Response Characterstics of Spinothalamic Tract Neurons That Project to the Posterior Thalamus in Rats

2005 ◽  
Vol 93 (5) ◽  
pp. 2552-2564 ◽  
Author(s):  
Xijing Zhang ◽  
Glenn J. Giesler

A sizeable number of spinothalamic tract axons terminate in the posterior thalamus. The functional roles and precise areas of termination of these axons have been a subject of recent controversy. The goals of this study were to identify spinothalamic tract neurons (STT) within the cervical enlargement that project to this area, characterize their responses to mechanical and thermal stimulation of their receptive fields, and use microantidromic tracking methods to determine the nuclei in which their axons terminate. Forty-seven neurons were antidromically activated using low-amplitude (≤30 μA) current pulses in the contralateral posterior thalamus. The 51 points at which antidromic activation thresholds were lowest were surrounded by ineffective tracks indicating that the surrounded axons terminated within the posterior thalamus. The areas of termination were located primarily in the posterior triangular, medial geniculate, posterior and posterior intralaminar, and suprageniculate nuclei. Recording points were located in the superficial and deep dorsal horn. The mean antidromic conduction velocity was 6.4 m/s, a conduction velocity slower than that of other projections to the thalamus or hypothalamus in rats. Cutaneous receptive fields appeared to be smaller than those of neurons projecting to other areas of the thalamus or to the hypothalamus. Each of the examined neurons responded exclusively or preferentially to noxious stimuli. These findings indicate that the STT carries nociceptive information to several target nuclei within the posterior thalamus. We discuss the evidence that this projection provides nociceptive information that plays an important role in fear conditioning.

2008 ◽  
Vol 100 (4) ◽  
pp. 2026-2037 ◽  
Author(s):  
Steve Davidson ◽  
Xijing Zhang ◽  
Sergey G. Khasabov ◽  
Donald A. Simone ◽  
Glenn J. Giesler

The primate posterior thalamus has been proposed to contribute to pain sensation, but its precise role is unclear. This is in part because spinothalamic tract (STT) neurons that project to the posterior thalamus have received little attention. In this study, antidromic mapping was used to identify individual STT neurons with axons that projected specifically to the posterior thalamus in Macaca fascicularis. Each axon was located by antidromic activation at low stimulus amplitudes (<30 μA) and was then surrounded distally by a grid of stimulating points in which 500-μA stimuli were unable to activate the axon antidromically, thereby indicating the termination zone. Several nuclei within the posterior thalamus were targets of STT neurons: the posterior nucleus, suprageniculate nucleus, magnocellular part of the medial geniculate nucleus, and limitans nucleus. STT neurons projecting to the ventral posterior inferior nucleus were also studied. Twenty-five posterior thalamus-projecting STT neurons recorded in lumbar spinal cord were characterized by their responses to mechanical, thermal, and chemical stimuli. Sixteen of 25 neurons were recorded in the marginal zone and the balance was located within the deep dorsal horn. Thirteen neurons were classified as wide dynamic range and 12 as high threshold. One-third of STT neurons projecting to posterior thalamus responded to noxious heat (50°C). Two-thirds of those tested responded to cooling. Seventy-one percent responded to an intradermal injection of capsaicin. These data indicate that the primate STT transmits noxious and innocuous mechanical, thermal, and chemical information to multiple posterior thalamic nuclei.


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)


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.


1988 ◽  
Vol 59 (3) ◽  
pp. 886-907 ◽  
Author(s):  
D. G. Ferrington ◽  
J. W. Downie ◽  
W. D. Willis

