scholarly journals Response characteristics of pruriceptive and nociceptive trigeminoparabrachial tract neurons in the rat

2015 ◽  
Vol 113 (1) ◽  
pp. 58-70 ◽  
Author(s):  
Nico A. Jansen ◽  
Glenn J. Giesler

We tested the possibility that the trigeminoparabrachial tract (VcPbT), a projection thought to be importantly involved in nociception, might also contribute to sensation of itch. In anesthetized rats, 47 antidromically identified VcPbT neurons with receptive fields involving the cheek were characterized for their responses to graded mechanical and thermal stimuli and intradermal injections of pruritogens (serotonin, chloroquine, and β-alanine), partial pruritogens (histamine and capsaicin), and an algogen (mustard oil). All pruriceptive VcPbT neurons were responsive to mechanical stimuli, and more than half were additionally responsive to thermal stimuli. The majority of VcPbT neurons were activated by injections of serotonin, histamine, capsaicin, and/or mustard oil. A subset of neurons were inhibited by injection of chloroquine. The large majority of VcPbT neurons projected to the ipsilateral and/or contralateral external lateral parabrachial and Kölliker-Fuse nuclei, as evidenced by antidromic mapping techniques. Analyses of mean responses and spike-timing dynamics of VcPbT neurons suggested clear differences in firing rates between responses to noxious and pruritic stimuli. Comparisons between the present data and those previously obtained from trigeminothalamic tract (VcTT) neurons demonstrated several differences in responses to some pruritogens. For example, responses of VcPbT neurons to injection of serotonin often endured for nearly an hour and showed a delayed peak in discharge rate. In contrast, responses of VcTT neurons endured for roughly 20 min and no delayed peak of firing was noted. Thus the longer duration responses to 5-HT and the delay in peak firing of VcPbT neurons better matched behavioral responses to stimulation in awake rats than did those of VcTT neurons. The results indicate that VcPbT neurons may have important roles in the signaling of itch as well as pain.

1993 ◽  
Vol 70 (3) ◽  
pp. 1168-1180 ◽  
Author(s):  
R. D. Sweazey ◽  
R. M. Bradley

1. To better understand sensory information processing in pontine neurons that receive afferent fiber terminations from oral cavity and upper airway receptors, we investigated the response characteristics of single neurons to stimulation of the oral cavity and epiglottis with different stimulus modalities. These response characteristics were then compared with previously recorded response properties of neurons located in other brain stem regions that receive oral cavity and upper airway sensory inputs. 2. Receptive field sizes of pontine neurons were mapped, and responses to mechanical, thermal, and chemical stimuli were determined. A total of 47 neurons were isolated and most neurons were located near the dorsomedial border of the rostral trigeminal subnucleus oralis and caudal principal trigeminal nucleus. The likelihood that a particular stimulus modality would elicit a response was somewhat dependent on a neuron's location. Neurons that responded to chemical stimuli were always located outside the trigeminal nucleus, whereas neurons that responded exclusively to mechanical or thermal stimuli were more frequently located in the trigeminal nucleus. Receptive fields were mapped for 45 of the 47 neurons. Forty-three of the neurons had a single ipsilateral receptive field and > 80% of the receptive fields were > 100 mm2. The majority of neurons responded to only one of the three stimulus modalities. The remaining neurons were multimodal and the combination of stimulus modalities most frequently observed was mechanical and chemical. 3. Mechanical stimuli were the most effective of the three stimulus modalities, eliciting responses in > 65% of the neurons. Neurons that responded to mechanical stimuli were generally rapidly adapting and a moving stimulus was more effective than a punctate stimulus. Mechanosensitive neurons that also responded to chemical stimuli exhibited larger mean response frequencies than mechanosensitive neurons that did not respond to chemical stimuli. Chemical stimuli elicited responses in about half the neurons. A greater percentage of neurons with receptive fields on the epiglottis than neurons with oral cavity receptive fields responded to chemical stimuli. The effectiveness of a chemical stimulus was dependent on a neuron's receptive field. NH4Cl was the most effective stimulus for neurons with receptive fields located in the oral cavity, whereas KCl was more effective for neurons with receptive fields on the epiglottis. Thermal stimuli were relatively ineffective whatever the location of a neuron's receptive field. The majority of neurons showed an increase in response frequency to cooling the receptive field and in all thermosensitive neurons the response was restricted to the dynamic phase of thermal stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)


