scholarly journals A Role For Wind-Up in Trigeminal Sensory Processing: Intensity Coding of Nociceptive Stimuli in the Rat

Cephalalgia ◽  
2008 ◽  
Vol 28 (6) ◽  
pp. 631-639 ◽  
Author(s):  
J Coste ◽  
DL Voisin ◽  
P Luccarini ◽  
R Dallel
Keyword(s):  
Sensory Processing ◽  
Time Course ◽  
Dynamic Range ◽  
Physiological Role ◽  
Repetitive Stimulation ◽  
Evoked Responses ◽  
Frequency Dependent ◽  
Nociceptive Neurons ◽  
C Fibre ◽  
Wdr Neurons

Wind-up is a progressive, frequency-dependent increase in the excitability of trigeminal and spinal dorsal horn wide dynamic range (WDR) nociceptive neurons evoked by repetitive stimulation of primary afferent nociceptive C-fibres. The correlate of wind-up in humans is temporal summation, which is an increase in pain perception to repetitive constant nociceptive stimulation. Although wind-up is widely used as a tool for studying the processing of nociceptive information, including central sensitization, its actual role is still unknown. Here, we recorded from trigeminal WDR neurons using in vivo electrophysiological techniques in rats and assessed the wind-up phenomenon in response to stimuli of different intensities and frequencies. First, we found that the amplitude of C-evoked responses of WDR neurons to repetitive stimulation increased progressively to reach a peak, then consistently showed a stable or slightly decreasing plateau phase. Only the first phase of this time course fitted in with the wind-up description. Therefore, to assess wind-up, we measured a limited number of initial responses. Second, we showed that wind-up, i.e. the slope of the frequency-dependent increase in the response to C-fibre stimulation, was linearly correlated to the stimulus intensity. Intensities of brief C-fibre inputs were thus coded into frequencies of action potentials by second-order neurons through frequency-dependent potentiation of the evoked responses. Third, wind-up also occurred at stimulation intensities below the threshold for C-evoked responses in WDR neurons, suggesting that wind-up can amplify subthreshold C-fibre inputs to WDR neurons. This might account for the observation that sparse, subliminal, neuronal activity in nociceptors can become painful via central integration of neural responses. Altogether, the present results show that wind-up can provide trigeminal WDR neurons with the capability to encode the intensity of short-duration orofacial nociceptive stimuli and to detect subthreshold nociceptive input. Thus, not only may wind-up play a physiological role in trigeminal sensory processing, but its enhancement may also underlie the pathophysiology of chronic orofacial pain conditions.

α2-Adrenoceptors Modulate NMDA-Evoked Responses of Neurons in Superficial and Deeper Dorsal Horn of the Medulla

1998 ◽  
Vol 80 (4) ◽  
pp. 2210-2214 ◽  
Author(s):  
Kai-Ming Zhang ◽  
Xiao-Min Wang ◽  
Angela M. Peterson ◽  
Wen-Yan Chen ◽  
Sukhbir S. Mokha
Keyword(s):  
Dorsal Horn ◽  
Dynamic Range ◽  
Inhibitory Effect ◽  
Male Rats ◽  
Evoked Responses ◽  
Superficial Dorsal Horn ◽  
Nociceptive Neurons ◽  
Adrenoceptor Antagonist ◽  
Medullary Dorsal Horn ◽  
Wdr Neurons

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.

Activation of Spinal Wide Dynamic Range Neurons by Intracutaneous Microinjection of Nicotine

1999 ◽  
Vol 82 (6) ◽  
pp. 3046-3055 ◽  
Author(s):  
Steven L. Jinks ◽  
E. Carstens
Keyword(s):  
Nicotinic Acetylcholine Receptors ◽  
Acetylcholine Receptors ◽  
Dynamic Range ◽  
Receptive Fields ◽  
Threshold Region ◽  
Partial Recovery ◽  
Evoked Responses ◽  
Wide Dynamic Range ◽  
Analgesic Effects ◽  
Wdr Neurons

