Physiological properties of primary sensory neurons appropriately and inappropriately innervating skin in the adult rat

1991 ◽  
Vol 66 (4) ◽  
pp. 1205-1217 ◽  
Author(s):  
G. R. Lewin ◽  
S. B. McMahon

1. We have studied the physiology of sensory neurons innervating skin of the rat hindlimb, in three groups of animals: 1) normal animals; 2) animals in which the sural nerve (Sn) had regenerated to its original cutaneous target; and 3) animals in which the gastrocnemius muscle nerve (Gn) had previously been cut and cross anastomosed with the distal stump of the cut Sn so that its axons regenerated to a foreign target, skin. 2. Single-unit recordings were made from 222 afferents in normal, intact animals. They had conduction velocities of 0.5-53.1 m/s. The conduction velocity distribution had distinct peaks at approximately 37.5, 2.5, and 1.25 m/s, presumably corresponding to A alpha beta-, A delta-, and C-fiber populations. Eighty-two percent of the characterized myelinated fibers had low-threshold mechanosensitive receptive fields, whereas 16% were high threshold, and only 2% appeared to have no receptive field. The very large majority of low-threshold mechanosensitive receptive fields (87%) were rapidly adapting hair follicle afferents. 3. In animals with regenerated Sn, 308 afferents were recorded with conduction velocities of 0.4-58.8 m/s. However, the mean conduction velocity was lower than in control animals (P less than 0.05), and only one peak, at 27.5 m/s, was apparent for myelinated fibers. Eighty-six percent of myelinated fibers were low-threshold mechanosensitive afferents, 8.5% were high-threshold mechanoreceptors (HTMRs), and 5.5% appeared to have no receptive fields. Fewer low-threshold mechanoreceptors (LTMRs; compared with controls) were activated by hair movement (63 vs. 87%). Most of the remainder appeared to be field receptors (which were therefore more commonly observed here than in normal animals). 4. In animals in which the Gn had regenerated to skin, 430 afferents were recorded. These had conduction velocities ranging from 0.6 to 71.4 m/s, and again only one peak was apparent in the myelinated conduction velocity histogram, at approximately 17.5 m/s. Of the myelinated fibers, 79% had low-threshold mechanosensitive receptive fields in skin and 10% high-threshold mechanosensitive receptive fields. The remaining 11% apparently had no receptive field (cf. 5.5% in regenerated Sn). In contrast to normal or regrown sural afferents, only 58% of low-threshold gastrocnemius afferents in skin were rapidly adapting. Of the 42% slowly adapting afferents, many surprisingly responded to hair movement. Thus some gastrocnemius afferents seemed to have retained the adaptation properties characteristic of muscle afferents. Also surprisingly, given that the Gn contains fewer fibers than the Sn, receptive-field areas were not significantly different from regrown or normal sural fibers.(ABSTRACT TRUNCATED AT 400 WORDS)

1975 ◽  
Vol 38 (3) ◽  
pp. 572-586 ◽  
Author(s):  
A. E. Applebaum ◽  
J. E. Beall ◽  
R. D. Foreman ◽  
W. D. Willis

A technique is described for recording from axons belonging to the spinothalamic tract of the monkey. The axons arose from cell bodies located within the spinal cord since the latency of orthodromic activation by afferents within the dorsal funiculus was short. The axons were antidromically activated from the ipsilateral diencephalon. The spectrum of conduction velocities indicates that the recordings favored large-diamter axons. However, all of the classes of spinothalamic tract units described from soma-dendritic recordings were represented in the sample. When the locations of the axons in the ventrolateral white matter were mapped, there was virtually complete overlap in the distributions of hair-activated, low-, and high-threshold spinothalamic tract axons, suggesting that the "lateral spinothalamic tract" conveys tactile, as well as pain and temperature, information. The only segregated population of axons were those belonging to units activated by receptors in deep tissues, including muscle. These were in a band along the ventral surface of the cord. The stimulus points for antidromically activating spinothalamic cells of axons were in the known diencephalic course of the spinothalamic tract, including the ventral posterior lateral nucleus. Stimulus point locations were similar for high-threshold and other categories of units. Receptive-field sizes were smaller for high-threshold spinothalamic cells or axons than for hair-activated or low-threshold units. Receptive-field size was correlated with position on the hindlimb. The smallest fields belonged to cells in lamina I, with progressively larger sizes for cells in laminae IV and V. Receptive-field shape was evaluated by the length/width ratio, which was smallest for high-threshold units and progressively larger for low-threshold and hair-activated units. The receptive-field positions of spinothalamic tract axons were related to the locations of the axons. There was a rough somatotopic representation in the tract, with the most caudal dermatomes represented dorsolaterally, and the most rostral ventromedially.