1995 ◽  
Vol 73 (5) ◽  
pp. 1752-1762 ◽  
Author(s):  
G. M. Bove ◽  
A. R. Light

1. We made recordings from rat dorsal root filaments to study unmyelinated afferent units (conduction velocity < or = 1.5 m/s) associated with deep paraspinal tissues of the dorsal sacrum and proximal tail. Data from 57 unmyelinated units were analyzed in 47 experiments. Receptive fields were identified in intact animals and then surgically isolated using microdissection. Units were characterized using mechanical, noxious chemical, and thermal stimuli. 2. These recordings revealed innervation of the nerve sheaths and surrounding connective tissue, muscles, tendons, and tissue apposed to the undersurface of the skin. No units were found with receptive fields directly on joint capsular tissue. The receptive fields of the units were often multiple and located in more than one tissue; 31 of 57 units showed convergence from different tissues. 3. The units with receptive fields on neurovascular bundles shared sensitivities with other deep tissue units described in this and other reports. These units may have clinical importance in pain due to peripheral neuropathies. 4. The units initially responded to strong mechanical stimulation of the intact animal and often to noxious stretch of the tail. Once surgically isolated, an individual unit's threshold to mechanical stimuli appeared lower. 5. Capsaicin (0.001%-0.1%) elicited responses in 81% (17 of 21) of the units tested. Bradykinin (20 micrograms/ml) elicited responses in 45% (10 of 22) of the units tested. Noxious cold (4-10 degrees C) and hot (55 degrees C) stimulation elicited discharges from 33% (5 of 15) and 25% (5 of 20) of the units tested, respectively. 6. The unmyelinated units had similar mechanical, chemical, and thermal sensitivities. These similarities and the observed convergence only allowed separation of units by the tissue in which the ending was found, and did not allow further classification. 7. The prevalence of background discharge suggested that many units were sensitized during the experiments. 8. The sensitivities of these paraspinal units were similar to those reported for other tissues. Because of the anatomic similarity of the paraspinal tissues of the proximal tail and the lumbar spine, the conclusions of the present study can be related to the lumbar spine. These afferent units are thought to participate in nociception from the deep paraspinal tissues.


1980 ◽  
Vol 43 (1) ◽  
pp. 27-45 ◽  
Author(s):  
L. M. Kow ◽  
F. P. Zemlan ◽  
D. W. Pfaff

1. To analyze further the sensory mechanisms for triggering the lordosis reflex, single-unit (n = 345) activity was recorded extracellularly from spinal segments L5-S1 of urethan-anesthetized female rats. Unit responses to pressure on the skin (necessary and sufficient for evoking lordosis) and other mechanical stimuli were studied. 2. Units were classified according to their responses to the battery of mechanical stimuli: 16% of the units responded only to pressure. The majority of these pressure-responsive units were excited, while a few were inhibited or responded differently, depending on the site stimulated; 52% did not respond to pressure, but responded to brushing, muscle-joint, and/or visceral stimulation, or did not respond at all. The remaining 32% responded to pressure plus other forms of stimulation. 3. Units responding only to the movement of individual types of hair tended to be located in the dorsal horn, more dorsal than units responding only to pressure (found primarily in the intermediate gray). Units responding to subdermal stimulation were usually found at greater depths. Segmental and somatotopic distributions of spinal units observed were very similar to those reported for cat (3) and monkey (5). 4. Compared to primary sensory units (28), spinal units had higher resting firing rates, more complicated responses to a given stimulus, a wider variety of unit types, and much larger receptive fields. These comparisons tend to indicate convergence of primary sensory neurons onto individual spinal units. 5. The range of pressure thresholds of pressure-responsive units is comparable to the range effective for triggering lordosis. We postulate that excitation of units responding only to pressure is centrally involved in triggering the lordosis reflex. Those units not responding to pressure are probably irrelevant for this behavior. Presently undetermined are the roles of units with complex or mixed-response types.


