOWLEDGMENTS
 
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 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
REFERENCES
 
We thank J. Armstrong, D. Brooks, E. Kaddumi, V. Dugan, and A. Kuntz for excellent technical assistance.


FOOTNOTES
 
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Address for reprint requests and other correspondence: C. H. Hubscher, Dept. of Anatomical Sciences and Neurobiology, Univ. of Louisville, Louisville, KY 40292 (E-mail: chhubs01{at}louisville.edu).


REFERENCES
 
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 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
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