scholarly journals A topographical and physiological exploration of C-tactile afferents and their response to menthol and histamine

Author(s):  
Line Sofie Loken ◽  
Helena Backlund Wasling ◽  
Håkan Olausson ◽  
Francis McGlone ◽  
Johan Wessberg

Unmyelinated tactile (CT) afferents are abundant in arm hairy skin and have been suggested to signal features of social affective touch. Here we recorded from unmyelinated low-threshold mechanosensitive afferents in the peroneal and radial nerves, with the most distal receptive fields located on the proximal phalanx of the third finger for the superficial branch of the radial nerve, and near the lateral malleolus for the peroneal nerve. We found that the physiological properties with regard to conduction velocity and mechanical threshold, as well as their tuning to brush velocity, were similar in CT units across the antebrachial (n=27), radial (n=8) and peroneal nerves (n=4). Moreover, we found that while CT afferents are readily found during microneurography of the arm nerves, they appear to be much more sparse in the lower leg compared to C nociceptors. We continued to explore CT afferents with regard to their chemical sensitivity and found that they could not be activated by topical application to their receptive field of either the cooling agent menthol or the pruritogen histamine. In light of previous studies showing the combined effects that temperature and mechanical stimuli have on these neurons, these findings add to the growing body of research suggesting that CT afferents constitute a unique class of sensory afferents with highly specialized mechanisms for transducing gentle touch.

2021 ◽  
Author(s):  
Line S Loken ◽  
Helena Backlund Wasling ◽  
Hakan Olausson ◽  
Francis S McGlone ◽  
Johan Wessberg

Numerous microneurography studies in the human peroneal nerve have suggested that CT afferents are lacking in the more distal parts of the limbs. Here we recorded from unmyelinated low-threshold mechanosensitive afferents in the peroneal and radial nerves, with the most distal receptive fields located on the proximal phalanx of the third finger for the superficial branch of the radial nerve, and near the lateral malleolus for the peroneal nerve. We found that the physiological properties with regard to conduction velocity and mechanical threshold, as well as their tuning to brush velocity, were similar in CT units across the antebrachial, radial and peroneal nerves. Moreover, we found that while CT afferents are readily found during microneurography of the arm nerves, they appear to be much more sparse in the lower leg compared to C nociceptors. We continued to explore CT afferents with regard to their chemical sensitivity and found that they could not be activated by topical application to their receptive field of either the cooling agent menthol or the pruritogen histamine. In light of previous studies showing the combined effects that temperature and mechanical stimuli have on these neurons, including a lack of responsiveness to heat, these findings add to the growing body of research suggesting that CT afferents constitute a unique class of sensory afferents with highly specialized mechanisms for transducing gentle touch.


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)


1990 ◽  
Vol 64 (5) ◽  
pp. 1502-1513 ◽  
Author(s):  
R. D. Treede ◽  
R. A. Meyer ◽  
J. N. Campbell

