Comparison of responses of cutaneous nociceptive and nonnociceptive brain stem neurons in trigeminal subnucleus caudalis (medullary dorsal horn) and subnucleus oralis to natural and electrical stimulation of tooth pulp

1984 ◽  
Vol 52 (1) ◽  
pp. 39-53 ◽  
Author(s):  
J. W. Hu ◽  
B. J. Sessle

The activity of 160 single neurons excited by electrical stimulation of the canine tooth pulp was studied in the subnucleus caudalis (medullary dorsal horn) and the subnucleus oralis of the trigeminal (V) spinal tract nucleus in chloralose-anesthetized cats to test the effects of natural as well as electrical stimulation of the tooth pulp. The neurons were functionally classified on the basis of their cutaneous receptive-field properties as low-threshold mechanoreceptive (LTM), wide dynamic range (WDR), or nociceptive specific (NS). The orofacial receptive-field properties and responses evoked by electrical stimulation of the tooth pulp indicated that the oralis and caudalis neurons examined had characteristics typical of those previously documented for oralis LTM neurons and for caudalis LTM, WDR, and NS neurons. Each neuron was also tested with cold and warm stimulation of the canine tooth, and some neurons were also tested for responsiveness to thermal stimulation of the premolar tooth or to mechanical and chemical stimuli delivered to the dentine of the canine tooth. Although all the neurons could be excited by electrical stimulation of the pulp, we found that the only neurons that consistently responded to thermal pulp stimuli were those located in the V subnucleus caudalis. Moreover, only those caudalis neurons that had been functionally classified as nociceptive (4 WDR and 21 NS neurons) showed this responsiveness. Heating of the canine or premolar tooth excited 24 of these 25 nociceptive neurons; cooling activated only 3, and none of the small number of neurons tested with mechanical and chemical stimulation of the dentine was excited. The response of the nociceptive neurons to heating of the tooth contrasted with the responses of the same neurons to pinching and heating of their cutaneous receptive field.(ABSTRACT TRUNCATED AT 400 WORDS)

1988 ◽  
Vol 59 (5) ◽  
pp. 1575-1589 ◽  
Author(s):  
J. G. Broton ◽  
J. W. Hu ◽  
B. J. Sessle

1. The extracellular activity of 196 single neurons in subnucleus caudalis (medullary dorsal horn) of the trigeminal (V) spinal tract nucleus was examined in chloralose-anesthesized, paralyzed cats. Electrical, mechanical, and algesic chemical stimuli were applied to the exposed temporomandibular joint (TMJ) in order to activate TMJ afferents. Seventy-eight neurons were studied that responded to electrical stimulation of the TMJ at a mean latency of 9.9 +/- 4.8 (SD) ms. 2. All neurons with TMJ input received additional afferent input, predominantly from facial skin or intraoral sites. Caudalis neurons were classified on the basis of their cutaneous mechanoreceptive field properties as low-threshold mechanoreceptive (LTM), wide dynamic range (WDR), or nociceptive specific (NS); a few neurons unresponsive to cutaneous stimuli were responsive to manipulation of deep subcutaneous structures. A sample of caudalis neurons was tested for responsiveness to electrical TMJ stimulation after the mechanoreceptive field properties of the neurons were determined. In this sample, 24% of the LTM neurons, 29% of the WDR neurons, 36% of the NS neurons, and 57% of the neurons with input from deep structures were responsive to TMJ stimulation. The WDR and NS neurons with TMJ inputs had mechanoreceptive field properties and laminar locations in caudalis that were comparable to those previously described for cutaneous nociceptive neurons in caudalis; also in accordance with recent studies, 74% of the neurons tested showed convergence of tooth pulp and/or hypoglossal (XII) nerve afferent inputs. 3. In contrast to the LTM neurons, the WDR and NS neurons were especially responsive to intense mechanical and algesic chemical stimulation of the TMJ as well as to electrical stimulation of TMJ afferents. For example, 71% of the WDR and NS neurons excited by electrical stimulation of the TMJ afferents and tested for their responsiveness to injections of algesic chemicals (7% NaCl, KCl, bradykinin, histamine) into the TMJ responded to at least one of these chemicals. The temporal characteristics of these responses were quantified. 4. The TMJ afferent inputs to the WDR and NS neurons were considered to be predominantly of a nociceptive character because of (1) the long latency and high threshold of most TMJ-evoked responses, which are consistent with previous demonstrations that small-diameter afferents predominantly supply the TMJ and, (2) the preferential responsiveness to noxious mechanical and chemical stimulation of TMJ afferents of neurons which were functionally identified as cutaneous nociceptive neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


