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J Neurophysiol (January 1, 2003). 10.1152/jn.00294.2002
Submitted on Submitted 19 April 2002; accepted in final form 27 August 2002
1Department of Anatomical Sciences and Neurobiology University of Louisville, Louisville, Kentucky 40292; and 2Department of Physiological Sciences, University of Florida Brain Institute, University of Florida, Gainesville, Florida 32610-0144
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Hubscher, Charles H. and Richard D. Johnson. Responses of Thalamic Neurons to Input From the Male Genitalia. J. Neurophysiol. 89: 2-11, 2003. There have been relatively few electrophysiological studies, in any species, describing the supraspinal processing of inputs from the male genital tract. The thalamus was the focus of the present study. In 11 urethan-anesthetized male rats, subregions of the thalamus were surveyed for neuronal responses to the search stimulus, bilateral electrical stimulation of the dorsal nerve of the penis (DNP). A total of 133 DNP-responsive neurons were found and further tested for degree of somatovisceral convergence from other peripheral structures. Histological reconstruction of the recording sites revealed that the penile-responsive neurons were distributed among various thalamic subregions. These thalamic subregions included the medial-dorsal nuclei and ventral and lateral thalamic subregions (majority of neurons responsive to both tactile and pinch stimulation of the penis) as well as intralaminar, posterior and reticular subregions (majority responsive to pinch only). Taken together, the data demonstrate the existence of thalamic neurons with inputs from the male genitalia with widespread somatovisceral convergence. These neurons likely contribute to the neural circuitries underlying various aspects of penile sensation associated with reproductive and nociceptive events.
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Our knowledge of the central
processing of inputs from the male genitalia is quite limited.
Peripherally, the electrophysiology and morphology of primary afferent
receptors innervating the genitalia has been characterized for both
male (Johnson 1988
; Johnson and Halata
1991; Johnson and Murray 1992) and female
(Berkley and Hubscher 1995b) rats. These and other
studies have shown that the receptors and physiological response
patterns (and human percepts) of this sensory system are unlike those
found in typical skin or viscera. The external genitalia are classified
as mucocutaneous tissue, possessing morphological characteristics of
skin and viscera. In males, the glans penis contains an unusually high
number of free nerve endings innervated by A-delta fibers
(Halata and Munger 1986; Johnson and Halata
1991), particularly around the external urethral orifice. In
the rat, primary dorsal nerve of the penis (DNP) afferents have their
cell bodies in L6/S1 dorsal
root ganglia and many of their central processes terminate bilaterally
(McKenna and Nadelhaft 1986; Nunez et al.
1986) on interneurons (Johnson 1989).
The spinal pathways and higher CNS regions involved in processing DNP
input have been the focus of our recent electrophysiological investigations. Medullary reticular formation (MRF) neurons, involved in regulating coordinated perineal muscle contractions that mediate sexual reflexes (de Groat and Booth 1993; Marson
and McKenna 1990), respond to low- and high-threshold levels of
penile stimulation (Hubscher and Johnson 1996) via
spinal projections within the dorsal columns and dorsal lateral
funiculus, respectively, at the T8 spinal level (Hubscher and
Johnson 1999b). The MRF is known to process (Bowsher
1976; Gebhart 1982; Hubscher and Johnson
1996, 1999a; Peschanski and Besson 1984) and
transmit nociceptive inputs rostrally to many thalamic subregions of
the rat (Jones and Yang 1985; Peschanski and
Besson 1984), particularly in "nonspecific" nuclei.
Therefore the objective of the present study was to survey portions of
thalamus for low- and high-threshold penile inputs.
Compared with somatosensory pathways from limbs, studies of pathways
from pelvic and visceral regions to thalamus have been limited. No
electrophysiological studies to date, in any species, describe thalamic
input from the male genital tract. In the present study, we
hypothesized that DNP input would be found in regions of the thalamus
where other pelvic and visceral inputs have already been demonstrated.