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)


2017 ◽  
Vol 117 (4) ◽  
pp. 1608-1614 ◽  
Author(s):  
Roger H. Watkins ◽  
Johan Wessberg ◽  
Helena Backlund Wasling ◽  
James P. Dunham ◽  
Håkan Olausson ◽  
...  

C-mechanoreceptors in humans comprise a population of unmyelinated afferents exhibiting a wide range of mechanical sensitivities. C-mechanoreceptors are putatively divided into those signaling gentle touch (C-tactile afferents, CTs) and nociception (C-mechanosensitive nociceptors, CMs), giving rise to positive and negative affect, respectively. We sought to distinguish, compare, and contrast the properties of a population of human C-mechanoreceptors to see how fundamental the divisions between these putative subpopulations are. We used microneurography to record from individual afferents in humans and applied electrical and mechanical stimulation to their receptive fields. We show that C-mechanoreceptors can be distinguished unequivocally into two putative populations, comprising CTs and CMs, by electrically evoked spike latency changes (slowing). After both natural mechanical stimulation and repetitive electrical stimulation there was markedly less latency slowing in CTs compared with CMs. Electrical receptive field stimulation, which bypasses the receptor end organ, was most effective in classifying C-mechanoreceptors, as responses to mechanical receptive field stimulation overlapped somewhat, which may lead to misclassification. Furthermore, we report a subclass of low-threshold CM responding to gentle mechanical stimulation and a potential subclass of CT afferent displaying burst firing. We show that substantial differences exist in the mechanisms governing axonal conduction between CTs and CMs. We provide clear electrophysiological “signatures” (extent of latency slowing) that can be used in unequivocally identifying populations of C-mechanoreceptors in single-unit and multiunit microneurography studies and in translational animal research into affective touch. Additionally, these differential mechanisms may be pharmacologically targetable for separate modulation of positive and negative affective touch information. NEW & NOTEWORTHY Human skin encodes a plethora of touch interactions, and affective tactile information is primarily signaled by slowly conducting C-mechanoreceptive afferents. We show that electrical stimulation of low-threshold C-tactile afferents produces markedly different patterns of activity compared with high-threshold C-mechanoreceptive nociceptors, although the populations overlap in their responses to mechanical stimulation. This fundamental distinction demonstrates a divergence in affective touch signaling from the first stage of sensory processing, having implications for the processing of interpersonal touch.


1991 ◽  
Vol 66 (4) ◽  
pp. 1218-1231 ◽  
Author(s):  
G. R. Lewin ◽  
S. B. McMahon

1. We have studied the physiology of primary sensory neurons innervating rat hindlimb muscle in the following: 1) normal control animals; 2) animals in which the gastrocnemius nerve (Gn) had regenerated to its original muscle target; and 3) animals in which the cutaneous sural nerve (Sn) had regenerated to a foreign target, muscle. 2. Single-unit recordings were made from 115 afferents in normal, intact animals. They had conduction velocities of 0.8-67.2 m/s, which were distributed with peaks at approximately 1.25, 17.5, and 47.5 m/s. Of the myelinated fibers, 88% had low-threshold mechanosensitive receptive fields and responded to ramp-and-hold stretches of the muscle. The large majority of these fibers (85%) gave slowly adapting responses to ramp-and-hold stretches or direct muscle probing. Stretch-sensitive afferents could be divided (on the basis of their responses to active muscle contraction) into in-parallel or in-series receptors (presumed muscle spindles and Golgi tendon organs, respectively). The in-parallel receptors outnumbered the in-series receptors by approximately 3:2. The 12% of fibers that were insensitive to stretches of the muscle in the physiological range could be divided into roughly equal groups of totally insensitive fibers and high-threshold fibers, which required excessive stretching of the muscle. 3. In the animals with regrown Gn, 94 single fibers with conduction velocities ranging from 11 to 60.6 m/s were studied. The myelinated conduction velocity distribution exhibited only one peak, at approximately 37.5 m/s. Only 67% of the afferents were stretch sensitive (vs. 88% in normal animals), and only about two-thirds of these (vs. 85% in normal animals) gave slowly adapting responses to ramp-and-hold stretches or muscle probing. The incidence of in-series receptors was also increased among regenerated gastrocnemius afferents. The 33% of fibers that were stretch insensitive were mostly unresponsive to even extreme forms of mechanical stimuli. This group presumably represents afferents that failed to make appropriate endings. 4. In the animals with Sn directed to muscle, 460 single afferents were recorded. Their conduction velocities ranged from 0.7 to 67.9 m/s, and the distribution exhibited only a single peak for myelinated fibers at approximately 22.5 m/s, significantly lower than for intact or regrown Gn. Only 41% of the myelinated fibers were stretch sensitive. Nearly all of these (98%) were rapidly adapting to ramp-and-hold stretches or muscle probing, in marked contrast to the other groups. Also, unlike other groups, nearly all stretch-sensitive afferents appeared to be in-series.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 72 (2) ◽  
pp. 883-889 ◽  
Author(s):  
D. A. Simone ◽  
P. Marchettini ◽  
G. Caputi ◽  
J. L. Ochoa

