Physiological characterization of spinohypothalamic tract neurons in the lumbar enlargement of rats

1991 ◽  
Vol 66 (1) ◽  
pp. 261-284 ◽  
Author(s):  
R. Burstein ◽  
R. J. Dado ◽  
K. D. Cliffer ◽  
G. J. Giesler

1. Ninety-six neurons in the lumbar enlargement of urethananesthetized rats were antidromically activated from the contralateral hypothalamus. The antidromic stimulating electrode was moved systematically within the hypothalamus until antidromic activation could be produced with currents of less than or equal to 50 microA (18.6 +/- 10.8 microA; mean +/- SD). The points at which antidromic activation thresholds were lowest were found in several regions of the hypothalamus but were concentrated in the optic tract and the supraoptic decussation. 2. The recording locations of 79 spinohypothalamic tract (SHT) neurons were marked and recovered. Twenty-nine were located in the superficial dorsal horn (SDH), 42 in the deep dorsal horn (DDH), 4 in the intermediate zone, and 2 in the gray matter surrounding the central canal. Two additional marks were located in the dorsal lateral funiculus (DLF). 3. The responses of 46 SHT neurons were examined during innocuous and noxious mechanical stimulation of their receptive fields. Forty-eight percent of recorded SHT neurons responded to both innocuous and noxious stimuli (wide dynamic range, WDR) and 39% responded only to noxious stimuli (high threshold, HT). Therefore 87% of SHT neurons responded preferentially or exclusively to noxious mechanical stimulation. Nine percent of SHT neurons responded exclusively to innocuous manipulation of joints and muscles. Four percent of SHT neurons responded only to innocuous tactile stimul (low threshold, LT). WDR, HT, and LT neurons were recorded widely throughout the dorsal horn; no relationship was found between the locations of recording sites in the dorsal horn and the response types of the neurons. SHT neurons that responded to stimulation of muscle, tendon, or joint were recorded deep in the gray matter. 4. The effects of heating the receptive fields were determined for 25 SHT neurons. Fourteen (56%) responded to thermal stimuli. Six (43%) of the responsive neurons responded at low frequencies to innocuous warming (38-41 degrees C) but more vigorously to noxious (greater than or equal to 45 degrees C) heating. The other eight responded only to noxious heat. Eighteen percent (3/17) of tested SHT neurons were activated by noxious cooling of their receptive fields. 5. Cutaneous receptive fields of most recorded SHT neurons were small, typically involving areas as small as two or three toes on the ipsilateral hindlimb; the largest receptive fields covered the entire paw. These findings indicate that relatively precise information about the location of innocuous and noxious stimuli is conveyed directly to the hypothalamus by SHT neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

1989 ◽  
Vol 62 (4) ◽  
pp. 854-863 ◽  
Author(s):  
J. M. Laird ◽  
F. Cervero

1. Single-unit electrical activity has been recorded from 42 dorsal horn neurons in the sacral segments of the rat's spinal cord. The sample consisted of 20 multireceptive (class 2) cells with both A- and C-fiber inputs and 22 nocireceptive (class 3) cells. All neurons had cutaneous receptive fields (RFs) on the tail. 2. The RF sizes of the cells and their response thresholds to mechanical stimulation of the skin were determined before and after each of a series of 2-min noxious mechanical stimuli. Up to five such stimuli were delivered at intervals ranging from 10 to 60 min. In most cases, only one cell per animal was tested. 3. The majority of neurons were tested in barbiturate-anesthetized animals. However, to test whether or not this anesthetic influenced the results obtained, experiments were also performed in halothane-anesthetized and decerebrate-spinal preparations. The results from these experiments are considered separately. 4. All of the neurons responded vigorously to the first noxious pinch stimulus and all but one to the rest of the stimuli in the series. The responses of the neurons varied from stimulus to stimulus, but there were no detectable trends in the two groups of cells. 5. The RFs of the class 2 cells showed large increases (624.3 +/- 175.8 mm2, mean +/- SE) after the application of the pinch stimuli. The RFs of the class 3 neurons, which were initially smaller than those of the class 2 cells, either did not increase in size or showed very small increases after the pinch stimuli (38.3 +/- 11.95 mm2, mean +/- SE). 6. Some cells in both groups (6/10 class 2 cells and 7/16 class 3 cells) showed a decrease in mechanical threshold as a result of the noxious mechanical stimulus, but none of the class 3 cells' thresholds dropped below 20 mN into the low-threshold range. 7. The results obtained in the halothane-anesthetized and decerebrate-spinal animals were very similar to those seen in the barbiturate-anesthetized experiments, with the exception that in the decerebrate-spinal animals, the RFs of the class 2 cells were initially larger and showed only small increases.(ABSTRACT TRUNCATED AT 400 WORDS)