For example, in females, individual neurons in and around the
ventrobasal complex (VB) of the thalamus have been shown to respond to
stimulation (noxious and nonnoxious range) of one or more portions of
the reproductive tract (uterus, cervix, and vagina) in addition to
small cutaneous regions (Berkley et al. 1993a). In
contrast, neurons in the intralaminar thalamic complex have been shown
to be driven by widespread cutaneous pinch and noxious reproductive
organ stimuli (Berkley et al. 1995). Possible sources of
reproductive organ input to thalamus in female rats include the MRF
(Hornby and Rose 1976; Hubscher and Johnson 2001) and/or solitary nucleus (Hubscher and Berkley
1994, 1995) to the intralaminar nuclei, and spinal cord
(Berkley et al. 1993b; Wall et al. 1993)
and/or dorsal column nuclei (Berkley and Hubscher 1995a)
to VB. Other pelvic/visceral inputs that have already been demonstrated
to medial and lateral thalamus in rats and other species include the
bladder, colon, esophagus, intestines, and cardiovascular structures
(Al-Chaer et al. 1996; Berkley et al. 1993a; Bruggemann et al. 1993, 1994a;
Chandler et al. 1992; Chernigovskiy and
Onischenko 1967; Davis and Dostrovsky 1988;
Horie and Yokota 1990; Hubscher and Johnson
1998).
In the present study, electrophysiological recordings of single
thalamic neurons were obtained to determine responsiveness to
electrical and mechanical stimulation of afferents in the dorsal nerve
of the penis. Because many thalamic neurons process convergent ascending somatovisceral sensory inputs, electrical stimulation of the
pelvic nerve (PN), distension of the distal colon, and mechanical
stimulation of the skin over the whole body (stroke/pressure/pinch) were also tested. Preliminary data have been reported in abstract form
(Hubscher and Johnson 1998).
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Eleven male Wistar rats at approximately 90-120 days of age
were used in these experiments. Each rat was anesthetized with urethan
(1.2 g/kg ip) and supplements of 5% urethan were given as needed
(intravenous infusion) to maintain an even level of anesthesia; i.e.,
just at the point that the corneal reflex is lost. 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, respectively (Johnson and
Murray 1992). Body temperature was maintained at 37°C through
an esophageal thermistor and circulating water heating pad and body coils.
The PN, DNP and the motor branch of the pudendal nerve were exposed
bilaterally beginning with a dorsal midline incision as previously
described (Hubscher and Johnson 1996). The head was clamped in a stereotaxic holder, with skull flat. An opening was made
over the cortex on the left side by first drilling a small hole into
the skull and then expanding the opening with bone rongeurs. The
exposure coordinates were 1.5 mm through 4.5 mm caudal to bregma and
4.5 mm from mid-line laterally.
The hindquarters were pivoted with hip pins and the tail tied in an
upward direction to allow the penis, ventral abdomen, and perineum to
be exposed for surface stimulation. Specially fabricated bipolar
silicone-cuff microelectrodes were then placed around both DNPs and
both viscerocutaneous branches of the PN (Fig.
1) (Hubscher and Johnson
1996). Recording electrodes were placed bilaterally around each
motor branch of the pudendal nerve. The pudendal reflex threshold,
assurance of cathodal nerve stimulation, and the segmental synaptic
integrity of DNP and PN afferents on pudendal reflex circuitry were
continually monitored by recording polysynaptic reflex discharges in
left and right pudendal motor axons (Johnson 1995;
Johnson and Hubscher 1998).
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Glass-coated platinum-plated tungsten microelectrodes (Merrill
and Ainsworth 1972) were then advanced stereotaxically into the
left thalamus with a stepping microdrive using previously described
protocols (Berkley et al. 1993b; Hubscher and
Berkley 1994; Hubscher and Johnson 1996). To
maximize the number of neurons recorded per experiment, two
microelectrodes were lowered simultaneously in the same
anterior/posterior plane (see Fig. 1). Two identical sets of recording
equipment (preamplifier, audio monitor, analog delay, oscilloscope, PCM
adapter, VCR channel) allowed for simultaneous recording from both
thalamic microelectrodes. The microelectrodes for most tracks were set
at 2,000 µm apart, i.e., one through the medial thalamus and one
through the lateral thalamus. Due to the size of the thalamus, the
search in the present study was limited to the rostral-to-caudal extent
of the ventroposterolateral nucleus [i.e., 
2.1 to 4.3 mm caudal to
bregma (Paxinos and Watson 1997)]. The depth range for
all tracks began at 4,000 µm below the cortex surface and traversed
to a depth of 7,500 µm; i.e., from just above to just below the
thalamus (Paxinos and Watson 1997). Single identified
neurons were recorded extracellularly, and the spikes were stored on
video tape. Conventional electrophysiological instrumentation was used.