Nicotine evokes pain in the skin and oral mucosa and excites a subpopulation of cutaneous nociceptors, but little is known about the central transmission of chemogenic pain. We have investigated the responses of lumbar spinal wide dynamic range (WDR)-type dorsal horn neurons to intracutaneous (ic) microinjection of nicotine in pentobarbital-anesthetized rats. Nearly all (97%) units responded to nicotine microinjected ic (1 μl) into the low-threshold region of the hind-paw mechanosensitive receptive field in a concentration-related manner (0.01–10%). Responses to repeated injections of 10% nicotine exhibited tachyphylaxis at 5-, 10-, and 15-min interstimulus intervals. Significant tachyphylaxis was not seen with 1% nicotine. All nicotine-responsive units tested ( n = 30) also responded to ic histamine (1 μl, 3%) and did not exhibit tachyphylaxis to repeated histamine. However, there was significant cross-tachyphylaxis of nicotine to histamine. Thus 5 min after ic nicotine, histamine-evoked responses were attenuated significantly compared with the initial histamine-evoked response prior to nicotine, with partial recovery over the ensuing 15 min. Neuronal excitation by ic nicotine was not mediated by histamine H1 receptors because ic injection of the H1 receptor antagonist, cetirizine, had no effect on ic nicotine-evoked responses, whereas it significantly attenuated ic histamine-evoked responses in the same neurons. The lowest-threshold portion of cutaneous receptive fields showed a significant expansion in area at 20 min after ic nicotine 10%, indicative of sensitization. Responses to 1% nicotine were significantly reduced after ic injection of the nicotinic antagonist, mecamylamine (0.1% ic), with no recovery over the ensuing 40–60 min. These data indicate that nicotine ic excites spinal WDR neurons, partly via neuronal nicotinic acetylcholine receptors that are presumably expressed in cutaneous nociceptor terminals. Repeated injections of high concentrations of nicotine led to tachyphylaxis and cross-tachyphylaxis with histamine, possibly relevant to peripheral analgesic effects of nicotine.

Response Properties and Organization of Nociceptive Neurons in Area 1 of Monkey Primary Somatosensory Cortex

2000 ◽  
Vol 84 (2) ◽  
pp. 719-729 ◽  
Author(s):  
Dan R. Kenshalo ◽  
Koichi Iwata ◽  
Maurice Sholas ◽  
David A. Thomas
Keyword(s):  
Somatosensory Cortex ◽  
Dynamic Range ◽  
Receptive Fields ◽  
Primary Somatosensory Cortex ◽  
Isolated Cells ◽  
Nociceptive Neurons ◽  
Response Properties ◽  
Stimulus Response ◽  
Noxious Mechanical Stimulation ◽  
Wdr Neurons

The organization and response properties of nociceptive neurons in area 1 of the primary somatosensory cortex (SI) of anesthetized monkeys were examined. The receptive fields of nociceptive neurons were classified as either wide-dynamic-range (WDR) neurons that were preferentially responsive to noxious mechanical stimulation, or nociceptive specific (NS) that were responsive to only noxious stimuli. The cortical locations and the responses of the two classes of neurons were compared. An examination of the neuronal stimulus-response functions obtained during noxious thermal stimulation of the glabrous skin of the foot or the hand indicated that WDR neurons exhibited significantly greater sensitivity to noxious thermal stimuli than did NS neurons. The receptive fields of WDR neurons were significantly larger than the receptive fields of NS neurons. Nociceptive SI neurons were somatotopically organized. Nociceptive neurons with receptive fields on the foot were located more medial in area 1 of SI than those with receptive fields on the hand. In the foot representation, the recording sites of nociceptive neurons were near the boundary between areas 3b and 1, whereas in the hand area, there was a tendency for them to be located more caudal in area 1. The majority of nociceptive neurons were located in the middle layers (III and IV) of area 1. The fact that nociceptive neurons were not evenly distributed across the layers of area 1 suggested that columns of nociceptive neurons probably do not exist in the somatosensory cortex. In electrode tracks where nociceptive neurons were found, approximately half of all subsequently isolated neurons were also classified as nociceptive. Low-threshold mechanoreceptive (LTM) neurons were intermingled with nociceptive neurons. Both WDR and NS neurons were found in close proximity to one another. In instances where the receptive field shifted, subsequently isolated cells were also classified as nociceptive. These data suggest that nociceptive neurons in area 1 of SI are organized in vertically orientated aggregations or clusters in layers III and IV.