2012 ◽  
Vol 107 (1) ◽  
pp. 357-363 ◽  
Author(s):  
C. Ma ◽  
H. Nie ◽  
Q. Gu ◽  
P. Sikand ◽  
R. H. LaMotte

Native cowhage spicules, and heat-inactivated spicules containing histamine or capsaicin, evoke similar sensations of itch and nociceptive sensations in humans. In ongoing studies of the peripheral neural mechanisms of chemical itch and pain in the mouse, extracellular electrophysiological recordings were obtained, in vivo, from the cell bodies of mechanosensitive nociceptive neurons in response to spicule stimuli delivered to their cutaneous receptive fields (RFs) on the distal hindlimb. A total of 43 mechanosensitive, cutaneous, nociceptive neurons with axonal conduction velocities in the C-fiber range (C-nociceptors) were classified as CM if responsive to noxious mechanical stimuli, such as pinch, or CMH if responsive to noxious mechanical and heat stimuli (51°C, 5 s). The tips of native cowhage spicules, or heat-inactivated spicules containing histamine or capsaicin, were applied to the RF. Heat-inactivated spicules containing no chemical produced only a transient response occurring during insertion. Of the 43 mechanosensitive nociceptors recorded, 20 of the 25 CMHs responded to capsaicin, and of these, 13 also responded to cowhage and/or histamine. In contrast, none of the 18 CMs responded to any of the chemical stimuli. The time course of the mean discharge rate of CMHs was similar in response to each type of spicule and generally similar, although reaching a peak earlier, to the temporal profiles of itch and nociceptive sensations evoked by the same stimuli in humans. These findings are consistent with the hypothesis that the itch and nociceptive sensations evoked by these punctuate chemical stimuli are mediated at least in part by the activity of mechanoheat-sensitive C-nociceptors. In contrast, activity in mechanosensitive C-nociceptors that do not respond to heat or to pruritic chemicals is hypothesized as contributing to pain but not to itch.


2017 ◽  
Author(s):  
Patrick D. McClanahan ◽  
Joyce H. Xu ◽  
Christopher Fang-Yen

AbstractThe roundworm Caenorhabditis elegans is an important model system for understanding the genetics and physiology of touch. Classical assays for C. elegans touch, which involve manually touching the animal with a probe and observing its response, are limited by their low throughput and qualitative nature. We developed a microfluidic device in which several dozen animals are subject to spatially localized mechanical stimuli with variable amplitude. The device contains 64 sinusoidal channels through which worms crawl, and hydraulic valves that deliver touch stimuli to the worms. We used this assay to characterize the behavioral responses to gentle touch stimuli and the less well studied harsh (nociceptive) touch stimuli. First, we measured the relative response thresholds of gentle and harsh touch. Next, we quantified differences in the receptive fields between wild type worms and a mutant with non-functioning posterior touch receptor neurons. We showed that under gentle touch the receptive field of the anterior touch receptor neurons extends into the posterior half of the body. Finally, we found that the behavioral response to gentle touch does not depend on the locomotion of the animal immediately prior to the stimulus, but does depend on the location of the previous touch. Responses to harsh touch, on the other hand, did not depend on either previous velocity or stimulus location. Differences in gentle and harsh touch response characteristics may reflect the different innervation of the respective mechanosensory cells. Our assay will facilitate studies of mechanosensation, sensory adaptation, and nociception.