Only single neurons well-isolated from surrounding activity were
counted in the sample. Single neuron isolation was established and
maintained by monitoring the action potential on an oscilloscope with a
spike-triggered analog delay module. Careful records of the stereotaxic
location of each neuron were kept (track location and depth). These
locations were confirmed and/or adjusted with postmortem histological reconstructions.
The peripheral search stimulus consisted of bilateral electrical
stimulation of the DNP (trains of 14 pulses at 70 pps, 100-ms train
duration, 1 train/s). Stimulus pulse strength was set at approximately
five times pudendal reflex threshold (i.e., 30-50 µA, 0.1-ms
duration). These stimuli activate myelinated DNP nerve fibers in the
A
and A
range (Johnson and Murray 1992). Following the isolation of a single neuron, the action potential was continually monitored on an oscilloscope as previously described (Hubscher and Johnson 1996). In addition, when the lateral electrode was positioned in the vicinity of VB, brushing of the skin over the contralateral body was also tested as an indicator of approximate location (as pertaining to previous maps of others) (e.g.,
Emmers 1964). However, during the course of the study
(5th animal of the 11), a neuron was found that responded to
stimulation of a small contralateral field on the face and this
response was altered with DNP stimulation (even though the neuron
itself did not directly respond to DNP stimulation or mechanical
stimulation of the penis). Thus for the remaining animals in the study,
all the neurons responsive to the contralateral brush stimulus were
further tested for convergent effects (cutaneous and pelvic/visceral).
All neurons excited or inhibited by electrical stimulation of the DNP were tested further. To determine the responsiveness to DNP and PN afferent inputs, an electrical stimulation array device was employed. In response to solitary stimulation of afferent fibers in each of the four cuffed nerves, the degree of facilitation or inhibition of the thalamic neuron was determined including the latency of the response. In addition, the bilaterality of response was determined using single and tandem afferent stimuli. If the thalamic neuron exhibited spontaneous activity, the receptive field (see following text) was scrutinized for evidence of both inhibitory and excitatory zones. A response to stimulation of a peripheral structure/nerve was noted if the number of spikes fired approximately two times (excitation) or one half (inhibition) of background levels based on digital oscilloscope records. Repetitive stimuli were often required to activate a neuron from a given nerve or receptive field ("wind-up"). If present, spontaneous firing rates were measured from oscilloscope records (mean firing rate over 3 1-min periods) prior to the sequence of testing. The spontaneous firing pattern was classified as regular (tonic discharge with consistent interspike interval) or intermittent (short phasic bursts separated by short quiescent periods).
Hand-held probes were used to map out the characteristics of receptive
fields on the penis and surrounding preputial, scrotal, anal, and
perineal skin areas in addition to visceral (urethral and colorectal)
regions. Stimuli were also presented on each side of the entire body to
determine if there were convergent inputs from areas outside the
pudendal and pelvic nerve territories. The stimuli and the hand held
probes were as follows: brush, camel's hair brush; firm touch and
pinch [gentle, moderate and strong: (Hubscher and Johnson
1999a)], small forceps; stretch, small forceps or fine glass
rod; pressure, serrated forceps; visceral, glass probe to
urethra/colorectal mucosa. In addition, a 1-cm-long latex balloon was
used for distension of the descending colon (Berkley et al.
1993b). Gentle stimuli, generating a low-threshold (LT) neuronal response, included brushing, firm touch, stretching, probing
(visceral), and pressure. Intense stimuli, generating high-threshold
(HT) neuronal responses, included pinching and distention (visceral).
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 in a 10% formalin/30% sucrose solution.
Microelectrode tracks were visualized in 50-µm vibratome sections
stained with cresyl violet. The microelectrode tracks and recording
sites were reconstructed under light and dark field illumination
(Paxinos and Watson 1997) as previously described
(Berkley et al. 1993b; Johnson and Hubscher
1998).
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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A total of 48 electrode tracks in 11 rats encompassed the search region within the thalamus (see shaded areas in Fig. 2). In all but five of these tracks, neurons were found that responded to the search stimulus, bilateral electrical stimulation of the DNP (n = 133). A histological reconstruction of the location of these DNP-responsive neurons is presented in Fig. 2. Thalamic subregions surveyed include the following: intralaminar (centromedial, centrolateral), lateral (dorsal, posterior), medial (dorsal: central, lateral, and medial), ventral (anterior, medial, lateral, posteromedial, posterolateral), posterior, submedius, and reticular nuclei.