1. Receptive-field properties were investigated in cutaneous C-fiber nociceptive afferents (CMH) responsive to mechanical and heat stimuli. Teased-fiber techniques were used to record from 28 CMHs that innervated the hairy skin of upper or lower limb in anesthetized monkeys. 2. The response to mechanical stimuli was studied with the use of calibrated von Frey probes. The response to heat stimuli was studied with the use of a laser thermal stimulator that provided stepped increases in skin temperature with rise times to the desired temperature near 100 ms. The size of the receptive field (RF) for mechanical stimuli was determined by use of a suprathreshold stimulus that consisted of a 0.5-mm-diam probe that exerted a 200-mN force (10 bar). The size of the heat RF was determined by use of a 49 degrees C stimulus applied to a 7.5-mm-diam area for 1 s. 3. Heat thresholds were determined with an ascending series of stimulus intensities and were found to be stable over many hours: they ranged from 37 to 46 degrees C (mean, 41.1 degrees C). Mechanical thresholds ranged from 1.3 to 7.3 bar (mean, 3.3 bar). There was no correlation between mechanical and heat thresholds. Both thresholds extended well below the corresponding psychophysical pain thresholds in the literature. This suggests that spatial and/or temporal summation of C-fiber input are important for pain induced by either stimulus modality. 4. Mechanical RF diameters ranged from 3.3 to 9.6 mm (mean, 4.7 mm); heat RF diameters ranged from punctate (less than 1 mm) to 9.5 mm (mean, 4.3 mm). There was a significant linear correlation between mechanical and heat RF sizes with a slope of one. The distance between the center of the mechanical RF and the center of the heat RF along one axis ranged from 0 to 1.1 mm (mean, 0.4 mm). These data indicate that the heat RFs coincided with the mechanical RFs. 5. Within the mechanical RF determined with the suprathreshold stimuli, all CMHs had one or more punctate areas of maximal mechanical sensitivity where mechanical threshold was lowest. Heat excitability extended greater than 2 mm beyond these mechanically sensitive spots. Because lateral transmission of the heat stimulus is small, this indicates that heat transduction occurs outside the regions of maximal mechanical sensitivity. 6. Both the threshold to heat and the response magnitude at suprathreshold intensities depended on the percentage of the RF area overlapped by the heat stimulus. This indicates that multiple transducer sites probably contribute to the total evoked response.(ABSTRACT TRUNCATED AT 400 WORDS)


1993 ◽  
Vol 70 (4) ◽  
pp. 1365-1377 ◽  
Author(s):  
V. Neugebauer ◽  
T. Lucke ◽  
H. G. Schaible

1. In 22 anesthetized rats we studied the involvement of N-methyl-D-aspartate (NMDA) and non-NMDA receptors in the generation and maintenance of hyperexcitability in spinal cord neurons with knee input that develops in the course of an acute inflammation in the knee. In all experiments one neuron with knee input was identified, and the responses to mechanical stimuli and the receptive fields were monitored before and after induction of inflammation by the intra-articular injections of kaolin and carrageenan into the joint cavity. In most experiments multibarrel electrodes were used to administer specific NMDA and non-NMDA antagonists ionophoretically close to the neuron to test their effects on the inflammation-evoked changes. 2. Six neurons in the deep dorsal horn in six rats were used to establish the time course of the development of hyperexcitability in the untreated animal. In control periods of up to 3 h, the responses to mechanical stimuli and the receptive fields were stable. After induction of inflammation, the neurons developed increased responsiveness to mechanical stimuli applied to the injected knee but also to mechanical stimuli applied to the ipsilateral ankle and paw (including a reduction in the mechanical threshold in nociceptive specific neurons). The receptive fields expanded in five out of six neurons. The changes of responsiveness occurred mainly in the 2nd to 3rd h after the injection of kaolin. 3. In four rats three to four intravenous injections of the NMDA antagonist ketamine (2 mg/kg) were given during the injections of kaolin and carrageenan and in the following periods (up to 101 min postkaolin). During this treatment none of the four neurons exhibited the changes of responsiveness that were usually seen in control animals, although swelling of the knee developed in the same fashion as in control rats. Similarly, the generation of hyperexcitability was prevented when the NMDA antagonists ketamine and DL-2-amino-5-phosphonovalerate (AP5) were administered ionophoretically (ketamine in 4, AP5 in 2 rats) during the injections of kaolin and carrageenan and up to 100 min postkaolin. The doses of ketamine and AP5 were sufficient to reduce the responses to NMDA, whereas the responses to the non-NMDA agonist alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) were not influenced. 4. The ionophoretic application of the non-NMDA antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) during the injections of the kaolin and carrageenan and up to 103 min postkaolin also prevented the generation of hyperexcitability in six neurons in six rats.(ABSTRACT TRUNCATED AT 400 WORDS)


1995 ◽  
Vol 73 (2) ◽  
pp. 693-702 ◽  
Author(s):  
H. R. Koerber ◽  
K. Mirnics ◽  
L. M. Mendell