1985 ◽  
Vol 53 (6) ◽  
pp. 1387-1400 ◽  
Author(s):  
T. Yokota ◽  
N. Koyama ◽  
N. Matsumoto

Recordings were made from single thalamic units in the urethan-chloralose anesthetized cat. Altogether 2,905 trigeminal single units having a receptive field in the contralateral trigeminal integument were isolated from the somatosensory part of nucleus ventralis posteromedialis, or VPM proper. Each isolated unit was tested for responses to a series of mechanical stimuli. The stimuli included brushing the skin, touch, pressure, noxious pinch, and pinpricks. The majority of VPM proper units responded with the greatest discharge frequency to gentle mechanical stimulation: either hair movement or light pressure to the trigeminal integument, but 341 units were identified as trigeminal nociceptive units. They were partitioned into two functionally defined subclasses, nociceptive specific (NS) and wide dynamic range (WDR) units, but not intermingled with low-threshold mechanoreceptive (LTM) units. Both NS and WDR units were found at or near the margin of the VPM proper but not outside this nucleus. This marginal area was referred to as the shell region of the VPM proper. A total of 248 NS units was found within the shell region of the caudal third of the VPM proper. This part was called the NS zone. These units were somatotopically organized. In the rostral part of the NS zone, ophthalmic NS units having a receptive field in the contralateral ophthalmic division were located dorsolaterally, maxillary NS units occurred dorsomedially, and mandibular NS units were found ventromedially. In the caudal part of the NS zone, maxillary NS units were encountered in the dorsal shell region, whereas mandibular NS units were found in the ventromedial shell region. Ophthalmic NS units were not found in this part of the NS zone. Altogether 93 WDR units were encountered in the shell region of the VPM proper. They were confined to a narrow band approximately 300 micron wide just rostral to the NS zone. These units were somatotopically organized. Ophthalmic WDR units having a low-threshold center of the receptive field in the contralateral ophthalmic division were located dorsolaterally, maxillary WDR units were located dorsomedially, and mandibular WDR units were located ventromedially. The majority of maxillary as well as mandibular WDR units were activated by electrical stimulation of the contralateral maxillary and/or mandibular canine tooth pulp afferents. Both NS and WDR zones of the VPM proper extended into the shell region of the nucleus ventralis posterolateralis (VPL).(ABSTRACT TRUNCATED AT 400 WORDS)


1986 ◽  
Vol 55 (2) ◽  
pp. 227-243 ◽  
Author(s):  
N. Amano ◽  
J. W. Hu ◽  
B. J. Sessle

The extracellular activity of single neurons was recorded in subnucleus caudalis (medullary dorsal horn) of chloralose-anesthetized cats to test the effects of electrical and natural stimuli that activated afferents supplying the jaw and tongue muscles as well as the face, teeth, and intraoral mucosa. Many caudalis neurons that could be functionally classified on the basis of their cutaneous receptive-field properties as low-threshold mechanoreceptive (LTM), wide-dynamic-range (WDR), or nociceptive-specific (NS) neurons could be excited by muscle afferent stimuli. Only five neurons were encountered that received muscle afferent inputs and had no demonstrable cutaneous, dental, or mucosal input. The muscle afferent inputs were a particular feature of the cutaneous nociceptive (i.e., WDR and NS) neurons. Approximately two-thirds of this nociceptive neuronal population (n = 109) could be excited by jaw and/or tongue muscle stimulation, whereas only a small proportion of the LTM neuronal population (n = 247) was activated by muscle afferent stimulation. Neurons with a demonstrated direct axonal projection to the contralateral thalamus as well as nonprojection neurons received muscle afferent inputs. The caudalis nociceptive neurons receiving muscle as well as cutaneous afferent inputs had receptive-field properties comparable to those previously described for caudalis cutaneous nociceptive neurons; they were predominantly located in laminae I/II and V/VI, and many also received convergence of tooth pulp afferent inputs. These neurons generally had larger cutaneous receptive fields than neurons unresponsive to muscle afferent stimulation. The muscle afferent inputs were considered to be predominantly of a nociceptive character for several reasons. These included the long latency and high threshold of most neuronal responses evoked by electrical stimulation of the muscle afferents, the predominance of afferents of small diameter in some of the muscle nerves stimulated, the preferential responsiveness to the muscle afferent stimulation of neurons that were functionally identified as cutaneous nociceptive neurons, and the responsiveness of most of the neurons excited by electrical stimulation of the muscle nerves also to noxious mechanical or thermal stimulation of muscle and the injection of two or more algesic chemicals into small arteries supplying the jaw and tongue muscles. Of the algesic chemicals used in this study (7% NaCl, KCl, bradykinin, histamine, 5-HT), the first two were found to be the most effective and to cause the most rapidly induced excitation.(ABSTRACT TRUNCATED AT 400 WORDS)