Responses of monkey medullary dorsal horn neurons during the detection of noxious heat stimuli

1989 ◽  
Vol 62 (2) ◽  
pp. 437-449 ◽  
Author(s):  
W. Maixner ◽  
R. Dubner ◽  
D. R. Kenshalo ◽  
M. C. Bushnell ◽  
J. L. Oliveras
Keyword(s):  
Dorsal Horn ◽  
Stimulus Intensity ◽  
Dynamic Range ◽  
Thermal Stimulus ◽  
Mechanical Stimuli ◽  
Behavioral Task ◽  
Noxious Heat ◽  
Nociceptive Neurons ◽  
Medullary Dorsal Horn ◽  
Wdr Neurons

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.

scholarly journals Hair-Cell Versus Afferent Adaptation in the Semicircular Canals

2005 ◽  
Vol 93 (1) ◽  
pp. 424-436 ◽  
Author(s):  
R. D. Rabbitt ◽  
R. Boyle ◽  
G. R. Holstein ◽  
S. M. Highstein
Keyword(s):  
Hair Cell ◽  
Hair Cells ◽  
Semicircular Canal ◽  
Time Course ◽  
Dynamic Range ◽  
Cell Voltage ◽  
Frequency Dependent ◽  
Adaptation Time ◽  
Phase Lead ◽  
Flat Gain

The time course and extent of adaptation in semicircular canal hair cells was compared to adaptation in primary afferent neurons for physiological stimuli in vivo to study the origins of the neural code transmitted to the brain. The oyster toadfish, Opsanus tau, was used as the experimental model. Afferent firing-rate adaptation followed a double-exponential time course in response to step cupula displacements. The dominant adaptation time constant varied considerably among afferent fibers and spanned six orders of magnitude for the population (∼1 ms to >1,000 s). For sinusoidal stimuli (0.1–20 Hz), the rapidly adapting afferents exhibited a 90° phase lead and frequency-dependent gain, whereas slowly adapting afferents exhibited a flat gain and no phase lead. Hair-cell voltage and current modulations were similar to the slowly adapting afferents and exhibited a relatively flat gain with very little phase lead over the physiological bandwidth and dynamic range tested. Semicircular canal microphonics also showed responses consistent with the slowly adapting subset of afferents and with hair cells. The relatively broad diversity of afferent adaptation time constants and frequency-dependent discharge modulations relative to hair-cell voltage implicate a subsequent site of adaptation that plays a major role in further shaping the temporal characteristics of semicircular canal afferent neural signals.

scholarly journals Effects of a Cannabinoid Agonist on Spinal Nociceptive Neurons in a Rodent Model of Neuropathic Pain

2006 ◽  
Vol 96 (6) ◽  
pp. 2984-2994 ◽  
Author(s):  
Cheng Liu ◽  
J. Michael Walker
Keyword(s):  
Neuropathic Pain ◽  
Receptive Field ◽  
Nerve Injury ◽  
Dynamic Range ◽  
Rodent Model ◽  
Field Size ◽  
Neural Basis ◽  
Noxious Heat ◽  
Nociceptive Neurons ◽  
Wdr Neurons

The effects of the synthetic cannabinoid WIN 55,212–2 on heat-evoked firing of spinal wide dynamic range (WDR) neurons were examined in a rodent model of neuropathic pain. Fifty-eight WDR neurons (1 cell/animal) were recorded from the ipsilateral spinal dorsal horns of rats with chronic constriction injury (CCI) and sham-operated controls. Relative to sham-operated controls, neurons recorded in CCI rats showed elevations in spontaneous firing, noxious heat-evoked responses, and afterdischarge firing as well as increases in receptive field size. WIN 55,212–2 (0.0625, 0.125, and 0.25 mg/kg, intravenous) dose-dependently suppressed heat-evoked activity and decreased the receptive field areas of dorsal horn WDR neurons in both nerve injured and control rats with a greater inhibition in CCI rats. At the dose of 0.125 mg/kg iv, WIN 55,212–2 reversed the hyperalgesia produced by nerve injury. The effect of intravenous administration of WIN 55,212–2 appears to be centrally mediated because administration of the drug directly to the ligated nerve did not suppress the heat-evoked neuronal activity in CCI rats. Pretreatment with the cannabinoid CB1 receptor antagonists SR141716A or AM251, but not the CB2 antagonist SR144528, blocked the effects. These results provide a neural basis for reports of potent suppression by cannabinoids of the abnormal sensory responses that result from nerve injury.