1983 ◽  
Vol 49 (3) ◽  
pp. 649-661 ◽  
Author(s):  
K. D. Kniffki ◽  
K. Mizumura

1. The responses evoked by electrical stimulation of cutaneous and muscle nerves, by noxious and innocuous mechanical stimulation of muscle, tendon, and cutaneous tissues, and by intra-arterial (ia) injection of algesic substances (potassium, bradykinin) into arteries supplying the gastrocnemius-soleus muscle (GS) were studied in single neurons located in the ventroposterolateral nucleus (VPL) and in the transitional zone between VPL and the ventrolateral nucleus (VL) of cats lightly anesthetized with thiopenthal. Such chemical stimulation of the muscles has been shown to activate muscular groups III and IV axons specifically (43, 44) and presumably is nociceptive in character (14, 17, 31). 2. One hundred eight neurons were tested. Eighty-three of the units responded only to various types of cutaneous stimulation of the hindlimb. The other 25 responded to algesic stimulation of muscle and/or tendon. Of these latter 25, 7 had no apparent cutaneous receptive field although 4 of them responded to electrical stimulation of the common peroneal and/or sural nerve. Thus, only three neurons responded exclusively to algesic chemical and noxious mechanical stimulation of the muscle. Of the other 18 neurons, 14 had cutaneous receptive fields restricted to the hindlimb and often responded to non-noxious repetitive light stroking and to noxious pinching with a high-frequency discharge. Four cells (two of which had cutaneous input only from low-threshold mechanoreceptors) had complex and large receptive fields extending to more than one limb. 3. Potassium was a more potent muscle receptor stimulant than bradykinin, the latter only weakly exciting 3 neurons of 24 tested with both substances. The responses to potassium were rapid (approximately 4.0 s in latency) and tended to be greater (have higher response rates) for the units that responded to cutaneous as well as muscle/tendon stimulation. 4. Most neurons that responded to noxious deep stimulation had a threshold for the GS nerve volley in the group III fiber range. The few neurons with thresholds slightly below the group III range did not respond to activation of group I or II muscle spindle afferents by intra-arterial application of succinylcholine or by stretching the muscle. 5. Neurons with responses to any of the muscle, tendon, or cutaneous nociceptive stimuli were located at the ventral and dorsal periphery of VPL and in the VPL-VL transitional zone. 6. These results strongly suggest that there exist regions within the lateral diencephalon of cats that are capable of processing nociceptive information and that these regions are located at the periphery of VPL.


1998 ◽  
Vol 79 (2) ◽  
pp. 964-982 ◽  
Author(s):  
Rami Burstein ◽  
Hiroyoshi Yamamura ◽  
Amy Malick ◽  
Andrew M. Strassman

Burstein, Rami, Hiroyoshi Yamamura, Amy Malick, and Andrew M. Strassman. Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J. Neurophysiol. 79: 964–982, 1998. Chemical activation and sensitization of trigeminal primary afferent neurons innervating the intracranial meninges have been postulated as possible causes of certain headaches. This sensitization, however, cannot explain the extracranial hypersensitivity that often accompanies headache. The goal of this study was to test the hypothesis that chemical activation and sensitization of meningeal sensory neurons can lead to activation and sensitization of central trigeminal neurons that receive convergent input from the dura and skin. This hypothesis was investigated by recording changes in the responsiveness of 23 [16 wide-dynamic range (WDR), 5 high threshold (HT), and 2 low threshold (LT)] dura-sensitive neurons in nucleus caudalis to mechanical stimulation of their dural receptive fields and to mechanical and thermal stimulation of their cutaneous receptive fields after local application of inflammatory mediators or acidic agents to the dura. Responses to brief chemical stimulation were recorded in 70% of the neurons; most were short, lasting the duration of the stimulus only. Twenty minutes after chemical stimulation of the dura, the following changes occurred: 1) 95% of the neurons showed significant increases in sensitivity to mechanical indentation of the dura: their thresholds to dural indentation changed from 1.57 to 0.49 g (means, P < 0.0001), and the response magnitude to identical stimuli increased by two- to fourfold; 2) 80% of the neurons showed significant increases in cutaneous mechanosensitivity: their responses to brush and pressure increased 2.5- ( P < 0.05) and 1.6-fold ( P < 0.05), respectively; 3) 75% of the neurons showed a significant increase in cutaneous thermosensitivity: their thresholds to slow heating of the skin changed from 43.7 ± 0.7 to 40.3 ± 0.7°C ( P < 0.005) and to slow cooling from 23.7 ± 3.3 to 29.2 ± 1.8°C ( P < 0.05); 4) dural receptive fields expanded within 30 min and cutaneous receptive fields within 2–4 h; and 5) ongoing activity developed in WDR and HT but not in LT neurons. Application of lidocaine to the dura abolished the response to dural stimulation but had minimal effect on the increased responses to cutaneous stimulation (suggesting involvement of a central mechanism in maintaining the sensitized state). Antidromic activation (current of <30 μA) of dura-sensitive neurons revealed projections to the hypothalamus, thalamus, and midbrain. These findings suggest that chemical activation and sensitization of dura-sensitive peripheral nociceptors could lead to enhanced responses in central neurons and that this central sensitization therefore could result in extracranial tenderness (mechanical and thermal allodynia) in the absence of extracranial pathology. The projection targets of these neurons suggest a possible role in mediating the autonomic, endocrine, and affective symptoms that accompany headaches.


