Trigeminohypothalamic and Reticulohypothalamic Tract Neurons in the Upper Cervical Spinal Cord and Caudal Medulla of the Rat

2000 ◽  
Vol 84 (4) ◽  
pp. 2078-2112 ◽  
Author(s):  
Amy Malick ◽  
Rew M. Strassman ◽  
Rami Burstein

Sensory information that arises in orofacial organs facilitates exploratory, ingestive, and defensive behaviors that are essential to overall fitness and survival. Because the hypothalamus plays an important role in the execution of these behaviors, sensory signals conveyed by the trigeminal nerve must be available to this brain structure. Recent anatomical studies have shown that a large number of neurons in the upper cervical spinal cord and caudal medulla project directly to the hypothalamus. The goal of the present study was to identify the types of information that these neurons carry to the hypothalamus and to map the route of their ascending axonal projections. Single-unit recording and antidromic microstimulation techniques were used to identify 81 hypothalamic-projecting neurons in the caudal medulla and upper cervical (C1) spinal cord that exhibited trigeminal receptive fields. Of the 72 neurons whose locations were identified, 54 were in laminae I–V of the dorsal horn at the level of C1 ( n = 22) or nucleus caudalis (Vc, n = 32) and were considered trigeminohypothalamic tract (THT) neurons because these regions are within the main projection territory of trigeminal primary afferent fibers. The remaining 18 neurons were in the adjacent lateral reticular formation (LRF) and were considered reticulohypothalamic tract (RHT) neurons. The receptive fields of THT neurons were restricted to the innervation territory of the trigeminal nerve and included the tongue and lips, cornea, intracranial dura, and vibrissae. Based on their responses to mechanical stimulation of cutaneous or intraoral receptive fields, the majority of THT neurons were classified as nociceptive (38% high-threshold, HT, 42% wide-dynamic-range, WDR), but in comparison to the spinohypothalamic tract (SHT), a relatively high percentage of low-threshold (LT) neurons were also found (20%). Responses to thermal stimuli were found more commonly in WDR than in HT neurons: 75% of HT and 93% of WDR neurons responded to heat, while 16% of HT and 54% of WDR neurons responded to cold. These neurons responded primarily to noxious intensities of thermal stimulation. In contrast, all LT neurons responded to innocuous and noxious intensities of both heat and cold stimuli, a phenomenon that has not been described for other populations of mechanoreceptive LT neurons at spinal or trigeminal levels. In contrast to THT neurons, RHT neurons exhibited large and complex receptive fields, which extended over both orofacial (“trigeminal”) and extracephalic (“non-trigeminal”) skin areas. Their responses to stimulation of trigeminal receptive fields were greater than their responses to stimulation of non-trigeminal receptive fields, and their responses to innocuous stimuli were induced only when applied to trigeminal receptive fields. As described for SHT axons, the axons of THT and RHT neurons ascended through the contralateral brain stem to the supraoptic decussation (SOD) in the lateral hypothalamus; 57% of them then crossed the midline to reach the ipsilateral hypothalamus. Collateral projections were found in the superior colliculus, substantia nigra, red nucleus, anterior pretectal nucleus, and in the lateral, perifornical, dorsomedial, suprachiasmatic, and supraoptic hypothalamic nuclei. Additional projections (which have not been described previously for SHT neurons) were found rostral to the hypothalamus in the caudate-putamen, globus pallidus, and substantia innominata. The findings that nonnociceptive signals reach the hypothalamus primarily through the direct THT route, whereas nociceptive signals reach the hypothalamus through both the direct THT and the indirect RHT routes suggest that highly prioritized painful signals are transferred in parallel channels to ensure that this critical information reaches the hypothalamus, a brain area that regulates homeostasis and other humoral responses required for the survival of the organism.

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.