Effects of subcutaneous formalin on the activity of trigeminal brain stem nociceptive neurones in the rat

1995 ◽  
Vol 73 (2) ◽  
pp. 496-505 ◽  
Author(s):  
P. Raboisson ◽  
R. Dallel ◽  
P. Clavelou ◽  
B. J. Sessle ◽  
A. Woda
Keyword(s):  
Brain Stem ◽  
Time Course ◽  
Dynamic Range ◽  
Neuron Activity ◽  
Formalin Injection ◽  
Second Phase ◽  
Mechanical Stimuli ◽  
Behavioral Experiments ◽  
Nociceptive Neurons ◽  
Short Period

1. The subcutaneous injection of Formalin (5%, 50 microliters) into the receptive field of convergent (wide dynamic range) nociceptive neurons in the spinal dorsal horn has previously been reported to produce a prolonged biphasic response with a time course similar to the observed in behavioral experiments. However, conflicting data in other studies led us to examine the effects of Formalin on the activity of convergent nociceptive neurons at two levels of the trigeminal (V) brain stem complex, namely V subnuclei oralis (Sp5O) and caudalis (Sp5C). 2. Single neuron activity was extracellularly recorded in anesthetized rats. Each neuron was classified as convergent on the basis of its responses to both mechanical and transcutaneous electrical stimuli applied to its mechanoreceptive field (RF). All neurons responded to innocuous and noxious mechanical stimuli and had electrically evoked responses corresponding to both A and C fiber afferent inputs. Seventeen Sp5O and 32 Sp5C convergent neurons received an injection (50 microliters sc) of 5% Formalin into the center of their RF. 3. Three groups of neurons were distinguished: one group that was not activated by the Formalin injection (Sp5O, n = 1; Sp5C, n = 2), another group that responded only with an early and short-lasting response [monophasic neurons: Sp5O, n = 11 (65%); Sp5C, n = 10 (31%)], and a third group that responded with two phases separated by a short period of quiescence [biphasic neurons: Sp5O, n = 5 (29%); Sp5C, n = 20 (62.5%)]. The proportion of biphasic neurons was significantly higher in Sp5C than in Sp5O. 4. The first phases of the Sp5O neurons were not significantly different in terms of duration and frequency from those of the Sp5C neurons. However, duration and discharge frequency of the first phase of biphasic neurons were significantly greater than for monophasic neurons in Sp5C (nonsignificant in Sp5O). The second tonic period of excitation of all biphasic neurons was gradual in outset and offset, and long in duration (23-39 min). The duration of the second phase was significantly longer for the biphasic neurons in Sp5C than for those in Sp5O. 5. Our findings suggest that the mono- and biphasic neurons may have different roles in the transmission of nociceptive information induced by the peripheral injection of Formalin.(ABSTRACT TRUNCATED AT 400 WORDS)

Spinothalamic and spinohypothalamic tract neurons in the sacral spinal cord of rats. II. Responses to cutaneous and visceral stimuli

1996 ◽  
Vol 75 (6) ◽  
pp. 2606-2628 ◽  
Author(s):  
J. T. Katter ◽  
R. J. Dado ◽  
E. Kostarczyk ◽  
G. J. Giesler
Keyword(s):  
Spinal Cord ◽  
Dorsal Horn ◽  
Dynamic Range ◽  
Receptive Fields ◽  
High Threshold ◽  
Mechanical Stimuli ◽  
Power Functions ◽  
Nociceptive Neurons ◽  
Wdr Neurons ◽  
Sacral Spinal Cord

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)

Nociceptive neurons of the raccoon lateral thalamus

1993 ◽  
Vol 69 (2) ◽  
pp. 318-328 ◽  
Author(s):  
D. A. Simone ◽  
M. E. Hanson ◽  
N. A. Bernau ◽  
B. H. Pubols
Keyword(s):  
Dynamic Range ◽  
Receptive Fields ◽  
Glabrous Skin ◽  
High Threshold ◽  
Nociceptive Neurons ◽  
The Core ◽  
Low Threshold ◽  
Wdr Neurons ◽  
Thermal Stimuli ◽  
Heat Hyperalgesia