2002 ◽  
Vol 87 (1) ◽  
pp. 103-112 ◽  
Author(s):  
Volker Neugebauer ◽  
Weidong Li

Pain has a strong emotional dimension, and the amygdala plays a key role in emotionality. The processing of nociceptive mechanical and thermal information was studied in individual neurons of the central nucleus of the amygdala, the target of the spino-parabrachio-amygdaloid pain pathway and a major output nucleus of the amygdala. This study is the first to characterize nociceptive amygdala neurons with input from deep tissue, particularly the knee joint. In 46 anesthetized rats, extracellular single-unit recordings were made from 119 central amygdala neurons that were activated orthodromically by electrical stimulation in the lateral pontine parabrachial area and were tested for receptive fields in the knee joints. Responses to brief mechanical stimulation of joints, muscles, and skin and to cutaneous thermal stimuli were recorded. Receptive-field sizes and thresholds were mapped and stimulus-response functions constructed. Neurons in the central nucleus of the amygdala with excitatory input from the knee joint ( n = 62) typically had large symmetrical receptive fields in both hindlimbs or in all four extremities and responded exclusively or preferentially to noxious mechanical stimulation of deep tissue ( n = 58). Noxious mechanical stimulation of the skin excited 30 of these neurons; noxious heat activated 21 neurons. Stimulus-response data were best fitted by a sigmoid nonlinear regression model rather than by a monotonically increasing linear function. Another 15 neurons were inhibited by noxious mechanical stimulation of the knee joint and other deep tissue. Fifteen neurons had no receptive field in the knee but responded to noxious stimulation of other body areas; 27 nonresponsive neurons were not activated by natural somesthetic stimulation. Our data suggest that excitation is the predominant effect of brief painful stimulation of somatic tissue on the population of central amygdala neurons with knee joint input. Their large symmetrical receptive fields and sigmoid rather than monotonically increasing linear stimulus-response functions suggest a role of nociceptive central amygdala neurons in other than sensory-discriminative aspects of pain.


1988 ◽  
Vol 59 (3) ◽  
pp. 861-885 ◽  
Author(s):  
J. W. Downie ◽  
D. G. Ferrington ◽  
L. S. Sorkin ◽  
W. D. Willis

1. The response properties of neurons of the spinocervicothalamic pathway were studied in anesthetized macaque monkeys. Graded innocuous and noxious mechanical stimuli, including sinusoidal vibration and thermal pulses, were applied to the cutaneous receptive fields. 2. Forty-nine cells in the lateral cervical nucleus (LCN) were identified by antidromic activation from the ventral posterior lateral (VPL) nucleus of the contralateral thalamus. Twelve spinocervical tract (SCT) cells in the lumbosacral enlargement of the spinal cord were identified by antidromic activation from stimulation of the ipsilateral dorsolateral funiculus below C3 but not above C1. 3. Latencies for antidromic activation of LCN neurons averaged 2.3 ms, corresponding to a mean conduction velocity of approximately 17 m/s. Mean latency for orthodromic activation of LCN neurons following electrical stimulation of peripheral nerves was 12.6 ms. Overall mean conduction velocity for the monkey spinocervicothalamic pathway was estimated to be 29 m/s. 4. Most LCN cells had receptive fields on hairy skin, but some had input from glabrous skin and a few had subcutaneous fields. The receptive fields of most SCT cells had a glabrous skin component. Receptive fields tended to be smaller for SCT than LCN cells even for fields on a comparable part of the distal hindlimb. 5. Based on their responses to a series of mechanical stimuli (brushing, pressure, pinch, and squeeze), LCN and SCT cells were classified as low-threshold (LT), wide dynamic range (WDR), or high-threshold (HT) neurons. Most of the cells were in the LT or WDR classes. Thus the spinocervicothalamic pathway in the monkey differs from the spinothalamic tract (STT), in that STT cells are generally of the WDR or HT classes. 6. With the use of discriminant analysis, LCN and SCT neurons were allocated to categories determined from a k-means cluster analysis of the responses of 318 STT cells. The LCN and SCT neurons were in different proportions in the various categories than were STT cells, suggesting differences in the signaling properties of the spinocervicothalamic and spinothalamic paths. 7. Innocuous steady indentation of the skin failed to excite any of the neurons tested. Thus no positive evidence was obtained for an input to LCN neurons from slowly adapting mechanoreceptors. 8. Sinusoidal vibratory stimuli were used to test the ability of LCN and SCT neurons to follow repeated innocuous mechanical stimuli. Vibration at 10 Hz and an amplitude of 100 micron resulted in repetitive discharges in most LCN neurons and half the SCT neurons tested; many LCN neurons had thresholds below 25 micron.(ABSTRACT TRUNCATED AT 400 WORDS)