1. The tibial and sural nerves in cats were cut, anastomosed to their distal stumps, and allowed to regenerate for 3-17.5 mo. In the terminal acute experiment, individual afferents were impaled in the dorsal root ganglion to study their receptive field properties, somatic spike parameters, and spinal projections using cord dorsum potential (CDP) measurements. Properties of the CDPs provided evidence on whether the afferent fibers were originally proprioceptive or cutaneous (rapidly or slowly adapting). 2. Fibers with the largest conduction velocity were selectively slowly adapting, suggesting that large muscle afferents maintained their adaptation properties regardless of the peripheral structure innervated. Similarly, the relationship of somatic spike configuration to mechanical threshold was largely normal. Cells with narrow spikes innervated low-threshold mechanoreceptors, whereas cells with broad spikes and an inflection on the descending limb innervated high-threshold mechanoreceptors. 3. Spikes with intermediate properties were observed in some cells that innervated low-threshold mechanoreceptors in the periphery. These were classified as "hybrid" spikes. 4. The largest CDPs were evoked by afferents classified as having originally been cutaneous fibers, regardless of whether they had reinnervated cutaneous or subcutaneous receptors. Fibers classified as has having originally been proprioceptive afferents produced much smaller CDPs; however, these afferents never produce CDPs in intact preparations. Afferents nonresponsive to peripheral stimulation, classified putatively as having been cutaneous, also evoked small CDPs. 5. Fibers classified as putatively cutaneous or proprioceptive could reinnervate foreign target tissue (subcutaneous tissue or skin, respectively), but a propensity to reinnervate the original target tissue was observed. 6. Among putative cutaneous afferents, those with rostrocaudal CDP distributions somatotopically correct for the location of their receptive fields evoked the largest CDPs regardless of the peripheral tissue innervated. 7. We conclude that receptive field properties (adaptation, mechanical threshold) of regenerated afferents are well matched with the electrophysiological properties of the soma and axon. The properties of the central projections of these afferents are not as well matched with their peripheral receptor properties. This is discussed in terms of the plasticity of the central projections of axotomized afferents.


1990 ◽  
Vol 4 (4) ◽  
pp. 367-377 ◽  
Author(s):  
D. M. Guthrie ◽  
J. R. Banks

AbstractThe anatomy and physiology of the retinotectal pathway of the perch was investigated using physiological and histological techniques. Massed responses of the optic nerve to single shocks exhibited five distinct peaks. Single-unit responses to shocks indicate two groups of fast fibers correlating well with peaks I and II of the massed response. The flash-evoked response in nerve and tectum has three major phases (PSPI-III), with a marked low-threshold fast component. Patterns of flash-evoked response from single fibers vary, but the responses of fast transient fibers coincide with the timing of PSPI, and longer latency groups with PSPII-III. Units reflexly activated by efferents were also seen, and 12% of units were photically inexcitable.Surprisingly, few fibers responded well to a scanned spot light, unlike tectal cells, and receptive fields were often large (>70 deg). ON/OFF responses, evoked either by whole field or local illumination, were much commoner than pure ON or OFF responses.Effects of electrical stimulation or cautery of the tectum on the flash-evoked response of fiber bundles, via the efferents were marginal, but repetitive stimulation or section of the optic nerve produced clear-cut deficits in the slow components of the flash-evoked response of the nerve. Stimulation of the eighth nerve produced a complex long-latency, large-amplitude response in the optic nerve.The fiber spectrum of the optic nerve taken from electron micrographs revealed the presence of a relatively small group (less than 1%) of thick fibers with diameters between 3 μm and 10 μm that could be correlated with fast responses recorded from the optic nerve, and the remainder with axon diameters down to 0.2 μm providing the slow responses. The distribution of cell-body diameters from sectioned and wholemount material indicated a marked distinction between small and large ganglion cells. The total number of fibers in the nerve was estimated 868,840.