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Properties of DNP-responsive neurons
Most of the 133 neurons responding to bilateral electrical DNP stimulation were excitatory (n = 122; 92%). Half of the thalamic neurons with excitatory responses to DNP stimulation (61 of 122) had no resting discharges. The remaining 72 thalamic neurons (61 excitatory, 11 inhibitory) had resting discharges with patterns that were either regular (19%) or intermittent (81%). The 14 neurons with a regular resting discharge had a firing rate of 24 ± 5 (SE) spikes/s. Eleven of these neurons were inhibited by stimulation of the DNP (and its convergent receptive field territories), and the majority were located in the reticular thalamic region. Those neurons (n = 58) with an intermittent resting discharge had a bursting pattern that was either high frequency (15; 21% of total intermittant) or low frequency (43; 60% of total intermittant). Those with a high-frequency intermittent burst of activity were most often found in the ventral and lateral subthalamic regions. In contrast, neurons with a low-frequency intermittent pattern were found throughout all of the thalamic subregions surveyed. These neurons had a mean firing rate of 4 ± 0.4 spikes/s.
Response characteristics to stimulation of the DNP/penis
All of the DNP-responsive neurons tested responded to both ipsilateral and contralateral DNP stimulation and the bilateral responses were often additive. Neuronal response latencies to DNP stimulation varied from 112 to 572 ms, with a mean ± SE latency of 336 ± 13 ms. The neuronal responses to noxious mechanical stimulation of the penis were rarely time-locked to the stimulus. On occasion, afterdischarges, usually upward of several seconds, lasted up to several minutes.
Of the 133 DNP-responsive neurons, all had receptive fields on the
penis. Of these, 84 were low threshold; i.e., the neuron responded to
gentle stroking of the glans (see example in Figs. 3 and 4),
although it is important to note that the stimulation was applied under
conditions of penile detumescence rather than tumescence, the latter
condition having been shown to increase DNP afferent firing frequency
(Johnson 1988). The location of the neurons to LT penile
stimulation were found in the medial-dorsal, ventral, and lateral
thalamic nuclei. Of the 84 neurons, 23 required wind-up (5 trains on
average, given at a rate of one train per second
see
METHODS) with bDNP stimulation to respond and 13 of these
neurons were located in the lateral-dorsal subnuclei (see Fig. 2,
).
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The remaining 49 of the 133 DNP-responsive neurons responded to
pinching of the penis, mostly to the external urethral orifice ("cup") and/or glans region. Of the 39 neurons located in the intralaminar, posterior and reticular nuclei, 33 (85%) were of this
type. Interestingly, the few neurons isolated in the reticular nucleus
were inhibited by stimulation of the penis and the DNP as was found in
the intermediate reticular nucleus of the MRF (Hubscher and
Johnson 1996). A summary and comparison of response characteristics by location is provided in Fig.
5.
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Convergent somatovisceral inputs on DNP-responsive thalamic neurons
One hundred and twenty-nine of the DNP-responsive neurons (97%) were additionally responsive to bilateral electrical stimulation of PN. All of these neurons responded to both ipsi- and contralateral PN stimulation, and the majority were excitatory (92%). All of these neurons responded to mechanical stimulation of one or more cutaneous territories innervated by the PN (e.g., dorsal perineum, anus). Just one of the visceral territories innervated by the PN was tested; i.e., distension of the descending colon. Overall, only 10 of the PN-responsive neurons responded to colon stimulation. An example is provided in Fig. 4. These neurons accounted for 18% of the neurons in the four thalamic subnuclei in which they were found: the medial-dorsal central, ventrolateral, lateral-dorsal/posterior, and submedius thalamic nuclei.
The same neurons, and the four not responsive to PN
stimulation, were also responsive to touching and/or
pinching (bilateral) of areas outside the DNP/PN-innervated territories
(see examples in Figs. 3 and 4). Many of these thalamic neurons had
convergent receptive fields as seen previously in our MRF recordings
(Hubscher and Johnson 1996); e.g., responses to pinching
of the ears and toes (both forepaw and hindpawoften around the
joints). Other neurons had whole body convergent cutaneous fields (35%
of the total DNP-responsive neurons). Whereas the majority of responses from cutaneous territories were to high-threshold levels of stimulation (pinch), a number of neurons were found that responded to low-threshold (stroking/gentle pressure) stimulation of the dorsal trunk and face
(see Figs. 3-5). Most of these were located in the lateral and
medial-dorsal thalamic subnuclei (see Figs. 2 and 5).