1. Intraneural microstimulation (INMS) and microneurography were used in combination to stimulate and record from muscle nociceptor primary afferent fibers of the common peroneal nerve of healthy volunteers. When pain evoked by INMS was projected to muscle, afferent activity could be evoked by innocuous and noxious pressure applied within the projected painful area. Conduction velocity of single fibers was determined by stimulating the receptive fields (RFs) electrically via needle electrodes inserted into the RF and measuring conduction latency and distance between the RF and recording electrode. 2. Pain projected to muscle during INMS trains 5–10 s in duration at threshold intensity for pain sensation was typically described as cramping and was well localized. Subjects mapped the area of the painful projected field (PF) over the skin using a pointer. 3. Fourteen slowly adaping mechanoreceptors with RF in muscle and with moderate to high receptor threshold were identified within or near the painful PF. Conduction velocities were in the range of Group III (n = 8) and Group IV (n = 6) fibers. Mean RF areas of Group III and Group IV afferents, determined by applying pressure percutaneously, were 2.71 +/- 1.14 (SE) cm2 and 3.40 +/- 1.08 (SE) cm2, respectively. Only one Group III afferent unit exhibited spontaneous activity (< 1 Hz). 4. One additional high-threshold mechanoreceptor was identified, with its RF located in the extensor tendon at the base of the big toe. This fiber had a conduction velocity of 32 m/s. During INMS, a well-localized sharp pain was projected to the tendon.(ABSTRACT TRUNCATED AT 250 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.


1986 ◽  
Vol 55 (1) ◽  
pp. 56-75 ◽  
Author(s):  
K. A. Olsson ◽  
K. Sasamoto ◽  
J. P. Lund

Eighty-one sensory neurons in the rostral trigeminal sensory nuclei (main sensory nucleus, nucleus oralis, and the lateral border zone of the motor nucleus) were recorded in urethan-anesthetized rabbits before and during mastication. Receptive-field characteristics were described, and responses evoked by electrical stimulation of the inferior alveolar and infraorbital nerves, sensorimotor cortex, and thalamus were recorded. Forty-four percent of neurons were stimulated by the movements of mastication; nevertheless, evidence is presented that the excitability of the 49 neurons that receive low-threshold mechanoreceptor inputs is depressed during mastication for the following reasons: The spontaneous activity of seven cells was inhibited during movement. The probability of firing in response to stimulation of the peripheral nerve on sensorimotor cortex was decreased during mastication. There was usually a corresponding increase in the latency of the action potentials. Injections of local anesthetic (prilocaine hydrochloride, 4%) into the receptive field of the neuron did not prevent the decrease in excitability during mastication. Fourteen neurons that received inputs from periodontal pressoreceptors were recorded medial to most of the low-threshold group. The excitability of six of these was reduced during jaw closure and during the occlusal phase of movement, that is, within the period in which they would be activated by pressure on the teeth. The rest were tonically suppressed. Eighteen neurons recorded in the lateral border zone of the motor nucleus had receptive fields that were of high threshold or were undefined. They responded to stimulation of the peripheral nerve at high threshold. The excitability of most of these neurons was strongly phase modulated during mastication. They were most excitable during jaw closure or during the occlusal phase of movement and inexcitable during opening. The excitability of the others was tonically depressed. In most cases, the changes in excitability described did not seem to be due to the patterns of activity of the neurons that were generated by the movements. We conclude that the pattern elaborated by the central pattern generator includes selective modifications of sensory transmission. One reason for this is to suppress reflex responses to low-threshold inputs while maintaining the protective response to tissue damage.


