Properties of regenerated primary afferents and their functional connections

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.

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.


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. 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)


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.


1976 ◽  
Vol 39 (3) ◽  
pp. 613-630 ◽  
Author(s):  
W. Singer ◽  
F. Tretter

An attempt was made to relate the alterations of cortical receptive fields as they result from binocular visual deprivation to changes in afferent, intrinsic, and efferent connections of the striate and parastriate cortex. The experiments were performed in cats aged at least 1 jr with their eyelids sutured closed from birth.The results of the receptive-field analysis in A17 confirmed the reduction of light-responsive cells, the occasional incongruity of receptive-field properties in the two eyes, and to some extent also the loss of orientation and direction selectivity as reported previously. Other properties common to numerous deprived receptive fields were the lack of sharp inhibitory sidebands and the sometimes exceedingly large size of the receptive fields. Qualitatively as well as quantitatively, similar alterations were observed in area 18. A rather high percentage of cells in both areas had, however, preserved at least some orientation preference, and a few receptive fields had tuning properties comparable to those in normal cats. The ability of area 18 cells in normal cats to respond to much higher stimulus velocities than area 17 cells was not influenced by deprivation.The results obtained with electrical stimulation suggest two main deprivation effects: 1) A marked decrease in the safety factor of retinothalamic and thalamocortical transmission. 2) A clear decrease in efficiency of intracortical inhibition. But the electrical stimulation data also show that none of the basic principles of afferent, intrinsic, and efferent connectivity is lost or changed by deprivation. The conduction velocities in the subcortical afferents and the differentiation of the afferents to areas 17 and 18 into slow- and fast-conducting projection systems remain unaltered. Intrinsic excitatory connections remain functional; this is also true for the disynaptic inhibitory pathways activated preferentially by the fast-conducting thalamocortical projection. The laminar distribution of cells with monosynaptic versus polsynaptic excitatory connections is similar to that in normal cats. Neurons with corticofugal axons remain functionally connected and show the same connectivity pattern as those in normal cats. The nonspecific activation system from the mesencephalic reticular formation also remains functioning both at the thalamic and the cortical level.We conclude from these and several other observations that most, if not all, afferent, intrinsic, and efferent connections of areas 17 and 18 are specified from birth and depend only little on visual experience. This predetermined structural plan, however, allows for some freedom in the domain of orientation tuning, binocular correspondence, and retinotopy which is specified only when visual experience is possible.


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)


1986 ◽  
Vol 55 (1) ◽  
pp. 76-96 ◽  
Author(s):  
R. P. Yezierski ◽  
R. H. Schwartz

Recordings were made from 90 identified spinomesencephalic tract (SMT) cells in the lumbosacral spinal cord of cats anesthetized with alpha-chloralose and pentobarbital sodium. Recording sites were located in laminae I-VIII. Antidromic stimulation sites were located in different regions of the rostral and caudal midbrain including the periaqueductal gray, midbrain reticular formation, and the deep layers of the superior colliculus. Twelve SMT cells were antidromically activated from more than one midbrain level or from sites in the medial thalamus. The mean conduction velocity for the population of cells sampled was 45.2 +/- 21.4 m/s. Cells were categorized based on their responses to graded intensities of mechanical stimuli and the location of excitatory and/or inhibitory receptive fields. Four major categories of cells were encountered: wide dynamic range (WDR); high threshold (HT); deep/tap; and nonresponsive. WDR and HT cells had excitatory and/or inhibitory receptive fields restricted to the ipsilateral hindlimb or extending to other parts of the body including the tail, forelimbs, and face. Some cells had long afterdischarges following noxious stimulation, whereas others had high rates of background activity that was depressed by nonnoxious and noxious stimuli. Deep/tap cells received convergent input from muscle, joint, or visceral primary afferent fibers. The placement of mechanical lesions at different rostrocaudal levels of the cervical spinal cord provided information related to the spinal trajectory of SMT axons. Six axons were located contralateral to the recording electrode in the ventrolateral/medial or lateral funiculi while two were located in the ventrolateral funiculus of the ipsilateral spinal cord. Stimulation at sites used to antidromically activate SMT cells resulted in the inhibition of background and evoked responses for 22 of 25 cells tested. Inhibitory effects were observed on responses evoked by low/high intensity cutaneous stimuli and by the activation of joint or muscle primary afferent fibers. Based on the response and receptive-field properties of SMT cells it is suggested that the SMT may have an important role in somatosensory mechanisms, particularly those related to nociception.


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)


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.


1986 ◽  
Vol 55 (6) ◽  
pp. 1187-1201 ◽  
Author(s):  
W. E. Renehan ◽  
M. F. Jacquin ◽  
R. D. Mooney ◽  
R. W. Rhoades

In Nembutal-anesthetized rats, 31 physiologically identified medullary dorsal horn (MDH) cells were labeled with horseradish peroxidase (HRP). Ten responded only to deflection of one or more vibrissae. Six cells were activated by guard hair movement only, six by deflection of guard hairs or vibrissa(e), and seven by pinch of facial skin with serrated forceps. Different classes of low-threshold cells could not be distinguished on the basis of their somadendritic morphologies or laminar distribution. Neurons activated by multiple vibrissae were unique, however, in that one sent its axon into the medial lemniscus, and three projected into the trigeminal spinal tract. None of the guard hair-only or vibrissae-plus-guard hair neurons had such projections. Cells that responded best to noxious stimulation were located mainly in laminae I, II, and deep V, while neurons activated by vibrissa(e) and/or guard hair deflection were located in layers III, IV, and superficial V. Low-threshold neurons generally had fairly thick dendrites with few spines, whereas high-threshold cells tended to have thinner dendrites with numerous spines. Moreover, the dendritic arbors of low-threshold cells were, for the most part, denser than those of the noxious cells. Neurons with mandibular receptive fields were located in the dorsomedial portion of the MDH; cells with ophthalmic fields were found in the ventrolateral MDH, and maxillary cells were interposed. Cells sensitive to deflection of dorsal mystacial vibrissae and/or guard hairs were located ventral to those activated by more ventral hairs. Neurons with rostral receptive fields were found in the rostral MDH, while cells activated by hairs of the caudal mystacial pad, periauricular, and periorbital regions were located in the caudal MDH. Receptive-field types were encountered that have not been reported for trigeminal primary afferent neurons: multiple vibrissae; vibrissae plus guard hairs; and wide dynamic range. The latter two can be explained by the convergence of different primary afferent types onto individual neurons. Our failure to find a significant relationship between dendritic area (in the transverse plane) and the number of vibrissae suggests that primary afferent convergence may not be responsible for the synthesis of the multiple vibrissae receptive field. Excitatory connections between MDH neurons may, therefore, account for multiple vibrissae receptive fields in the MDH.


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