1. Recordings were made from 67 neurons in the nucleus gracilis (NG) of anesthetized macaque monkeys. All of the cells were activated antidromically from the ventral posterior lateral (VPL) nucleus of the contralateral thalamus. Stimuli used to activate the cells orthodromically were graded innocuous and noxious mechanical stimuli, including sinusoidal vibration and thermal pulses. 2. The latencies of antidromic action potentials following stimulation in the VPL nucleus were significantly shorter for cells in the caudal compared with the rostral NG. The mean minimum afferent conduction velocity of the afferent conduction velocity of the afferent fibers exciting the NG cells was 52 m/s, as judged from the latencies of the cells to orthodromic volleys evoked by electrical stimulation of peripheral nerves. The overall conduction velocity of the pathway from peripheral nerve to thalamus was approximately 40 m/s. 3. Cutaneous receptive fields on the distal hindlimb usually occupied an area equivalent to much less than a single digit. However, a few cells had receptive fields up to or exceeding the area of the foot. 4. NG cells were classified by their responses to graded mechanical stimulation of the skin as low threshold (LT) or wide dynamic range (WDR). No high-threshold NG cells were found. A special subcategory of pressure-sensitive LT (SA) neurons was recognized. Many of these cells were maximally responsive to maintained indentation of the skin. The sample of NG cells differed from the population of primate spinothalamic and spinocervicothalamic pathways so far examined, in having a larger proportion of LT neurons and a smaller proportion of WDR cells. A few NG cells responded best to manipulation of subcutaneous tissue. 5. Discriminant analysis permitted the NG cells to be assigned to classes determined by a k-means cluster analysis of the responses of a reference set of 318 primate spinothalamic tract (STT) cells. There were four classes of cells based on normalized responses of individual neurons and another four classes based upon responses compared across the population of cells. The NG cells were allocated to the various categories in different proportions than either primate STT cells or spinocervicothalamic neurons, consistent with the view that the functional roles of these somatosensory pathways differ. 6. Some of the pressure-sensitive NG cells were excited when the skin was stretched, suggesting an input from type II slowly adapting (Ruffini) mechanoreceptors.(ABSTRACT TRUNCATED AT 400 WORDS)


1997 ◽  
Vol 77 (1) ◽  
pp. 435-451 ◽  
Author(s):  
Ewa Kostarczyk ◽  
Xijing Zhang ◽  
Glenn J. Giesler

Kostarczyk, Ewa, Xijing Zhang, and Glenn J. Giesler, Jr. Spinohypothalamic tract neurons in the cervical enlargement of rats: locations of antidromically identified ascending axons and their collateral branches in the contralateral brain. J. Neurophysiol. 77: 435–451, 1997. Antidromic activation was used to determine the locations of ascending spinohypothalamic tract (SHT) axons and their collateral projections within C1, medulla, pons, midbrain, and caudal thalamus. Sixty-four neurons in the cervical enlargement were antidromically activated initially by stimulation within the contralateral hypothalamus. All but one of the examined SHT neurons responded either preferentially or specifically to noxious mechanical stimuli. A total of 239 low-threshold points was classified as originating from 64 ascending (or parent) SHT axons. Within C1, 38 ascending SHT axons were antidromically activated. These were located primarily in the dorsal half of the lateral funiculus. Within the medulla, the 29 examined ascending SHT axons were located ventrolaterally, within or adjacent to the lateral reticular nucleus or nucleus ambiguus. Within the pons, the 25 examined ascending SHT axons were located primarily surrounding the facial nucleus and the superior olivary complex. Within the caudal midbrain, the 23 examined SHT ascending axons coursed dorsally in a position adjacent to the lateral lemniscus. Within the anterior midbrain, SHT axons traveled rostrally near the brachium of the inferior colliculus. Within the posterior thalamus, all 17 examined SHT axons coursed rostrally through the posterior nucleus of thalamus. A total of 114 low-threshold points was classified as collateral branch points. Sixteen collateral branches were seen in C1; these were located primarily in the deep dorsal horn. Forty-five collateral branches were located in the medulla. These were primarily in or near the medullary reticular nucleus, nucleus ambiguus, lateral reticular nucleus, parvocellular reticular nucleus, gigantocellular reticular nucleus, cuneate nucleus, and the nucleus of the solitary tract. Twenty-six collateral branches from SHT axons were located in the pons. These were in the pontine reticular nucleus caudalis, gigantocellular reticular nucleus, parvocellular reticular nucleus, and superior olivary complex. Twenty-three collateral branches were located in the midbrain. These were in or near the mesencephalic reticular nucleus, brachium of the inferior colliculus, cuneiform nucleus, superior colliculus, central gray, and substantia nigra. In the caudal thalamus, two branches were in the posterior thalamic nucleus and two were in the medial geniculate. These results indicate that SHT axons ascend toward the hypothalamus in a clearly circumscribed projection in the lateral brain stem and posterior thalamus. In addition, large numbers of collaterals from SHT axons appear to project to a variety of targets in C1, the medulla, pons, midbrain, and caudal thalamus. Through its widespread collateral projections, the SHT appears to be capable of providing nociceptive input to many areas that are involved in the production of multifaceted responses to noxious stimuli.