1996 ◽  
Vol 75 (6) ◽  
pp. 2581-2605 ◽  
Author(s):  
J. T. Katter ◽  
R. J. Dado ◽  
E. Kostarczyk ◽  
G. J. Giesler

1. A goal of this study was to determine the sites in the diencephalon to which neurons in sacral spinal segments of rats project. Therefore, 95 neurons were recorded extracellularly in spinal segments L6-S2 of rats that were anesthetized with urethan. These neurons were activated initially antidromically with currents < or = 30 microA from a monopolar stimulating electrode placed into the contralateral posterior diencephalon. The mean +/- SE current for antidromic activation from these sites was 16 +/- 0.8 microA. These neurons were recorded in the superficial dorsal horn (4%), deep dorsal horn (89%), and intermediate zone and ventral horn (4%). 2. Systematic antidromic mapping techniques were used to map the axonal projections of 41 of these neurons within the diencephalon. Thirty-three neurons (80%) could be activated antidromically with currents < or = 30 microA only from points in the contralateral thalamus and are referred to as spinothalamic tract (STT) neurons. Eight neurons (20%) were activated antidromically with low currents from points in both the contralateral thalamus and hypothalamus, and these neurons are referred to as spinothalamic tract/ spinohypothalamic tract (STT/SHT) neurons. Three additional neurons were activated antidromically with currents < or = 30 microA only from points within the contralateral hypothalamus and are referred to as spinohypothalamic tract (SHT) neurons. The diencephalic projections of another 51 neurons were mapped incompletely. These neurons are referred to as spinothalamic/unknown (STT/ U) neurons to indicate that it was not known whether their axons ascended beyond the site in the thalamus from which they initially were activated antidromically. 3. For 31 STT neurons, the most anterior point at which antidromic activation was achieved with currents < or = 30 microA was determined. Fourteen (45%) were activated antidromically only from sites posterior to the ventrobasal complex (VbC) of the thalamus. Sixteen STT neurons (52%) were activated antidromically with low currents from sites at the level of the VbC, but not from more anterior levels. One STT neuron (3%) was activated antidromically from the anteroventral nucleus of the thalamus. 4. STT/SHT neurons were antidromically activated with currents < or = 30 microA from the medial lemniscus (ML), anterior pretectal nucleus (APt), posterior nuclear group and medial geniculate nucleus (Po/MG), and zona incerta in the thalamus and from the optic tract (OT), supraoptic decussation, or lateral area of the hypothalamus. No differences in the sites in the thalamus from which STT and STT/SHT neurons were activated antidromically were apparent. Five STT/SHT neurons (62%) were activated antidromically from points in the thalamus in the posterior diencephalon and from points in the hypothalamus at more anterior levels. Three STT/SHT neurons (38%) were activated antidromically with currents < or = 30 microA from sites in both the thalamus and hypothalamus at the same anterior-posterior level of the diencephalon. All three of these STT/SHT neurons projected to the intralaminar nuclei (parafascicular or central lateral nuclei) of the thalamus. 5. Seven STT/SHT neurons were tested for additional projections to the ipsilateral brain. Two (29%) were activated antidromically with currents < or = 30 microA and at longer latencies from sites in the ipsilateral diencephalon. One could only be activated antidromically from the hypothalamus ipsilaterally. The other was activated antidromically at progressively increasing latencies from points in the ipsilateral brain that extended as far posteriorly as the posterior pole of the MG. 6. Fifty-eight STT, STT/SHT, and STT/U neurons were classified as low-threshold (LT), wide dynamic range (WDR), or highthreshold (HT) neurons based on their responsiveness to innocuous and noxious mechanical stimuli applied to their cutaneous receptive fields.(ABSTRACT TRUNCATED)