1. Responses to noxious mechanical and thermal stimuli were examined in 48 thalamic neurons in barbiturate or chloralose-anesthetized raccoons, with special attention to neurons whose peripheral receptive fields (RFs) included glabrous skin of the forepaw. Recording loci were in the core of the ventrobasal complex (VB; n = 32), its ventral or dorsal border (n = 5), or the medial division of the posterior nuclear group (POm; n = 11). 2. Twenty-one VB neurons and 7 POm neurons were classed as wide dynamic range (WDR), whereas 2 VB neurons and 4 POm neurons were classed as nociceptive specific (NS). Response properties of 14 light touch (LT) neurons located in VB were also examined. 3. WDR and NS neurons were not segregated, but rather were intermixed along the ventral and dorsal borders of VB, as well as in POm, and WDR and LT neurons were intermixed in the core of VB. Within the VB core, both LT and WDR neurons were somatotopically organized. 4. All WDR neurons had larger high-threshold than low-threshold RFs, and this difference was greater for POm neurons than for VB neurons. RF areas of LT neurons and low-threshold RF areas of WDR neurons were comparable to those previously reported for raccoon VB units. 5. Out of 25 WDR cells tested, 20 had heat thresholds > 53 degrees C; the range of thresholds in the remaining 5 was 49-53 degrees C. Four out of five NS neurons tested had heat thresholds > 53 degrees C; the threshold of the fifth was 51 degrees C. Of the six neurons with heat thresholds < or = 53 degrees C, two each were in the core of VB, along the border of VB, and in POm. 6. Sensitization to heat after a mild heat injury to the glabrous RF (53 degrees C for 90 s, or 55 degrees C for 30 s) occurred in 8 out of 16 neurons tested, and persisted for up to 2 h. Median thresholds decreased from > 53 degrees C before injury to 47 degrees C after injury, and responses to suprathreshold stimuli were enhanced. There was a significantly greater likelihood (P = 0.02) for sensitization to occur in POm neurons (6/7) than in VB neurons (2/9). 7. It is suggested that a small proportion of neurons located in VB and POm contribute to the sensation of heat pain. Furthermore, sensitization of these neurons may contribute to heat hyperalgesia after an injury to glabrous skin.

Nociceptive neurons in rat superior colliculus: response properties, topography, and functional implications

1989 ◽  
Vol 62 (2) ◽  
pp. 510-525 ◽  
Author(s):  
J. G. McHaffie ◽  
C. Q. Kao ◽  
B. E. Stein
Keyword(s):  
Superior Colliculus ◽  
Dynamic Range ◽  
The Body ◽  
Body Parts ◽  
Power Functions ◽  
Noxious Heat ◽  
Nociceptive Neurons ◽  
Tactile Stimuli ◽  
Noxious Stimuli ◽  
Wdr Neurons

1. Extracellular recordings were made from single superior colliculus neurons in urethane-anesthetized rats in response to mechanical and/or thermal stimulation of the skin. In addition to those activated by low-threshold (LT) tactile stimuli, many neurons responded preferentially, or solely, to noxious stimuli. Two functionally defined subtypes of nociceptive neurons were distinguished: wide-dynamic-range (WDR) neurons, which responded optimally to noxious stimuli but also to innocuous stimuli; and nociceptive-specific (NS) neurons, which responded solely to frankly noxious stimuli. The thermal thresholds were 42-45 degrees C, and the stimulus-response relationships were positively accelerating power functions with exponents of 2.9 (WDR) and 3.1 (NS). 2. WDR neurons also responded to cooling of the skin to temperatures below 24 degrees C. Like noxious heat responses, cold responses were monotonically graded as the intensity of the cold stimulus was increased. Thus the temperature sensitivity of thermal-sensitive neurons in the superior colliculus appeared to be tuned to detect large deviations from ambient skin temperature in either direction once threshold is reached. 3. LT neurons were somatotopically organized, with the head and forelimbs rostral and the trunk and hindlimbs caudal. The limbs were generally represented further lateral in the structure, whereas more proximal body parts were more medial. Nevertheless, there was extensive overlap of body parts especially in areas of transition. Thus, a "block-to-block" or "area-to-area" rather than a "point-to-point" representation of the body surface was evident. 4. The nociceptive representation did not violate the general LT somatotopy but neither was it coextensive. Virtually all nociceptive neurons had trigeminal receptive fields and were thus heavily represented in the rostral superior colliculus, where the LT face representation was also located. No nociceptive neurons were present in the caudal one-third of the structure. A general dorsal-to-ventral segregation of somatosensory neurons also was noted, so that in a given electrode penetration, LT neurons usually were the most superficial, WDR neurons were just below these, and NS neurons were deepest of all. 5. The presence of overlapping LT and nociceptive trigeminal representations in the superior colliculus seems particularly adaptive in view of the fact that rodents use their vibrissae for exploring their environment and thus put rostral body parts at risk during such behaviors.(ABSTRACT TRUNCATED AT 400 WORDS)

Sign in / Sign up

Export Citation Format

Share Document