The modulation of sensory transmission through the medullary dorsal horn during cortically driven mastication

1986 ◽  
Vol 64 (7) ◽  
pp. 999-1005 ◽  
Author(s):  
Joong Soo Kim ◽  
M. Catherine Bushnell ◽  
Gary H. Duncan ◽  
James P. Lund

During mastication, reflexes are modulated and sensory transmission is altered in interneurons and ascending pathways of the rostral trigeminal sensory complex. The current experiment examines the modulation of sensory transmission through the most caudal part of the trigeminal sensory system, the medullary dorsal horn, during fictive mastication produced by cortical stimulation. Extracellular single unit activity was recorded from the medullary dorsal horn, and multiple unit activity was recorded from the trigeminal motor nucleus in anesthetized, paralyzed rabbits. The masticatory area of sensorimotor cortex was stimulated to produce rhythmic activity in the trigeminal motor nucleus (fictive mastication). Activity in the dorsal horn was compared in the presence and absence of cortical stimulation. Fifty-two percent of neurons classified as low threshold and 83% of neurons receiving noxious inputs were influenced by cortical stimulation. The cortical effects were mainly inhibitory, but 21% of wide dynamic range and 6% of low threshold cells were excited by cortical stimulation. The modulation produced by cortical stimulation, whether inhibitory or excitatory, was not phasically related to the masticatory cycle. It is likely that, when masticatory movements are commanded by the sensorimotor cortex, the program includes tonic changes in sensory transmission through 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.


1983 ◽  
Vol 49 (4) ◽  
pp. 948-960 ◽  
Author(s):  
J. O. Dostrovsky ◽  
Y. Shah ◽  
B. G. Gray

1. This study examined the inhibitory effects elicited by brain stem stimulation on the somatosensory responses of trigeminal medullary dorsal horn (subnucleus caudalis of the spinal trigeminal nucleus) neurons. Single-unit extracellular recordings were obtained in chloralose-anesthetized cats. Neurons were classified as wide dynamic range (WDR), nociceptive specific (NS), or low-threshold mechanoreceptive (LTM). Conditioning stimuli were delivered to the periaqueductal gray (PAG), nucleus cuneiformis (CU), nucleus raphe magnus (NRM), nucleus reticularis gigantocellularis (NGC), and nucleus reticularis magnocellularis (NMC). 2. Over 97% of the neurons tested could be inhibited by stimulation in all regions except PAG. Stimulation in the PAG inhibited 91% of the neurons tested. There was no statistically significant difference in the incidence of inhibition of WDR and NS nociceptive (noci) neurons and the LTM nonnociceptive (nonnoci) neurons. 3. Mean stimulation intensities necessary to produce inhibition were determined for each neuron from each stimulation site. The current thresholds necessary to inhibit the responses of noci neurons were found to be significantly lower, on the average, than those of nonnoci neurons at stimulation sites in the PAG, CU, and NGC. 4. Inhibition of the responses of WDR neurons required a lower mean current than for NS neurons but was statistically significant only for PAG and NGC. Thresholds for inhibiting the responses of NS neurons were similar to those for inhibiting the responses of LTM neurons for all regions except CU, where LTM thresholds were markedly but not significantly higher. 5. Stimulation thresholds were found to be lowest in NMC, while in NGC, NRM, and CU they were all similar and slightly higher. Stimulation in the PAG required the highest currents to produce inhibition. 6. These results indicate that stimulation in NRM and PAG not only inhibits the responses of noci neurons but also those of nonnoci neurons. Furthermore, stimulation in reticular regions adjacent to NRM and PAG is frequently even more effective in inhibiting the responses of both noci and nonnoci neurons. In addition, WDR neurons are more effectively inhibited than NS or LTM neurons. These results are compared with those obtained using similar methods in cat lumbar dorsal horn.