VENTROBASAL COMPLEX NEURONS.
In addition to the 133 DNP-responsive thalamic neurons, 26 neurons were
found to respond to brushing of a small contralateral skin region (Fig.
2, 
). These neurons did not respond to DNP stimulation. For one of
these neurons, a split receptive field was identified (see Fig.
6); this does not conform to the
traditional views of VB response properties. In addition, during the
course of experimentation, the responses of two of the neurons located in the ventroposteromedial (VPM) part of VB (see 
at 3.6 mm level
in Fig. 2) was altered with stimulation of the DNP (counted toward the
133 total DNP-responsive neurons). The responses of one of these
neurons is provided in Fig. 7. Pinching
the toes of either hindfoot also modulated the responses to facial
stimulation (i.e., the convergence on these neurons was not limited to
the pelvic region).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The present study documents for the first time, using electrophysiological techniques, the existence of inputs from the genitalia to thalamus in the male rat. The sampling of various subregions in this initial survey of single neurons within the thalamus demonstrates that electrical stimulation of the DNP activates neurons contained within widespread thalamic regions in anesthetized rats. The results further demonstrate that DNP-responsive thalamic neurons receive convergent inputs from large, bilateral somatic territories as well as from pelvic-visceral territories, which adds to well established data, in a number of species, of widespread somatosensory inputs onto several subregions of the thalamus. Variations in neuronal response properties (excitation vs. inhibition; low vs. high threshold; DNP alone vs. DNP + PN) and location (intralaminar, ventral, posterior, etc.) suggest that these neurons may serve several different functions within the realm of male reproductive mechanisms and sensation.
DNP-RESPONSIVE NEURONS.
Many neurons throughout thalamus responded to stimulation of DNP. The
number of neurons per electrode track may be an underestimate of DNP
input to this region because the search stimulus only activated A
and A DNP afferents. The DNP also contains a large population of C
fibers (Johnson and Halata 1991).
). The
majority of neurons responsive to DNP stimulation had no background
activity, which was also found for DNP-responsive MRF neurons. However, the response latencies for the DNP-responsive thalamic neurons were on
average three times longer than those found in MRF, suggesting that at
least some of these inputs to thalamus from the penis may be conveyed
rostrally via a spino-reticulo-thalamic pathway that has been
implicated in the transmission of nociceptive information (Peschanski and Besson 1984).
Some of the DNP-responsive thalamic neurons, like those studied in the
MRF, required wind-up with bilateral electrical stimulation of the DNP
(on average, 7 trains) to respond. This finding suggests that in a
functional context, the neurons requiring wind-up may be firing near
the threshold required for the ejaculatory response, which depends on a
gradual build-up of activity produced by multiple rapid
intromissions (Sachs and Meisel 1988). Wind-up,
a response and/or increase in response requiring repeated exposure to a
stimulus, was also occasionally a prerequisite for detection of
convergent cutaneous inputs. Multiple brief stimuli to the same
cutaneous territory or prior stimulation of another territory with a
lower response threshold were sometimes necessary to reach the response threshold and then sustain the response. Aside from the DNP stimulus, the convergent territory most often used for "wind-up" was the ears
(i.e., typically have a lower response threshold) (Hubscher and
Johnson 1996).
DNP VS. PN.
Most DNP-responsive neurons responded to bilateral (and unilateral)
stimulation of the PN. This high degree of convergence differs from
what was found previously in the MRF (Hubscher and Johnson
1996), where only one-half of the DNP-responsive neurons responded to stimulation of the PN. This difference can be explained by
the multitude of inputs to thalamus (e.g., Desbois and
Villanueva 2001; Herkenham 1979; Krout
and Loewy 2000; McAllister and Wells 1981;
Shibata 2000), only some of which are from the MRF
(e.g., Kevetter and Willis 1982; Peschanski and
Besson 1984). Likewise, the MRF projects to many different
areas (Jones 1995; Jones and Yang 1985),
only some of which are located in the thalamus. Note that it is
possible that there is a group of neurons that may respond to
unilateral and/or bilateral stimulation of the PN but not the DNP
(search stimulus). This possibility will be addressed in future studies.
). Stimulation of PN-innervated cutaneous
regions produced responses for all thalamic neurons responding to
electrical stimulation of PN. In addition, responses were also expected
from PN-innervated visceral territories. In the present
study, only distention of the distal descending colon was tested.