1996 ◽  
Vol 75 (6) ◽  
pp. 2606-2628 ◽  
Author(s):  
J. T. Katter ◽  
R. J. Dado ◽  
E. Kostarczyk ◽  
G. J. Giesler

1. A goal of this study was to determine whether neurons in the sacral spinal cord that project to the diencephalon are involved in the processing and transmission of sensory information that arises in the perineum and pelvis. Therefore, 58 neurons in segments L6-S2 were activated antidromically with currents < or = 30 microA from points in the contralateral diencephalon in rats that were anesthetized with urethan. 2. Responses to mechanical stimuli applied to the cutaneous receptive fields of these neurons were used to classify them as low-threshold (LT), wide dynamic range (WDR) or high-threshold (HT) neurons. Twenty-two neurons (38%) responded preferentially to brushing (LT neurons). Eighteen neurons (31%) responded to brushing but responded with higher firing frequencies to noxious mechanical stimuli (WDR neurons). Eighteen neurons (31%) responded only to noxious intensities of mechanical stimulation (HT neurons). LT neurons were recorded predominantly in nucleus proprius of the dorsal horn. Nociceptive neurons (WDR and HT) were recorded throughout the dorsal horn. 3. Cutaneous receptive fields were mapped for 56 neurons. Forty-five (80%) had receptive fields that included at least two of the following regions ipsilaterally: the rump, perineum, or tail. Eleven neurons (20%) had receptive fields that were restricted to one of these areas or to the ipsilateral hind limb. Thirty-eight neurons (68%) had cutaneous receptive fields that also included regions of the contralateral tail or perineum. On the perineum, receptive fields usually encompassed perianal and perivaginal areas including the clitoral sheath. There were no statistically significant differences in the locations or sizes of receptive fields for LT neurons compared with nociceptive (WDR and HT) neurons. 4. Thirty-seven LT, WDR, and HT neurons were tested for their responsiveness to heat stimuli. Five (14%) responded to increasing intensities of heat with graded increases in their firing frequencies. Thirty-two LT, WDR, and HT neurons also were tested with cold stimuli. None responded with graded increases in their firing frequencies to increasingly colder stimuli. There were no statistically significant differences among the responses of LT, WDR, and HT neurons to either heat or cold stimuli. 5. Forty LT, WDR, and HT neurons were tested for their responsiveness to visceral stimuli by distending a balloon placed into the rectum and colon with a series of increasing pressures. Seventeen (43%) exhibited graded increases in their firing frequencies in response to increasing pressures of colorectal distention (CrD). None of the responsive neurons responded reproducibly to CrD at an intensity of 20 mmHg, and all responded at intensities of > or = 80 mmHg. More than 90% responded abruptly at stimulus onset, responded continuously throughout the stimulus period, and stopped responding immediately after termination of the stimulus. 6. Thirty-one neurons were tested for their responsiveness to distention of a balloon placed inside the vagina. Eleven (35%) exhibited graded increases in their firing frequencies in response to increasing pressures of vaginal distention (VaD). The thresholds and temporal profiles of the responses to VaD were similar to those for CrD. Twenty-nine neurons were tested with both CrD and VaD. Thirteen (45%) were excited by both stimuli, four (14%) responded to CrD but not VaD, and one (3%) was excited by VaD but not CrD. Neurons excited by CrD, VaD, or both were recorded throughout the dorsal horn. 7. As a population, WDR neurons, but not LT or HT neurons, encoded increasing pressures of CrD and VaD with graded increases in their firing frequencies. The responses of WDR neurons to CrD differed significantly from those of either LT or HT neurons. Regression analyses of the stimulus-response functions of responsive WDR neurons to CrD and VaD were described by power functions with exponents of 1.6 and 2.4, respectively.(ABSTRACT TRUNCATED)


2002 ◽  
Vol 87 (1) ◽  
pp. 469-477 ◽  
Author(s):  
K. M. Horn ◽  
M. Pong ◽  
S. R. Batni ◽  
S. M. Levy ◽  
A. R. Gibson