1990 ◽  
Vol 63 (3) ◽  
pp. 473-490 ◽  
Author(s):  
J. F. Bernard ◽  
J. M. Besson

1. Neurons were recorded in the parabrachial (PB) area, located in the dorsolateral region of the pons (with the use of extracellular micropipette), in the anesthetized rat. Parabrachioamygdaloid (PA) neurons (n = 67) were antidromically identified after stimulation in the centralis nucleus of the amygdala (Ce). The axons of these neurons exhibit a very slow conduction velocity, between 0.26 and 1.1 m/s, i.e., in the unmyelinated range. 2. These PA neurons were located in a restricted region of the PB area: the subnuclei external lateral (PBel) and external medial (PBem). A relative somatotopic organization was found in this region. 3. These units were separated into two groups: 1) a group of nociceptive-specific (NS) neurons (69%), which responded exclusively to noxious stimuli, and 2) a group of nonresponsive (NR) neurons (31%). 4. The NS neurons exhibited low or lacked spontaneous activity. They responded exclusively to mechanical (pinch or squeeze) and/or thermal (waterbath or waterjet greater than 44 degrees C) noxious stimuli with a marked and sustained activation with a rapid onset and generally without afterdischarge. Noxious thermal stimuli generally induced a stronger response than the noxious mechanical stimuli. These neurons exhibited a clear capacity to encode thermal stimuli in the noxious range: 1) the stimulus-response function was always positive and monotonic; 2) the slope of the curve progressively increased up to a maximum where it was very steep, then the steepness of the slope decreased close to the maximum response; and 3) the mean threshold was 44.1 +/- 2 degrees C, and the point of steepest slope of the mean curve was around 47 degrees C. 5. The excitatory receptive fields of the NS neurons were large in the majority (70%) of the cases and included several areas of the body. A more marked activation was often obtained from stimuli applied to one part of the body, denoted as the preferential receptive field (PRF). In the other cases (30%), the excitatory receptive field was relatively small (SRF) and restricted to one part of the body (the tail, a paw, a hemiface, or the tongue). Both the PRF and SRF were more often located on the contralateral side. In addition, noxious stimuli applied outside the excitatory receptive field were found to strongly inhibit the responses of NS neurons. 6. All the NS neurons responded to intense transcutaneous electrical stimulation applied to the PRF or SRF with two peaks of activation.(ABSTRACT TRUNCATED AT 400 WORDS)


1987 ◽  
Vol 57 (6) ◽  
pp. 1686-1704 ◽  
Author(s):  
K. C. Kajander ◽  
G. J. Giesler

The majority of neurons at the origin of the spinocervical tract are driven by noxious stimulation of their receptive fields. Surprisingly, previous studies have encountered only a small percentage of nociceptive neurons within the terminus of the spinocervical tract, the lateral cervical nucleus (LCN). To determine if previous reports have underestimated the proportion of nociceptive LCN neurons, 129 neurons within the nucleus were physiologically identified and examined in cats prepared using three different methods. Fifty-nine percent of the neurons studied in unanesthetized cats that were decerebrated and spinalized responded either differentially or exclusively to noxious mechanical stimulation of the skin within discrete receptive fields. LCN neurons also gave accelerating responses to increasingly more intense noxious thermal stimuli. LCN neurons are, therefore, capable of coding both the intensity and location of noxious stimuli. Only 6% of LCN neurons responded to noxious cutaneous stimuli in unanesthetized, decerebrated cats in which the spinal cord was intact. Only 4% of LCN neurons in intact urethan-anesthetized cats were driven by noxious stimulation. Several previous studies of the LCN have been performed in cats that were deeply anesthetized with barbiturates. Therefore, the effects of barbiturates on the nociceptive responses of LCN neurons were determined. Subanesthetic doses of intravenously administered barbiturates reduced or eliminated the responses of nociceptive LCN neurons to noxious thermal stimuli in decerebrated and spinalized cats. Responses to innocuous mechanical stimuli by these neurons were not blocked by barbiturates. Nociceptive LCN neurons in decerebrated and spinalized cats were somatotopically organized. Neurons with forelimb receptive fields were located in the ventromedial half of the LCN; neurons with hindlimb receptive fields were located in the dorsolateral half of the nucleus. This report and previous studies of the spinocervical tract suggest that the spinocervicothalamic pathway is capable of playing an important role in nociception.