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)


2000 ◽  
Vol 83 (3) ◽  
pp. 1722-1732 ◽  
Author(s):  
Amy M. Ritter ◽  
C. Jeffery Woodbury ◽  
Kathryn Albers ◽  
Brian M. Davis ◽  
H. Richard Koerber

In the rodent, cutaneous sensory neurons mature over the first two postnatal weeks, both in terms of their electrical properties and their responses to mechanical stimulation of the skin. To examine the coincidence of these events, intracellular recordings were made from neurons in the dorsal root ganglion (DRG) in an in vitro spinal cord, DRG, and skin preparation from mice between the ages of postnatal day 0 and 5 ( P0–P5). We also examined mice in which nerve growth factor (NGF) is overexpressed in the skin. NGF has been shown to be involved in a number of aspects of sensory neuron development and function. Therefore we ask here whether excess target-derived NGF will alter the normal course of development, either of somal membrane properties, physiological response properties, or neuropeptide content. In wild-type mice, somal action potentials (APs) were heterogeneous, with some having simple, uninflected falling phases and some displaying an inflection or break on the falling limb. The proportion of neurons lacking an inflection increased with increasing age, as did mean conduction velocity. A variety of rapidly and slowly adapting responses could be obtained by gently probing the skin; however, due to relatively low thresholds and firing frequencies, as well as lack of mature peripheral receptors such as hairs, it was not possible to place afferents into the same categories as in the adult. No correlation was seen between the presence or absence of an inflection on the somal AP (a marker for high-threshold mechanoreceptors in adult animals) and either peripheral threshold or calcitonin-gene related peptide (CGRP) content. Small differences in the duration and amplitude of the somal AP were seen in the NGF-overexpressing mice that disappeared by P3–P5. Excess target-derived NGF did not alter physiological response properties or the types of neurons containing CGRP. The changes that did occur, including a loss of the normal relationship between AP duration and conduction velocity, and a decrease in mean conduction velocity in the inflected population, might best be explained by an increase in the relative proportions of myelinated nociceptors. Of greatest interest was the finding that in both NGF overexpressers and wild-type mice, the correlation between mechanical threshold and presence or absence of an inflection on the somal spike is not apparent by P5.


1998 ◽  
Vol 15 (6) ◽  
pp. 1145-1155 ◽  
Author(s):  
D.-J. OH ◽  
D.P.M. NORTHMORE

After being severed, optic axons in goldfish regenerate and eventually restore the retinotectal map; refinement of the map depends upon impulse activity generated by the ganglion cells. Because little is known about the changes in activity and receptive-field properties of ganglion cells during regeneration, we made extracellular recordings from them in the intact eye up to 95 days after sectioning their axons in the optic tract. Their receptive fields were classified as OFF-, ON–OFF-, or ON-centers, and their axonal conduction velocities measured by antidromic activation. The rate of encountering single units dropped drastically at 4–8 days postsection when only a few OFF-center units could be recorded, recovering to normal between 42 and 63 days. Receptive-field centers were normal in size, except for the few OFF-centers at 4–8 days which were abnormally large. Maintained discharge rates of all types were depressed up to 42 days, but ON–OFF-center units were more spontaneously active than normal around 42 days. Light-evoked responses in OFF-center units were subnormal at 4–8 days, becoming supernormal at 16 days and normal thereafter. ON–OFF- and ON-center units started to regain responsiveness at 16 days, and became supernormal at 42 days, before returning to normal. Conduction velocities of all fiber groups dropped to a minimum at 8 days, the fastest being affected most. There was a gradual recovery to normal conduction velocity by 63 days. The conduction latencies of OFF- and ON–OFF-center units recovered to normal by 42 days, and ON-center units by 63 days. Recovery of ganglion cell responsiveness correlates with functional recovery in the retinotectal system: OFF-center units recover light-evoked responses at about the time OFF activity first reappears in the tectum. ON- and ON–OFF-center units recover later, exhibiting supernormal spiking activity around the time that ON responses reappear in the tectum.


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