1986 ◽  
Vol 56 (1) ◽  
pp. 80-98 ◽  
Author(s):  
T. Yokota ◽  
Y. Nishikawa ◽  
N. Koyama

A population of neurons in the somatosensory part of the nucleus ventralis posteromedialis (VPM proper) that responded to electrical stimulation of the tooth pulp were studied in cats under urethan-chloralose anesthesia. Two classes of units responsive to electrical stimulation of the contralateral canine tooth pulp were identified. One class was responsive only to tooth pulp stimulation and these units were designated as tooth pulp specific (TPS) units. The other class of units responded to mechanical stimulation of the contralateral trigeminal integument in addition to tooth pulp stimulation. Their receptive field characteristics identified them as wide dynamic range (WDR) units responsive to tooth pulp stimulation. Both classes of units were located in the shell region of the caudal VPM proper; TPS units were coexistent with trigeminal nociceptive specific (NS) units and were found in the dorsomedial as well as ventromedial parts of the NS zone. WDR units responsive to electrical stimulation of the tooth pulp were located in the dorsomedial as well as ventromedial parts of WDR zone, a narrow band, approximately 300 micron wide, just in front of the NS zone. Tooth pulp units in the dorsomedial shell region of the VPM proper responded to the maxillary canine tooth pulp, whereas those in the ventromedial shell region responded to the mandibular canine tooth pulp. Some tooth pulp units in these two regions were responsive to stimulation of both maxillary and mandibular canine teeth. Both TPS and WDR units were antidromically excited by electrical stimulation of the SI area of the somatosensory cortex. Cooling the dorsolateral surface of the caudal medulla oblongata reversibly blocked tooth pulp evoked responses of TPS and WDR units. Trigeminal tractotomy just above the level of the obex irreversibly abolished tooth pulp-evoked responses of TPS and WDR units. These findings suggested that TPS neurons in the marginal layer of the trigeminal subnucleus caudalis and WDR neurons in the lateral part of the subnucleus reticularis dorsalis relay afferent impulses derived from the tooth pulp to the shell region of the VPM proper.


2006 ◽  
Vol 51 (10) ◽  
pp. 930-939
Author(s):  
Norio Matsumoto ◽  
Daisuke Fukuda ◽  
Junichiro Murata ◽  
Hiroyuki Yamada ◽  
Hiroyuki Miura ◽  
...  

1998 ◽  
Vol 80 (4) ◽  
pp. 2210-2214 ◽  
Author(s):  
Kai-Ming Zhang ◽  
Xiao-Min Wang ◽  
Angela M. Peterson ◽  
Wen-Yan Chen ◽  
Sukhbir S. Mokha

Kai-Ming Zhang, Xiao-Min Wang, Angela M. Peterson, Wen-Yan Chen, and Sukhbir S. Mokha. α2-Adrenoceptors modulate NMDA-evoked responses of neurons in the superficial and deeper dorsal horn of the medulla. J. Neurophysiol. 80: 2210–2214, 1998. Extracellular single unit recordings were made from neurons in the superficial and deeper dorsal horn of the medulla (trigeminal nucleus caudalis) in 21 male rats anesthetized with urethan. NMDA produced an antagonist-reversible excitation of 46 nociceptive as well as nonnociceptive neurons. Microiontophoretic application of a preferential α2-adrenoceptor (α2AR) agonist, (2-[2,6-dichloroaniline]-2-imidazoline) hydrochloride (clonidine), reduced the NMDA-evoked responses of 86% (6/7) of nociceptive-specific (NS) neurons, 82% (9/11) of wide dynamic range (WDR) neurons, and 67% (4/6) of low-threshold (LT) neurons in the superficial dorsal horn. In the deeper dorsal horn, clonidine inhibited the NMDA-evoked responses of 94% (16/17) of NS and WDR neurons and 60% (3/5) of LT neurons. Clonidine facilitated the NMDA-evoked responses in 14% (1/17) of NS, 9% (1/11) of WDR, and 33% (2/6) of LT neurons in the superficial dorsal horn. Idazoxan, an α2AR antagonist, reversed the inhibitory effect of clonidine in 90% (9/10) of neurons, whereas prazosin, an α1-adrenoceptor antagonist with affinity for α2BAR, and α2CAR, were ineffective. We suggest that activation of α2ARs produces a predominantly inhibitory modulation of the NMDA-evoked responses of nociceptive neurons in the medullary dorsal horn.