Magnocellular (RNm) and parvicellular (RNp) divisions of the cat red nucleus (RN) project to the cervical spinal cord. RNp projects more heavily to upper cervical levels and RNm projects more heavily to lower levels. The cells in RN are active during reaching and grasping, and the differences in termination suggest that the divisions influence different musculature during this behavior. However, the spinal termination may not reflect function because most rubrospinal terminations are to interneuronal regions, which can influence motor neurons at other spinal levels. To test for functional differences between RNm and RNp, we selectively stimulated RNm and RNp as well as the efferent fibers from each region. Electromyographic activity was recorded from seven muscles of the cat forelimb during reaching. The activity from each muscle was averaged over several thousand stimuli to detect influences of stimulation on muscle activity. Stimulation within the RN produced a characteristic pattern of poststimulus effects. The digit dorsiflexor, extensor digitorum communis (edc), was most likely to show facilitation, and several other muscles showed suppression. The pattern of activation did not differ between RNm and RNp. In contrast, stimulation of RNp fibers favored facilitation of shoulder muscles (spinodeltoideus and supraspinatus), and stimulation of RNm fibers favored facilitation of digit and wrist muscles (edc, palmaris longus, and extensor carpi ulnaris). Fiber stimulation produced few instances of poststimulus suppression. The results from fiber stimulation indicate that the physiological actions of RNm and RNp match their levels of spinal termination. The complex pattern of facilitation and suppression seen with RN stimulation may reflect synaptic actions within the nucleus.


1989 ◽  
Vol 61 (6) ◽  
pp. 1153-1160 ◽  
Author(s):  
H. Hayashi ◽  
T. Tabata

1. One hundred forty-one trigeminomesencephalic neurons in the sensory trigeminal nucleus of cats anesthetized with alpha-chloralose were identified by antidromic stimulation of the mesencephalic parabrachial area (PBA) which includes the nucleus cuneiformis, lateral periaqueductal gray matter, and the region between the inferior colliculus and brachium conjunctivum. 2. Neurons were categorized based on their responses to non-noxious and noxious mechanical and heat stimuli delivered to their peripheral receptive fields (RFs) including skin, mucosa, guard hairs, vibrissae, cornea, and tooth pulps. They were classified into three types: 48 nociceptive-specific (NS) neurons which responded to heavy pressure and/or noxious mechanical stimuli, and/or noxious radiant heat; 19 wide dynamic range (WDR) neurons which had a graded response to light tactile stimuli, noxious pinch, and/or noxious radiant heat; and 36 low-threshold mechanoreceptive (LTM) neurons which responded maximally to innocuous tactile stimuli. In subnucleus caudalis (Vc), NS and WDR neurons were the majority (75%) among the three types, while in the rostral subnuclei they were about one-half (54%) of the population. 3. The RFs were distributed over the orofacial and head region but mainly in the facial region. Twelve neurons (33% of the LTM neurons) responded to deflection of vibrissae and only 1 NS neuron out of 52 NS and WDR neurons tested responded to electrical stimulation of a tooth pulp. 4. A contralateral projection was dominant (57%), 30% projected ipsilaterally and 13% projected bilaterally.(ABSTRACT TRUNCATED AT 250 WORDS)


1992 ◽  
Vol 67 (5) ◽  
pp. 1092-1104 ◽  
Author(s):  
W. D. Hutchison ◽  
M. A. Luhn ◽  
R. F. Schmidt