Responses were found in similar thalamic subregions (see
RESULTS) as reported in three previous studies (see
Berkley et al. 1993b; Kawakita et al.
1997; Yang et al. 1998). In the present study,
however, only 18% of the neurons in these subregions responded. This
value is significantly lower than the numbers found in two of these
three previous studies [79% overall (Yang et al.
1998); 80% overall (Kawakita et al. 1997)].
This difference may be due to the size and location of the stimulus
itself, and/or differences in the search protocols. For example,
studies examining neural responses to colorectal distention use a much
larger balloon (7-8 cm long) and stimulate the rectum in addition to
the distal portion of the descending colon (Al-Chaer et al.
1996; Kawakita et al. 1997; Ness and
Gebhart 1987; Yang et al. 1998). In the present
study, a 1-cm balloon restricted to the descending colon was used.
PERIPHERAL RECEPTIVE FIELDS.
All neurons that responded to bDNP and bPN electrical stimulation also
responded to stimulation of their respective cutaneous and
mucocutaneous targets [as discussed in the preceding text and as seen
previously in MRF (Hubscher and Johnson 1996)].
Convergent input from sources outside the pudendal/pelvic territories
were also found, including inputs confined to distal body parts (e.g., ears, toes of forepaw and hindpaw). Only some of the neurons received convergent inputs from the entire body. In most thalamic regions, the
responses were elicited by noxious levels of mechanical stimulation (moderate to strong pinch). In the lateral (dorsal and posterior) and
medial-dorsal subnuclei, some neurons were found with low-threshold cutaneous receptive fields. The findings of noxious cutaneous inputs
with large, mostly excitatory and bilateral response
properties/receptive field characteristics is consistent with previous
electrophysiological recording studies in rat thalamus
(Dostrovsky and Guilbaud 1990; Guilbaud et al.
1980; Kawakita et al. 1993; Prieto-Gomez
et al. 1989). However, evidence showing neurons with small
contralateral receptive fields with convergent visceral input (e.g.,
Al-Chaer et al. 1996; Berkley et al.
1993b; Yang et al. 1998) suggest that DNP-responsive thalamic neurons represent a distinct subpopulation of
thalamic neurons. Moreover, none of the low-threshold (tactile) penile-responsive neurons in the present study lacked a cutaneous convergent territory, suggesting that the receptive field specificity typical for many thalamic cutaneous neurons may not exist for mucocutaneous penile tissue.
). Response modulation of VB neurons with DNP (i.e.,
penile) stimulation could exert its influence during mating, for
example. However, nonspecific modulation was observed (i.e., noxious
stimulation of various cutaneous fields exerted the same modulatory
effect), suggesting that these neurons may be part of the circuitry
important for more global functions, such as autonomic responses
related to behavior and emotion (Allen et al. 1991;
Cechetto 1987).
VARIATIONS AMONG DIFFERENT THALAMIC SUBNUCLEI.
DNP-responsive neurons were found throughout the thalamus. Regional
differences in response properties were observed (Figs. 2 and 5). For
example, the majority of neurons tested within intralaminar and
posterior nuclear regions responded to high-threshold levels of penile
stimulation versus the majority of those in medial and ventral areas
which responded to both low- and high-threshold levels of stimulation
(Fig. 5). In contrast, most DNP-responsive neurons in lateral-dorsal
divisions of thalamus required wind-up with either the DNP search
stimulus or a sustained pinch to respond (usually to a distal cutaneous
structure such as the ears or a single digit of the forepaw or
hindpaw). In addition, most of the neurons with spontaneous activity
that were inhibited by DNP stimulation were localized within the
reticular nucleus of the thalamus, which is known as a generator of
GABA-mediated inhibition within the thalamus (Thomson
1988). These differences in responses among the various
thalamic subregions are likely due to the different functions subserved
by each of these regions (see FUNCTIONAL CONSIDERATIONS).
, 1994b) but are different from
those found for the squirrel monkey (Bruggemann et al.
1994a) where visceroceptive neurons were found in VPL proper.
These variable results may be due to species differences. However,
other studies using rats have found visceroceptive neurons (uterus,
colon) in VB proper (Al-Chaer et al. 1996;
Berkley et al. 1993a). These differences may be due to
one or more of the following: different search protocols, different
types of tissue (visceral vs. mucocutaneous), sex differences, or other
methodological differences [such as depth of anesthesia
(Friedberg et al. 1999)].