1987 ◽  
Vol 58 (3) ◽  
pp. 480-495 ◽  
Author(s):  
W. S. Ammons

Spinoreticular (SRT) and spinothalamic (STT) neurons were studied for responses to renal and somatic stimuli in 34 cats that were anesthetized with alpha-chloralose. SRT cells were antidromically activated from the medial medullary reticular formation near the gigantocellular tegmental field contralateral (35 cells), ipsilateral (15 cells), or both contralateral and ipsilateral (11 cells) to the recording site. Collision tests showed that activation from two electrodes resulted from stimulation of separate axonal branches and not from current spread. Twenty STT cells were activated from the spinothalamic tract just medial to the medial geniculate nucleus. SRT cells were located in laminae I, V, VII, and VIII of the T12-L2 segments. Most cells were located in lamina VII. STT cells were found in laminae I, V, and VII. The axons of 12 SRT cells were located in the ventrolateral or ventral quadrants of the upper cervical spinal cord. Antidromic conduction velocities of SRT cells averaged 48.7 +/- 3.7 m/s. No differences in conduction velocity were found between cells projecting to different reticular sites. In addition conduction velocity did not vary with the type of somatic or renal input. Antidromic conduction velocities of STT cells averaged 46.4 +/- 4.7 m/s. Renal nerve stimulation excited 58 and inhibited 3 SRT cells. All 20 STT cells were excited. Thirty SRT cells were excited only by A-delta input, 26 received both A-delta- and C-fiber inputs, and 2 cells received only C-fiber input. Ten STT cells received A-delta input only and 10 received both A-delta- and C-fiber inputs. All cells with renal input also received somatic input. Thirty-six SRT cells (59%) were classified as high threshold, 12 (20%) as wide dynamic range, and 10 (16%) as deep. Ten STT cells were classified as high threshold and 10 as wide dynamic range. Somatic receptive fields of STT cells were usually simple and invariably included the left flank region, although many of the fields extended to the left hindlimb or abdomen. Eighteen of the 20 were restricted to the ipsilateral side. In contrast, somatic receptive fields of SRT cells were primarily bilateral (71%). While all but two receptive fields included the left flank area, most extended to one or both hindlimbs, the abdomen, or the right flank. Inhibitory receptive fields were found for 33% of the SRT cells and 20% of the STT cells.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 71 (3) ◽  
pp. 959-980 ◽  
Author(s):  
R. J. Dado ◽  
J. T. Katter ◽  
G. J. Giesler

1. Seventy-seven neurons in the cervical enlargement of rats anesthetized with urethan were initially antidromically activated using currents < or = 30 microA from the contralateral posterior thalamus. A goal of these experiments was to determine the course of physiologically characterized spinal axons within the diencephalon. Therefore, in 38 cases, additional antidromic mapping was done throughout the mediolateral extent of the diencephalon at multiple anterior-posterior planes. 2. Electrolytic lesions marking the recording sites were recovered for 71 neurons. Thirty-one were located in the superficial dorsal horn (SDH); 39 were in nucleus proprius or the lateral reticulated area of the deep dorsal horn (DDH), and one was in the ventral horn. 3. Eight of 38 (21%) neurons that were tested for more anterior projections could only be antidromically activated with currents < or = 30 microA from sites in the contralateral posterior thalamus. Such neurons are referred to as spinothalamic tract (STT) neurons. Lesions marking the lowest threshold points for antidromic activation were located in or near the posterior thalamic group (Po). At more anterior levels, considerably higher currents were required for antidromic activation or it was not possible to activate the neurons with currents up to 500 microA. Four of these neurons were physiologically characterized and each responded preferentially to noxious mechanical stimuli (wide dynamic range, WDR). Each of the three neurons that were tested responded to noxious heat stimuli. These findings confirm anatomic studies that have shown that a number of STT axons terminate in Po and suggest that such axons that originate in the cervical enlargement carry nociceptive input from the upper extremity. 4. In 15 cases, electrode penetrations were made systematically throughout much of the contralateral ventrobasal complex (VbC). In 17 cases, penetrations were made throughout the intralaminar nuclei contralaterally, including the central lateral nucleus (CL). Surprisingly, only one of the examined axons was antidromically activated with low currents from CL and one from VbC, although both of these nuclei are known to receive sizeable inputs from the STT. 5. Many of the axons (27 of the 38 tested, 71%) that were initially antidromically activated from the contralateral posterior thalamus could also be antidromically activated with low currents (< or = 30 microA) and at increased latencies from sites located anteriorly in the contralateral hypothalamus. Such neurons are referred to as spinothalamic tract/spinohypothalamic tract (STT/SHT) neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