1. Experiments were carried out in chloralose-anesthetized cats to study the responses of neurons in the lateral thalamus to excitation of afferent fibres from the knee joint. 2. Single- and multi-unit recordings were made with tungsten electrodes in dorsoventral penetrations through the ventral posterior lateral nucleus (VPL) during electrical stimulation of the medial articular nerve (MAN) of the cat's knee joint at an intensity sufficient to excite slowly conducting unmyelinated fibers. The locations of the recording sites were verified by recovering electrolytic lesion sites in histological sections (Nissl and cytochrome oxidase staining). 3. The average earliest latency for excitation of thalamic responses was 19.1 +/- 8.5 (SD) ms (n = 50). The threshold for excitation of most thalamic units was found to correspond to peripheral joint afferent fibers of the A-delta group. 4. The majority of neurons responding to MAN stimulation were found to be dorsal or ventral to the low-threshold cutaneous hindlimb region of the lateral division of the VPL (stereotaxic coordinates: AP 9.0-11.5; ML 7.0-9.5). In the ventral periphery of the VPL, most neurons responding to MAN stimulation (11/14) were wide dynamic range (WDR) with a discrete cutaneous receptive field on the hindpaw digits. Six WDR neurons were found dorsal to the hindlimb VPL with a convergent receptive field on the hindlimb (but not hindpaw digits). No nociceptive-specific knee joint units were found. 5. Other neurons were found dorsal to the hindlimb VPL with large receptive fields often encompassing the whole contralateral leg, including skin and deep hindlimb structures, possibly in a region described as the dorsal portion of the posterior complex (POd). Some neurons were found with no receptive field. 6. This study provides the first observations on the responses of lateral thalamic neurons to stimulation of the MAN of the cat knee joint. These results demonstrate a central pathway conveying impulses from specific deep joint afferents of the MAN to the peripheral region of the VPL and overlying region known as the POd, regions implicated in the transmission of nociceptive information.


1992 ◽  
Vol 68 (2) ◽  
pp. 384-391 ◽  
Author(s):  
J. X. Hao ◽  
X. J. Xu ◽  
Y. X. Yu ◽  
A. Seiger ◽  
Z. Wiesenfeld-Hallin

1. The activity of 197 single dorsal horn neurons was recorded extracellularly in the spinal cord of decerebrate, spinalized, unanesthetized rats. The response properties of 174 wide dynamic range (WDR) neurons to electrical, mechanical, and thermal stimulation in three groups of rats were studied:normal, 1-4 days after transient spinal cord ischemia induced photochemically by laser irradiation when the rats exhibited behavioral hypersensitivity to mechanical stimuli (allodynia), and 10-20 days after spinal ischemia when the allodynia had ceased. 2. In normal rats, the responses of dorsal horn WDR neurons to suprathreshold electrical stimulation of their receptive fields consisted of a short-latency (A) and a long-latency (C) response. In 77% of the neurons (57/74), there was a separation between the A- and C-fiber responses. The response threshold (defined as 20% increase in neuronal discharges above background activity) to mechanical stimulation applied with calibrated von Frey hairs was 13.8 g, and the discharges of these neurons to graded stimulation increased linearly. 3. In 68% of WDR neurons in allodynic rats (38/56), the response to suprathreshold electrical stimuli was a single burst with no separation between A- and C-fiber responses. The magnitude and duration of the response were significantly increased compared with those recorded in normal rats. The sensitivity of these neurons to mechanical stimulation was also greatly increased, expressed by a lowered threshold (2.1 +/- 0.3 g, mean +/- SE) and a shift to the left of the nonlinear stimulus-response curve. The background activity of the neurons and the size of the receptive fields were, however, unchanged.(ABSTRACT TRUNCATED AT 250 WORDS)


Cephalalgia ◽  
1995 ◽  
Vol 15 (3) ◽  
pp. 191-199 ◽  
Author(s):  
H Angus-Leppan ◽  
B Olausson ◽  
P Boers ◽  
GA Lambert

We have previously shown convergence of craniovascular and tooth pulp afferents in the cervical spinal cord of cats. This study looked for similar convergence in the thalamus. Fifty-four thalamic cells with input from tooth pulp, superior sagittal sinus, or both, were identified. Twenty-nine cells with tooth pulp and superior sagittal sinus input were located in the ventrobasal complex or the intralaminar nuclei. Most of these 29 cells were also excited by cooling the contralateral tooth pulp, and 21 had receptive fields on the contralateral face or forelimb. Twenty cells excited by stimulation of superior sagittal sinus, and not tooth pulp, were found in several nuclei. The 5 cells excited by stimulation of tooth pulp, but not sagittal sinus, were restricted to the ventrobasal complex. The data confirm convergence from sagittal sinus, tooth pulp, and skin in the thalamus of anaesthetized cats.


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