1999 ◽  
Vol 82 (2) ◽  
pp. 1054-1058 ◽  
Author(s):  
X. Zhang ◽  
H. N. Wenk ◽  
A. P. Gokin ◽  
C. N. Honda ◽  
G. J. Giesler

Recent anatomic results indicate that a large direct projection from the spinal cord to the hypothalamus exists in monkeys. The aim of this study was to determine whether the existence of this projection could be confirmed unambiguously using electrophysiological methods and, if so, to determine the response characteristics of primate spinohypothalamic tract (SHT) neurons. Fifteen neurons in the lumbar enlargement of macaque monkeys were antidromically activated using low-amplitude current pulses in the contralateral hypothalamus. The points at which antidromic activation thresholds were lowest were found in the supraoptic decussation ( n = 13) or in the medial hypothalamus ( n = 2). Recording points were located in the superficial dorsal horn ( n = 1), deep dorsal horn ( n = 10), and intermediate zone ( n = 4). Each of the 12 examined neurons had cutaneous receptive fields on the ipsilateral hindlimb. All neurons responded exclusively or preferentially to noxious stimuli, suggesting that the transmission of nociceptive information is an important role of primate SHT axons. Twelve SHT neurons were also antidromically activated from the thalamus. In all cases, the antidromic latency from the thalamus was shorter than that from the hypothalamus, suggesting that the axons pass through the thalamus then enter the hypothalamus. These results confirm the existence of a SHT in primates and suggest that this projection may contribute to the production of autonomic, neuroendocrine, and emotional responses to noxious stimuli in primates, possibly including humans.


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)


1994 ◽  
Vol 71 (3) ◽  
pp. 981-1002 ◽  
Author(s):  
R. J. Dado ◽  
J. T. Katter ◽  
G. J. Giesler

1. The goal of this study was to gather data that would increase our understanding of nociceptive processing by spinothalamic tract (STT) neurons that receive inputs from the hand and arm. Fifty neurons in the cervical enlargement of urethan-anesthetized rats were antidromically activated from the contralateral posterior thalamus. A stimulating electrode was moved systematically within an anterior-posterior plane in the thalamus until a point was located where the smallest amount of current antidromically activated the neuron. The antidromic thresholds at each of these lowest threshold points was < or = 30 microA; the mean antidromic threshold was 15.4 +/- 1.0 (SE) microA. Lowest threshold points were found primarily in the posterior thalamic group (Po), zona incerta, and in or near the supraoptic decussation. 2. The recording sites of 47 neurons were marked and recovered. Recording sites were located in the superficial dorsal horn (SDH, n = 15), deep dorsal horn (DDH, n = 31), and ventral horn (n = 1). Recording sites were located across the mediolateral extent of the SDH. Within the DDH, recording sites were concentrated laterally in nucleus proprius and dorsally in the lateral reticulated area. The locations of the recording points confirm previous anatomic descriptions of STT neurons in the cervical enlargement. 3. Cutaneous excitatory receptive fields were restricted to the ipsilateral forepaw or forelimb in 67% (10/15) of the neurons recorded in the SDH and 42% (13/31) of the neurons recorded in the DDH. Neurons having larger, more complex receptive fields were also commonly encountered. Thirty-three percent (5/15) of the neurons recorded in the SDH and 58% (18/31) recorded in the DDH had receptive fields that were often discontinuous and included areas of the ipsilateral shoulder, thorax, and head, including the face. 4. Innocuous and noxious mechanical stimuli were applied to the receptive field of each neuron. Fifty percent (25/50) responded to innocuous mechanical stimuli but responded at higher frequencies to noxious stimuli (wide dynamic range, WDR). Forty-four percent (22/50) responded only to noxious stimuli (high threshold, HT). Six percent (3/50) responded preferentially to innocuous stimuli (low threshold, LT). WDR and HT neurons were recorded in both the SDH and DDH, including nucleus proprius, an area not typically associated with nociceptive transmission at other levels of the cord. Sixty percent (9/15) of the units recorded in the SDH were classified as WDR neurons; the other 40% (6/15) were classified HT. Forty-eight percent (15/31) of the units recorded in the DDH were classified as WDR neurons and 42% (13/31) as HT.(ABSTRACT TRUNCATED AT 400 WORDS)


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