1989 ◽  
Vol 61 (6) ◽  
pp. 1197-1206 ◽  
Author(s):  
J. W. Hu ◽  
B. J. Sessle

1. Effects of deafferentation of the tooth pulps of the posterior mandibular teeth were studied in single neurons recorded in the ipsilateral subnucleus caudalis of the trigeminal (V) spinal tract nucleus of adult cats and kittens. The functional properties of neurons in each anesthetized animal were determined electro-physiologically in a series of microelectrode penetrations of the subnucleus. 2. The more than 800 neurons investigated could be subdivided on the basis of their cutaneous mechanoreceptive field properties into low-threshold mechanoreceptive (LTM) neurons, wide dynamic range (WDR) neurons, or nociceptive-specific (NS) neurons. Comparisons of neuronal properties were made between control (intact) cats and 7-15 day deafferented cats studied in a blind design, as well as groups of longer term deafferented cats, and kittens undergoing a “natural” deafferentation as a result of exfoliation of primary teeth. 3. There was no apparent change in the somatotopic pattern of organization of the subnucleus in the kittens and pulp-deafferented cats and no statistically significant differences were noted between kittens and control cats in any property except for alterations in the incidence of spontaneously active neurons. 4. Limited but statistically significant alterations were noted in some of the neuronal properties in the deafferented cats. These changes were especially apparent in the LTM neurons. The incidence of spontaneous activity was significantly decreased in the neurons of most long-term deafferented groups of cats. In the 7–15 day deafferented group, significantly more LTM neurons had a mechanoreceptive field involving all three divisions of the V nerve, and there was a significant increase in the incidence of LTM neurons activated by electrical stimulation of intraoral sites. Mechanosensitive neurons responsive only to tap stimuli were found only in the deafferented groups of cats. 5. These alterations in caudalis contrast with previous reports claiming marked hyperexcitability of caudal V brain stem neurons as a consequence of deafferentation and implicating such effects in the development of pain. However, some of the changes are in general not inconsistent with deafferentation-induced changes reported in spinal somatosensory neurons and with the pulp deafferentation-induced changes that we have recently documented in LTM neurons of subnucleus oralis of the V spinal tract nucleus of adult cats.(ABSTRACT TRUNCATED AT 400 WORDS)


2001 ◽  
Vol 86 (6) ◽  
pp. 2868-2877 ◽  
Author(s):  
Koichi Iwata ◽  
Takao Imai ◽  
Yoshiyuki Tsuboi ◽  
Akimasa Tashiro ◽  
Akiko Ogawa ◽  
...  

The effects of inferior alveolar nerve (IAN) transection on escape behavior and MDH neuronal activity to noxious and nonnoxious stimulation of the face were precisely analyzed. Relative thresholds for escape from mechanical stimulation applied to the whisker pad area ipsilateral to the transection were significantly lower than that for the contralateral and sham-operated whisker pad until 28 days after the transection, then returned to the preoperative level at 40 days after transection. A total of 540 neurons were recorded from the medullary dorsal horn (MDH) of the nontreated naive rats [low-threshold mechanoreceptive (LTM), 27; wide dynamic range (WDR), 31; nociceptive specific (NS), 11] and sham-operated rats with skin incision (LTM, 34; WDR, 30; NS, 23) and from the ipsilateral (LTM, 82; WDR, 82; NS, 31) and contralateral MDH relative to the IAN transection (LTM, 77; WDR, 82; NS, 33). The electrophysiological properties of these neurons were precisely analyzed. Background activity of WDR neurons on the ipsilateral side relative to the transection was significantly increased at 2–14 days after the operation as compared with that of naive rats. Innocuous and noxious mechanical-evoked responses of LTM and WDR neurons were significantly enhanced at 2–14 days after IAN transection. The mean area of the receptive fields of WDR neurons was significantly larger on the ipsilateral MDH at 2–7 days after transection than that of naive rats. We could not observe any modulation of thermal responses of WDR and NS neurons following IAN transection. Also, no MDH neurons were significantly affected in the rats with sham operations. The present findings suggest that the increment of neuronal activity of WDR neurons in the MDH following IAN transection may play an important role in the development of the mechano-allodynia induced in the area adjacent to the area innervated by the injured nerve.


1984 ◽  
Vol 52 (1) ◽  
pp. 170-187 ◽  
Author(s):  
M. C. Bushnell ◽  
G. H. Duncan ◽  
R. Dubner ◽  
L. F. He