1997 ◽  
Vol 77 (1) ◽  
pp. 299-308 ◽  
Author(s):  
Geoffrey M. Bove ◽  
Michael A. Moskowitz

Bove, Geoffrey M. and Michael A. Moskowitz. Primary Afferent Neurons Innervating Guinea Pig Dura. J. Neurophysiol. 77: 299–308, 1997. We made recordings from filaments of guinea pig nasociliary nerve to study response properties of afferent axons innervating the anterior superior sagittal sinus and surrounding dura mater. We analyzed 38 units in 14 experiments. Units were initially located with the use of mechanical stimuli, and were then characterized by their conduction velocity and sensitivities to mechanical, thermal, and chemical stimuli. Single-unit recordings revealed innervation of dura and superior sagittal sinus by slowly conducting axons, mostly in the unmyelinated range. The receptive fields were 1–30 mm2, and typically had one to three punctate spots of highest sensitivity. All units tested responded to topical application of chemical agents. Ninety-seven percent of units responded to 10−5 M capsaicin, 79% responded to a mixture of inflammatory mediators, and 37% responded to an acidic buffer (pH 5). These data underline the importance of chemical sensitivity in intracranial sensation. Heat and cold stimuli evoked responses in 56 and 41% of units tested, respectively. Although the response patterns during heating were typical of polymodal nociceptors innervating other tissues, the thresholds were lower than for other tissues (32.3–42°C). Cooling led to a phasic discharge, with thresholds between 25 and 32°C. Although units had different combinations of responses to mechanical, chemical, and thermal stimuli, when grouped by their sensitivities the groups did not differ regarding mechanical thresholds or presence of ongoing activity. This suggests that meningeal primary afferents are relatively homogeneous. Sensitivities of these units are in general consistent with nociceptors, although the thermal thresholds differ. These data provide the first detailed report of response properties of intracranial primary afferent units, likely to be involved in transmission of nociception and possibly mediation of intracranial pain.


1996 ◽  
Vol 75 (6) ◽  
pp. 2441-2450 ◽  
Author(s):  
D. D. Rasmusson

1. Single neurons in the ventroposterior lateral thalamic nucleus were studied in 10 anesthetized raccoons, 4 of which had undergone amputation of the fourth digit 4-5 mo before recording. Neurons with receptive fields on the glabrous skin of a forepaw digit were examined in response to electrical stimulation of the “on-focus” digit that contained the neuron's receptive field and stimulation of an adjacent, “off-focus” digit. 2. In normal raccoons all neurons responded to on-focus stimulation with an excitation at a short latency (mean 13 ms), whereas only 63% of the neurons responded to off-focus digit stimulation. The off-focus responses had a longer latency (mean 27.2 ms) and a higher threshold than the on-focus responses (800 and 452 microA, respectively). Only 3 of 32 neurons tested with off-focus stimulation had both a latency and a threshold within the range of on-focus values. Inhibition following the excitation was seen in the majority of neurons with both types of stimulation. 3. In the raccoons with digit removal, the region of the thalamus that had lost its major peripheral input (the “deafferented” region) was distinguished from the normal third and fifth digit regions on the basis of the sequence of neuronal receptive fields within a penetration and receptive field size as described previously. 4. Almost all of the neurons in the deafferented region (91%) were excited by stimulation of one or both adjacent digits. The average latency for these responses was shorter (15.3 ms) and the threshold was lower than was the case with off-focus stimulation in control animals. These values were not significantly different from the responses to on-focus stimulation in the animals with digit amputation. 5. These results confirm that reorganization of sensory pathways can be observed at the thalamic level. In addition to the changes in the somatotopic map that have been shown previously with the use of mechanical stimuli, the present paper demonstrates an improvement in several quantitative measures of single-unit responses. Many of these changes suggest that this reorganization could be explained by an increased effectiveness of preexisting, weak connections from the off-focus digits; however, the increase in the proportion of neurons responding to stimulation of adjacent digits may indicate that sprouting of new connections also occurs.