1984 ◽  
Vol 51 (4) ◽  
pp. 616-635 ◽  
Author(s):  
T. Yamamoto ◽  
N. Yuyama ◽  
T. Kato ◽  
Y. Kawamura

The responses of 111 cortical neurons to the four classical taste stimuli (sucrose, NaCl, HCl, and quinine HCl) applied to the anterior part of the tongue were recorded extracellularly in lightly anesthetized rats. Basic response properties of these cortical taste neurons were analyzed. The location of 88 of 111 neurons were histologically identified. They were distributed from anterodorsal to posteroventral direction in the insular cortex just dorsal to the rhinal sulcus and ventral to the somatic sensory area I. The receptive fields of 17 cortical neurons were examined. Most (94%) of the neurons had a narrow focus on the ipsilateral, contralateral, or bilateral sides of the tongue surface. Half of the foci were surrounded by a less-sensitive receptive field of relatively wide size. No apparent relationship was detected between the location of the cortical neurons and the site or extent of the receptive fields of those neurons, indicating a lack of topographical organization in the cortical gustatory area. The mean rate of the spontaneous discharges was 7.1 impulses/3 s, which is about 3 times larger than that in a first-order taste nerve (chorda tympani). The statistically significant difference of spontaneous discharges among response types of cortical neurons was observed only between the neurons responding in an excitatory manner to only one or two kinds of basic stimuli (6.2 impulses/3 s) and the neurons responding in an inhibitory manner to more than three kinds of taste stimuli (14.2 impulses/3 s). When the net responses (spontaneous rate subtracted) to each of the four tastes were compared with the spontaneous discharges in each neuron, the magnitude of spontaneous discharges was significantly negatively correlated with the net response to sucrose. This fact indicates that a neuron with a larger spontaneous discharge rate has a tendency to respond less to sucrose. Response characteristics of cortical taste neurons were quite distinct from those of the first-order taste neurons in the following respects: 1) a decrease in the average evoked discharge rate, which resulted in a small signal-to-noise ratio; 2) a tendency toward equalization of effectiveness of the four basic taste stimuli; 3) about 27% of the neurons decreased their firing rate during the first 3 s after the onset of taste stimulation; and 4) no clear initial phasic response, with a fluctuation in impulse discharges in some neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


1976 ◽  
Vol 39 (6) ◽  
pp. 1160-1175 ◽  
Author(s):  
R. E. Beitel ◽  
R. Dubner