We analyzed the activity of 51 trigeminothalamic neurons in the medullary dorsal horn (trigeminal nucleus caudalis) of monkeys during the performance of behavioral tasks requiring the monkeys to discriminate innocuous and noxious thermal stimuli applied to the face and to detect the onset of visual stimuli. Static properties of trigeminothalamic neurons in behaving monkeys were similar to those in anesthetized monkeys. Responses to passively presented mechanical and thermal stimuli, receptive-field properties, and conduction velocities did not differ in the awake and anesthetized states. For most wide dynamic range and nociceptive-specific trigeminothalamic neurons, there was a negative correlation between the magnitude of thermally evoked activity and behavioral latencies to discriminate 47 and 49 degrees C stimuli. Thus, both groups of neurons provide information that could be used by the monkey to discriminate noxious thermal stimuli. The magnitude of thermal responses of trigeminothalamic neurons was modulated by the behavioral significance of the stimulus. Behaviorally relevant thermal stimuli presented during the thermal discrimination task produced a greater neuronal response than equivalent irrelevant thermal stimuli presented between behavioral trials or presented while the monkey performed the visual detection task. Neurons whose activity is modulated by behavioral state are likely to be involved in discrimination of thermal stimuli, since the activity of these neurons correlates with the behavioral response to the stimuli and information from the modulated neurons is sent to the thalamus. Some trigeminothalamic neurons that exhibited somatosensory responses also responded to behaviorally relevant stimuli and events associated with trial initiation and receipt of reward in the behavioral tasks. Similar events outside a behavioral task evoked no neuronal responses. These task-related responses were similar to those described previously for medullary dorsal horn neurons not identified as to projection sites (14).(ABSTRACT TRUNCATED AT 400 WORDS)


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.


2002 ◽  
Vol 68 (4) ◽  
pp. 479-488 ◽  
Author(s):  
Fusami Gojyo ◽  
Shinichi Sugiyo ◽  
Ryotaro Kuroda ◽  
Atsufumi Kawabata ◽  
Vidya Varathan ◽  
...  

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.


2000 ◽  
Vol 84 (3) ◽  
pp. 1180-1185 ◽  
Author(s):  
Xijing Zhang ◽  
Christopher N. Honda ◽  
Glenn J. Giesler

Percutaneous upper cervical cordotomy continues to be performed on patients suffering from several types of severe chronic pain. It is believed that the operation is effective because it cuts the spinothalamic tract (STT), a primary pathway carrying nociceptive information from the spinal cord to the brain in humans. In recent years, there has been controversy regarding the location of STT axons within the spinal cord. The aim of this study was to determine the locations of STT axons within the spinal cord white matter of C2 segment in monkeys using methods of antidromic activation. Twenty lumbar STT cells were isolated. Eleven were classified as wide dynamic range neurons, six as high-threshold cells, and three as low-threshold cells. Eleven STT neurons were recorded in the deep dorsal horn and nine in superficial dorsal horn. The axons of the examined neurons were located at antidromic low-threshold points (<30 μA) within the contralateral lateral funiculus of C2. All low-threshold points were located ventral to the denticulate ligament, within the lateral half of the ventral lateral funiculus (VLF). None were found in the dorsal half of the lateral funiculus. The present findings support our previous suggestion that STT axons migrate ventrally as they ascend the length of the spinal cord. Also, the present findings indicate that surgical cordotomies that interrupt the VLF in C2 likely disrupt the entire lumbar STT.


1983 ◽  
Vol 49 (2) ◽  
pp. 424-441 ◽  
Author(s):  
R. P. Yezierski ◽  
K. D. Gerhart ◽  
B. J. Schrock ◽  
W. D. Willis

1. Stimulation of the sensorimotor cortex was found to excite and/or inhibit nociceptive spinothalamic tract cells. Thirteen wide dynamic range cells were inhibited by cortical stimulation, 6 were excited and 14 were both excited and inhibited. Four of six high-threshold cells were excited and one was inhibited. 2. Intermediate (200 ms) or long (2 s) duration conditioning trains were effective in reducing responses of spinothalamic cells evoked by noxious mechanical or thermal stimuli and by A- and C-fiber volleys in the sural nerve. Preferential inhibition of low-threshold responses with little or no effect on high-threshold discharges was observed in some cases. 3. Inhibitory actions were obtained primarily from stimulation of the SI sensory cortex and area 5, while excitation or excitation followed by inhibition was the dominant effect from motor cortex (area 4). Spinothalamic cells were also excited by stimulation of the medullary pyramid. 4. In eight animals extensive mapping of the sensorimotor cortex showed that for a given cell, stimulation of the sensory cortex produced inhibition while stimulation of motor cortex resulted in excitation. 5. The average latency of inhibition from sensory cortex was 29.8 +/- 10 ms, while the average latency of excitation from motor cortex was significantly shorter, 13.5 +/- 9 ms. The shortest latencies for excitation from pyramidal stimulation in the cases evaluated ranged from 2 to 9 ms. 6. Spinal cord lesions were made in five animals to determine the descending pathway(s) mediating corticofugal effects. Cortical and pyramidal effects were eliminated or considerably reduced by lesions involving the dorsal part of the lateral funiculus. This observation combined with latency data suggest that the corticospinal tract may be involved in the mediation of cortical excitation, while both pyramidal and extrapyramidal pathways are likely to be involved in cortical inhibition.


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