2018 ◽  
Author(s):  
Jan Walcher ◽  
Julia Ojeda-Alonso ◽  
Julia Haseleu ◽  
Maria K. Oosthuizen ◽  
Ashlee H. Rowe ◽  
...  

AbstractRodents use their forepaws to actively interact with their tactile environment. Studies on the physiology and anatomy of glabrous skin that makes up the majority of the forepaw are almost non-existent in the mouse. Here we developed a preparation to record from single sensory fibers of the forepaw and compared anatomical and physiological receptor properties to those of the hind paw glabrous and hairy skin. We found that the mouse forepaw skin is equipped with a very high density of mechanoreceptors; >3 fold more than hind paw glabrous skin. In addition, rapidly adapting mechanoreceptors that innervate Meissner’s corpuscles of the forepaw were several-fold more sensitive to slowly moving mechanical stimuli compared to their counterparts in the hind paw glabrous skin. All other mechanoreceptors types as well as myelinated nociceptors had physiological properties that were invariant regardless of which skin area they occupied. We discovered a novel D-hair receptor innervating a small group of hairs in the middle of the hind paw glabrous skin in mice. Glabrous D-hair receptors were direction sensitive albeit with an orientation sensitivity opposite to that described for hairy skin D-hair receptors. Glabrous D-hair receptors do not occur in all rodents, but are present in North American and African rodent species that diverged more than 65 million years ago. The function of these specialized hairs is unknown, but they are nevertheless evolutionarily very ancient. Our study reveals novel physiological specializations of mechanoreceptors in the glabrous skin that likely evolved to facilitate tactile exploration.


1985 ◽  
Vol 53 (6) ◽  
pp. 1387-1400 ◽  
Author(s):  
T. Yokota ◽  
N. Koyama ◽  
N. Matsumoto

Recordings were made from single thalamic units in the urethan-chloralose anesthetized cat. Altogether 2,905 trigeminal single units having a receptive field in the contralateral trigeminal integument were isolated from the somatosensory part of nucleus ventralis posteromedialis, or VPM proper. Each isolated unit was tested for responses to a series of mechanical stimuli. The stimuli included brushing the skin, touch, pressure, noxious pinch, and pinpricks. The majority of VPM proper units responded with the greatest discharge frequency to gentle mechanical stimulation: either hair movement or light pressure to the trigeminal integument, but 341 units were identified as trigeminal nociceptive units. They were partitioned into two functionally defined subclasses, nociceptive specific (NS) and wide dynamic range (WDR) units, but not intermingled with low-threshold mechanoreceptive (LTM) units. Both NS and WDR units were found at or near the margin of the VPM proper but not outside this nucleus. This marginal area was referred to as the shell region of the VPM proper. A total of 248 NS units was found within the shell region of the caudal third of the VPM proper. This part was called the NS zone. These units were somatotopically organized. In the rostral part of the NS zone, ophthalmic NS units having a receptive field in the contralateral ophthalmic division were located dorsolaterally, maxillary NS units occurred dorsomedially, and mandibular NS units were found ventromedially. In the caudal part of the NS zone, maxillary NS units were encountered in the dorsal shell region, whereas mandibular NS units were found in the ventromedial shell region. Ophthalmic NS units were not found in this part of the NS zone. Altogether 93 WDR units were encountered in the shell region of the VPM proper. They were confined to a narrow band approximately 300 micron wide just rostral to the NS zone. These units were somatotopically organized. Ophthalmic WDR units having a low-threshold center of the receptive field in the contralateral ophthalmic division were located dorsolaterally, maxillary WDR units were located dorsomedially, and mandibular WDR units were located ventromedially. The majority of maxillary as well as mandibular WDR units were activated by electrical stimulation of the contralateral maxillary and/or mandibular canine tooth pulp afferents. Both NS and WDR zones of the VPM proper extended into the shell region of the nucleus ventralis posterolateralis (VPL).(ABSTRACT TRUNCATED AT 400 WORDS)


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