Two neurons with small contralateral receptive fields on the face found
medially in VB (see Figs. 2 and 7), however, were not DNP-responsive
but were modulated when stimulated simultaneously with DNP or pinching
of the penis. This effect was not exclusive to the penis (mucocutaneous
tissue) because pinching of a single digit on the hindpaw also
modulated the responses as well. Perhaps some of the DNP-responsive
neurons in adjacent nuclei that receive convergent inputs from many
parts of the body have dendritic arbors that extend into VB to exert
this modulatory effect. These effects once again reflect the dynamic
nature of central neurons (see previous discussions on access vs. usage
in Berkley and Hubscher 1995b; Hubscher and
Johnson 1999b).
THALAMIC INPUTS/OUTPUTS.
Activation of neurons in the parvicellular part of the
subparafascicular nucleus in caudal thalamus has been demonstrated following sexual behavior (Veening and Coolen 1998).
These neurons have been shown to be interconnected (bidirectional) with
the medial preoptic area, which is an essential site for the regulation of male sexual behavior (Coolen et al. 1998). The
pathways through which DNP inputs reach the thalamus, however, are
unknown and will be the subject of future studies. All of the thalamic
regions containing DNP-responsive neurons receive inputs from multiple sources. Some possibilities may include both direct second-order projections from neurons within one of the three main ports of entry
into the CNS (i.e., spinal cord, dorsal column nuclei, or solitary
nuclei) as well as indirect projections via multiple synaptic relays
(e.g., a spinoreticulothalamic pathway or a postsynaptic-dorsal column-medial leminiscal pathway).
) demonstrated a large area of primary sensory cortex activated by stimulation of penile afferent fibers and concluded
with a proposed modification of the human male sensory homunculus.
Recent investigations of the representation of pelvic/visceral sensory
inputs in the human brain have shown a vast network of cortical regions
activated during micturition (Nour et al. 2000), anal/rectal (Lotze et al. 2001), and esophageal
(Aziz et al. 2000) stimulation. A number of experimental
studies in the rat have shown cortical neurons with visceral inputs,
many with somatovisceral convergence (Allen et al. 1991;
Follett and Dirks 1994, 1995; Ito 1998).
FUNCTIONAL CONSIDERATIONS.
Neurons in several different thalamic subregions responded to inputs
from the male genitalia. These regions are known to serve many
different functions (e.g., Davis et al. 1995;
Duncan et al. 1998; Lenz and Dougherty
1997; McAlonan et al. 2000; Portas et al.
1998; Shibata 2000; Sziklas and Petrides
1999). For example, nociceptive neurons in medial and lateral
thalamus are likely involved in the processing of information related
to affective/motivational and sensory discriminative aspects of pain,
respectively (see references in Apkarian and Shi 1994).
These functional implications for nociceptive thalamic neurons are
based on sources of inputs to some of the subregions within medial and
lateral thalamus [spinoreticulothalamic vs. spinothalamic,
respectively (Peschanski and Besson 1984)], response
properties for many of the neurons such as receptive field size/degree
of convergence [large/bilateral/complex vs. small/unilateral,
respectively; see references in Willis and Coggeshall (1991)] and outputs to cortex (Willis 1995).
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ACKNOWLEDGMENTS |
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The authors thank V. Dugan for excellent technical assistance.
Experiments were performed at the University of Florida and were supported by a fellowship to C. Hubscher from the Paralyzed Veterans of America and a grant from the Brain and Spinal Cord Injury Rehabilitation Trust Fund of Florida.
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FOOTNOTES |
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Address for reprint requests: C. H. Hubscher, Dept. of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, KY 40292 (E-mail: chhubs01{at}gwise.louisville.edu).
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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; n = 133) and neurons responsive
to stimulation of small unilateral cutaneous receptive fields but not
DNP (
,
search regions. Distances in mm are relative to bregma. LPLR, lateral
posterior, laterorostral; LPMR, lateral posterior, mediorostral; MDC,
mediodorsal, central; MDL, mediodorsal, lateral; MDM, mediodorsal,
medial; Po, posterior; SubD, submedius, dorsal; SubV, submedius,
ventral; VA, ventral anterior; VPPC, ventral posterior, parvicellular.
Thalamic diagrams modified from Paxinos and Watson
(1997)
