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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
INTRODUCTION
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 T 10 (Al-Chaer et al. 1996b). The T 10 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
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 mgrkg 01rh 01 ). Body temperature was monitored
and kept around 377C 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
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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 Å
5) and chemical (n Å 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.
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E. D. AL-CHAER, K. N. WESTLUND, AND W. D. WILLIS
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
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 ú40 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).
Recordings
Recordings from individual neurons of the VPL nucleus were
performed with the use of tungsten microelectrodes ( 125 mm,
shank; 12 MV ) . 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
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Histology
At the end of each experiment the recording site in the VPL
nucleus was marked by passing a continuous current (250 mA
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 mm. The sections were stained with cresyl violet. The VPL
recording sites were identified and the extent of each NG lesion
was reconstructed.
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 õ 0.05 was obtained.
RESULTS
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
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FIG . 1. Photomicrograph of section through rat brain stem. Arrow: site
of electrolytic lesion in nucleus gracilis (NG).
Electrolytic (n Å 5) or chemical (n Å 4) lesions of the NG
were made. For an electrolytic lesion (n Å 5), an extra fine microelectrode (125-mm 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 mm
beneath the surface. The lesion was made by passing a continuous
current (250 mA 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.
NUCLEUS GRACILIS: A VISCERAL SOMATIC INTEGRATOR?
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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.
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.
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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
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E. D. AL-CHAER, K. N. WESTLUND, AND W. D. WILLIS
Figure 3 shows photomicrographs of the injection site
in one experiment at low- ( 12, Fig. 3A) and high-power
magnification ( 140, 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.
Cumulative effect of both electrolytic and chemical lesions
DISCUSSION
FIG . 3. Photomicrograph of section through rat brain stem. Arrow: site
of injection of kainic acid.
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.
Figure 1 shows photomicrographs of the site of the smallest electrolytic NG lesion that had an effect on VPL neuronal
responses, in low- ( 12, Fig. 1A) and high-power magnification ( 120, 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.
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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
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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.
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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.
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 T 10 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
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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 DCDCN 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
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E. D. AL-CHAER, K. N. WESTLUND, AND W. D. WILLIS
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
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.
Address reprint requests to W. D. Willis.
Received 28 January 1997; accepted in final form 13 March 1997.
REFERENCES
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.
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AIDAR, O., GEOHEGAN, W. A., AND UNGEWITTER, L. H. Splanchnic afferent
pathways in the central nervous system. J. Neurophysiol. 15: 131–138,
1952.
AL-CHAER, E. D., LAWAND, N. B., WESTLUND, K. N., AND WILLIS, W. D.
Visceral nociceptive input into the ventral posterolateral nucleus of the
thalamus: a new function for the dorsal column pathway. J. Neurophysiol.
76: 2661–2674, 1996a.
AL-CHAER, E. D., LAWAND, N. B., WESTLUND, K. N., AND WILLIS, W. D.
Pelvic visceral input into the nucleus gracilis is largely mediated by the
postsynaptic dorsal column pathway. J. Neurophysiol. 76: 2675–2690,
1996b.
APK ARIAN, A. V., BRÜGGEMANN, J., SHI, T., AND AIRAPETIAN, L. R. A
thalamic model for true and referred visceral pain. In: Visceral Pain,
edited by G. F. Gebhart. Seattle, WA: IASP, 1995, chapt. 10, p. 217–
259.
ATWEH, S. F., BANNA, N. R., JABBUR, S. J., AND TO’MEY, G. F. Polysensory
interactions in the cuneate nucleus. J. Physiol. Lond. 238: 343–355,
1974.
BERKLEY, K. J. AND HUBSCHER, C. H. Are there separate central nervous
system pathways for touch and pain? Nature Med. 1: 766–773, 1995.
BLAIR, R. W. AND THOMPSON, G. M. Convergence of multiple sensory inputs onto neurons in the dorsolateral medulla in cats. Neuroscience 67:
721–729, 1995.
BURSTEIN, R., DADO, R. J., AND GIESLER, G.J.J. The cells of origin of the
spinothalamic tract of the rat: a quantitative reexamination. Brain Res.
511: 329–337, 1990.
CHANDLER, M. J., ZHANG, J., AND FOREMAN, R. D. Cardiopulmonary sympathetic afferent input excites cuneate-thalamic neurons in monkeys. Soc.
Neurosci. Abstr. 22: 863, 1996.
CLIFFER, K. D. AND GIESLER, G.J.J. Postsynaptic dorsal column pathway
of the rat. III. Distribution of ascending afferent fibers. J. Neurosci. 9:
3146–3168, 1989.
08-05-97 13:44:37
neupa
LP-Neurophys
Downloaded from http://jn.physiology.org/ by 10.220.33.3 on April 28, 2017
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 Å 5), and after a chemical lesion
of NG (n Å 4). Asterisks: P ° 0.05.
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.