1980 ◽  
Vol 44 (5) ◽  
pp. 862-877 ◽  
Author(s):  
D. Menetrey ◽  
A. Chaouch ◽  
J. M. Besson

1. Spinoreticular tract neurons at the rat lumbar cord level were identified by antidromic activation following stimulation at mainly pontine and mesencephalic levels. These units, which were found in the dorsal half of the cord, could be separated into two groups according to their spinal location, electrophysiological properties, and their central projections. 2. Units in the dorsolateral funiculus nucleus projected mainly to the cuneiformis area and adjacent structures with frequent bilateral projections. They had the slowest conduction velocities, sometimes in the unmyelinated range. Generally, they were driven only by stimulation of subcutaneous and/or deep structures. 3. Neurons located in the dorsal horn mainly projected contralaterally to pontine and mesencephalic levels. their conduction velocities and the electrophysiological properties were identical to those observed for the rat spinothalamic tract (22). Almost all (86%) had clear cutaneous sensitivity and generally large receptive fields: 40% responded to nonnoxious and noxious mechanical cutaneous stimuli and frequently to noxious radiant heat, 26% were exclusively excited by light tactile stimuli, and 20% required noxious cutaneous mechanical stimulation for activation. There was a good correlation between responses to natural and transcutaneous electrical stimulation: units driven by noxious mechanical stimuli received A-delta- and/or C-fiber inputs. The remaining units (14%) had more complex receptive fields associated with both excitatory and inhibitory inputs originating from a single peripheral area. 4. The functional heterogeneity of the rat spinoreticular tract is reminiscent of that demonstrated for the rat and monkey spinothalamic tracts. Similarly, the rat spinoreticular neurons are under the influence of descending inhibitory controls originating from the nucleus raphe magnus and bulbar reticular formation. 5. Responses of the rat spinoreticular tract neurons are consistent with the involvement of this pathway in the transmission of messages of both innocuous and noxious origins.


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)


1996 ◽  
Vol 76 (4) ◽  
pp. 2661-2674 ◽  
Author(s):  
E. D. Al-Chaer ◽  
N. B. Lawand ◽  
K. N. Westlund ◽  
W. D. Willis

1. Extracellular recordings were made from single neurons in the ventral posterolateral (VPL) nucleus of the thalamus in anesthetized male rats. VPL cells that responded to colorectal distension (CRD) were further tested with cutaneous and visceral stimuli before and after sequential lesions of the dorsal column (DC) and of the ventrolateral column (VLC). 2. A total of 105 VPL viscerosensitive cells was isolated. In this study, we report results from 27 cells that were tested for visceral responses before and after lesions of the DC and the VLC. 3. Ten VPL cells, isolated in 10 different rats, that responded to CRD and to activation of their cutaneous receptive fields with innocuous and noxious stimuli were tested before and after a lesion of the DC and again after a lesion of the VLC. Ten other VPL cells were isolated in 10 different rats. These were also tested for responses to CRD and to cutaneous stimuli spanning the innocuous and the noxious range before and after a lesion of the VLC and again after a lesion of the DC. 4. A lesion of the DC dramatically reduced the responses of VPL cells to CRD as well as to innocuous cutaneous stimuli. A lesion of the VLC reduced and sometimes abolished the responses of VPL cells to noxious cutaneous stimuli; however, its effect on the responses to visceral or innocuous cutaneous stimuli was minor when compared with that of a DC lesion. 5. The activity of seven VPL cells that responded to CRD and to cutaneous stimuli was observed after an injection of a chemical irritant, mustard oil (MO), into the colon. These cells showed an increase in background activity that started approximately 25-30 min after the MO injection. A lesion of the DC reduced the background activity of the cells to levels near initial values. 6. We conclude that the DC in the rat contains a pathway that is more important for transmitting visceral nociceptive signals to the VPL nucleus than are pathways in the VLC, including the spinothalamic tract. Conversely, the VLC is more important for transmitting nociceptive information of cutaneous origin.


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