1986 ◽  
Vol 55 (6) ◽  
pp. 1187-1201 ◽  
Author(s):  
W. E. Renehan ◽  
M. F. Jacquin ◽  
R. D. Mooney ◽  
R. W. Rhoades

In Nembutal-anesthetized rats, 31 physiologically identified medullary dorsal horn (MDH) cells were labeled with horseradish peroxidase (HRP). Ten responded only to deflection of one or more vibrissae. Six cells were activated by guard hair movement only, six by deflection of guard hairs or vibrissa(e), and seven by pinch of facial skin with serrated forceps. Different classes of low-threshold cells could not be distinguished on the basis of their somadendritic morphologies or laminar distribution. Neurons activated by multiple vibrissae were unique, however, in that one sent its axon into the medial lemniscus, and three projected into the trigeminal spinal tract. None of the guard hair-only or vibrissae-plus-guard hair neurons had such projections. Cells that responded best to noxious stimulation were located mainly in laminae I, II, and deep V, while neurons activated by vibrissa(e) and/or guard hair deflection were located in layers III, IV, and superficial V. Low-threshold neurons generally had fairly thick dendrites with few spines, whereas high-threshold cells tended to have thinner dendrites with numerous spines. Moreover, the dendritic arbors of low-threshold cells were, for the most part, denser than those of the noxious cells. Neurons with mandibular receptive fields were located in the dorsomedial portion of the MDH; cells with ophthalmic fields were found in the ventrolateral MDH, and maxillary cells were interposed. Cells sensitive to deflection of dorsal mystacial vibrissae and/or guard hairs were located ventral to those activated by more ventral hairs. Neurons with rostral receptive fields were found in the rostral MDH, while cells activated by hairs of the caudal mystacial pad, periauricular, and periorbital regions were located in the caudal MDH. Receptive-field types were encountered that have not been reported for trigeminal primary afferent neurons: multiple vibrissae; vibrissae plus guard hairs; and wide dynamic range. The latter two can be explained by the convergence of different primary afferent types onto individual neurons. Our failure to find a significant relationship between dendritic area (in the transverse plane) and the number of vibrissae suggests that primary afferent convergence may not be responsible for the synthesis of the multiple vibrissae receptive field. Excitatory connections between MDH neurons may, therefore, account for multiple vibrissae receptive fields in the MDH.


1989 ◽  
Vol 62 (2) ◽  
pp. 437-449 ◽  
Author(s):  
W. Maixner ◽  
R. Dubner ◽  
D. R. Kenshalo ◽  
M. C. Bushnell ◽  
J. L. Oliveras

1. We examined the activity of thermally sensitive trigeminothalamic neurons and nonprojection neurons in the medullary dorsal horn (trigeminal nucleus caudalis) in three monkeys performing thermal and visual detection tasks. 2. An examination of neuronal stimulus-response functions, obtained during thermal-detection tasks in which noxious heat stimuli were applied to the face, indicated that wide-dynamic-range neurons (WDR, responsive to innocuous mechanical stimuli with greater responses to noxious mechanical stimuli) could be subclassified based on the slope values of linear regression lines. WDR1 neurons exhibited significantly greater sensitivity to noxious heat stimulation than WDR2 neurons or nociceptive-specific neurons (NS, responsive only to noxious stimuli). 3. In one behavioral task, the monkeys detected 1.0 degrees C increases in noxious heat from preceding noxious heat stimuli ranging from 44 to 48 degrees C. WDR1, WDR2, and NS neurons increased their discharge frequency as a function of the intensity of the first noxious heat temperature (T1) as well as the final temperature (T2). The responses of WDR1 neurons were greater than those produced by WDR2 or NS neurons across all the temperatures examined. The order of stimulus presentation affected the responses of WDR1 neurons to 1.0 degrees C increases in the noxious heat range but not those of WDR2 or NS neurons. 4. In a second behavioral task, the monkeys detected small increases in noxious heat (0.2-0.8 degrees C) from a first temperature of 46 degrees C. Although the responses of all three classes of neurons were monotonically related to stimulus intensity, WDR1 neurons exhibited greater sensitivity to small temperature increases than either WDR2 or NS neurons. 5. Subpopulations of all three classes of neurons exhibited responses that were independent of thermal stimulus parameters or sensory modality and that only occurred during the behavioral task. These task-related responses were time-locked to specific behavioral events associated with trial initiation and trial continuation. 6. These data provide evidence that a subpopulation of WDR neurons is the dorsal horn cell type most sensitive to small increases in noxious heat in the 45-49 degrees C temperature range and provides the most information about stimulus intensity. The findings support the view that nociceptive neurons have the capacity to precisely encode stimulus features in the noxious range and that WDR neurons are likely to participate in the monkeys' ability to perceive the intensity of such stimuli.


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