NUCLEUS GRACILIS: A VISCERAL SOMATIC INTEGRATOR?
/ 9k16$$jy01
J076-7RC
NESS, T. J. AND GEBHART, G. F. Colorectal distension as a noxious visceral
stimulus: physiologic and pharmacologic characterization of pseudaffective reflexes in the rat. Brain Res. 450: 153–169, 1988.
NESS, T. J., METCALF, A. M., AND GEBHART, G. F. A psychophysiological
study in humans using phasic colonic distension as a noxious visceral
stimulus. Pain 43: 377–386, 1990.
RIGAMONTI, D. D. AND HANCOCK, M. B. Analysis of field potentials elicited
in the dorsal column nuclei by splanchnic nerve A-beta afferents. Brain
Res. 77: 326–329, 1974.
RIGAMONTI, D. D. AND HANCOCK, M. B. Viscerosomatic convergence in
the dorsal column nuclei. Exp. Neurol. 61: 337–348, 1978.
RUSTIONI, A. Non-primary afferents to the nucleus gracilis from the lumbar
cord of the cat. Brain Res. 51: 81–95, 1973.
SAADÉ, N. E., DAJANI, B. M., ATWEH, S. F., AND JABBUR, S. J. Inhibition of
dorsal column nuclei by stimulation of trigeminal afferents in decerebrate
decerebellate cats. Brain Res. 348: 405–407, 1985.
SAADÉ, N. E. AND JABBUR, S. J. Interactions of ventral tract and dorsal
column inputs into the cat cuneate nucleus. Brain Res. 299: 178–181,
1984.
SCHRIMSHER, G. W. AND REIER, P. J. Forelimb motor performance following
dorsal column, dorsolateral funiculi, or ventrolateral funiculi lesions of
the cervical spinal cord in the rat. Exp. Neurol. 120: 264–276, 1993.
WALL, P. D. The sensory and motor role of impulses travelling in the dorsal
columns towards cerebral cortex. Brain 93: 505–524, 1970.
WESTLUND, K. N., AL-CHAER, E. D., AND WILLIS, W. D. The nucleus gracilis (NG): a cross-road for pelvic visceral and cutaneous inputs into the
thalamus. Soc. Neurosci. Abstr. 22: 108, 1996.
WILLIS, W. D. AND COGGESHALL, R. E. Sensory Mechanisms of the Spinal
Cord (2nd ed.). New York: Plenum, 1991.
08-05-97 13:44:37
neupa
LP-Neurophys
Downloaded from http://jn.physiology.org/ by 10.220.33.3 on April 28, 2017
CLIFFER, K. D., HASEGAWA, T., AND WILLIS, W. D. Responses of neurons
in the gracile nucleus of cats to innocuous and noxious stimuli: basic
characterization and antidromic activation from the thalamus. J. Neurophysiol. 68: 818–832, 1992.
COYLE, J. T., MOLLIVER, M. E., AND KUHAR, M. J. In situ injection of kainic
acid: a new method for selectively lesioning neuronal cell bodies while
sparing axons of passage. J. Comp. Neurol. 180: 301–324, 1978.
DOSTROVSKY, J. O. AND MILLAR, J. Receptive fields of gracile neurons after
transection of the dorsal columns. Exp. Neurol. 56: 610–621, 1977.
DOYLE, C. A. AND MAXWELL, D. J. Direct catecholaminergic innervation
of spinal dorsal horn neurons with axons ascending the dorsal columns
in cat. J. Comp. Neurol. 331: 434–444, 1993.
GEBHART, G. F. AND SENGUPTA, J. N. Evaluation of visceral pain. In: Handbook of Methods in Gastrointestinal Pharmacology, edited by T. S. Gaginella. New York: CRC, 1996, chapt. 15, p. 359–373.
HIRSHBERG, R. M., AL-CHAER, E. D., LAWAND, N. B., WESTLUND, K. N.,
AND WILLIS, W. D. Is there a pathway in the posterior funiculus that
signals visceral pain? Pain 67: 291–305, 1996.
JUNDI, A. S., SAADÉ, N. E., BANNA, N. R., AND JABBUR, S. J. Modification
of transmission in the cuneate nucleus by raphe and periaqueductal gray
stimulation. Brain Res. 250: 349–352, 1982.
KEMPLAY, S. AND WEBSTER, K. E. A quantitative study of the projections
of the gracile, cuneate and trigeminal nuclei and of the medullary reticular
formation to the thalamus in the rat. Neuroscience 32: 153–167, 1989.
KUO, D. C. AND DE GROAT, W. C. Primary afferent projections of the major
splanchnic nerve to the spinal cord and the nucleus gracilis of the cat.
J. Comp. Neurol. 231: 421–434, 1985.
MASSON, R.L.J., SPARKES, M. L., AND RITZ, L. A. Descending projections
to the rat sacrocaudal spinal cord. J. Comp. Neurol. 307: 120–130, 1991.
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