1. The response of C polymodal nociceptors to thermal and mechanical stimuli applied to the monkey's face was recorded extracellulary in the trigeminal ganglion in rhesus monkeys anesthetized with sodium pentobarbital. Conduction velocities, determined from electrical stimulation of receptive fields (RFs), were in the range for unmyelinated C fibers (mean=0.82 m/s, n=20; SD=+/-0.17). With two exceptions cutaneous RFs were single spots (median=2 mm2; n=37) and usually were identical for thermal and mechanical stimuli. The median force threshold for the sample of units was 1.2 g (von Frey technique; n = 39; range = 0.07-8.5 g). 2. Discharges to thermal stimuli were investigated with a feedback-controlled contact thermode which permitted temperature changes less than or equal 12.0 degrees C/s. Thermal thresholds ranged from 38 degree to 49 degree C (median=46 degrees C; n=37), and maximum discharge frequencies were obtained in the noxious heat range (45-55 degrees C). For a graded series of 5 s duration stimuli from an adapting temperature of 35 degrees C, the number of impulses increased as a monotonic function of stimulus intensity over the range from threshold temperature to 50-53 degrees C. Many stimulus-response functions were positively accelerated, and linear regression analyses showed that most units examined were best fit by nonlinear functions. 3. The typical pattern of activity to 5 s duration temperature shifts into the noxious heat range was a short accelerating burst of impulses followed by deceleration to a lower rate of discharge prior to termination of the stimulus. The temporal profile of the discharge of impulses was virtually identical at different adapting temperatures. In units tested with 30 s duration stimuli at 2-6 degrees C above threshold, the mean frequency of discharge during the final 25 s was 1.46 impulses/s (n=6; SD=+/-0.89). 4. Application of noxious heat stimuli a few degrees above threshold temperature typically sensitized or enhanced the response of the unit to subsequent application of heat stimuli. The signs of sensitization consisted of a decrease in threshold temperature, increased frequency of discharge, decreased latency to the first impulse, and afterdischarges. Units failed to respond throughout the duration of 30 s stimuli if the final temperature exceeded 50 degrees C. Depressed responses were sometimes produced by application of intense (greater than or equal 55 degrees C) stimuli, presumably as a result of partial inactivation of the receptor. 5. In a correlative analysis, the latency and pattern of discharge in a sample of units were compared with escape responses in two monkeys to temperature shifts into the noxious heat range (49 and 51 degrees C). The analysis revealed that the discharge of C polymodal nociceptors alone cannot account for fast escape responses, but the discharge may contribute to escape responses which occur more than 3.5 s after the onset of stimulation.


1988 ◽  
Vol 59 (1) ◽  
pp. 142-163 ◽  
Author(s):  
K. J. Berkley ◽  
A. Robbins ◽  
Y. Sato

1. In the present three-part study electrophysiological techniques were used to characterize responses of afferent fibers in the rat hypogastric nerve to mechanical or chemical stimulation of the uterus, and anatomical techniques were used to identify the spinal segments through which uterine afferent fibers enter the spinal cord. 2. In an in vivo barbiturate-anesthetized preparation, hypogastric afferent fibers responded in a time-locked manner to mechanical stimulation confined to restricted regions of the uterus and adjacent ligament. Receptive fields were most often located on the uterine body, particularly over the cervix. The few located on the uterine horn were usually near regions irritated during preparative surgery. Effective mechanical stimuli (pressure, stretching, squeezing, probing, rarely contractions) were typically greater than 5 g and simultaneously accompanied by transient ischemia around the probe or contracted area. Distension, unless extreme, was not an effective stimulus. Retrospective analysis of the data indicated that fibers may be more sensitive to uterine stimulation when rats are in vaginal estrus/proestrus than in diestrus/metestrus. 3. In an in vitro preparation, hypogastric afferent fibers responded in a dose-dependent fashion to injections into the uterine artery of the algesic chemicals bradykinin, 5-hydroxytryptamine, and KCl. They also responded to high doses of CO2 (in saline) and NaCN, but rarely to lower doses. Nearly all fibers responded to more than one chemical with response characteristics unique to each chemical (e.g., latency, duration, peak rate). 4. Injections of horseradish peroxidase into the uterine body and small portions of the adjacent horns in rats in vaginal estrus consistently labeled a small number of cells in the L1-S1 dorsal root ganglia, with peaks at L2 and L6. Virtually no cells were labeled in rats whose estrous cycle had been disrupted (by inadvertently keeping them in constant light conditions for several weeks). 5. These results indicate that uterine afferent fibers travel to the central nervous system through both the hypogastric (e.g., L1-L4 ganglia) and pelvic (e.g., L5-S1 ganglia) nerves in the rat, and that hypogastric fibers are capable of conveying fairly precise information about temporal and spatial aspects of uterine mechanical and chemical stimulation. The results also encourage future research into the possibility that the responses of these fibers vary as a function of estrous stage or other aspects of the condition of the uterus (e.g., its irritation).(ABSTRACT TRUNCATED AT 400 WORDS)


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