Modulation of transmission in rostral trigeminal sensory nuclei during chewing

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.

1989 ◽  
Vol 143 (1) ◽  
pp. 419-434
Author(s):  
B. A. Bannatyne ◽  
S. E. Blackshaw ◽  
M. McGregor

1. New growth in cutaneous mechanosensory neurones elicited by axotomy or axon crush was studied using intracellular injection of horseradish peroxidase at different times after the lesion, ranging from a few days to over a year. 2. Cutting or crushing major, large-calibre axon branches of mechanosensory neurones elicits sprouting of new processes, either centrally within the ganglion neuropile or at the site of the lesion in the peripheral nerve. In contrast, cutting or crushing fine-calibre axon branches supplying accessory parts of the receptive field does not elicit sprouting of the main arbor or main axon branches. 3. Different modalities of mechanosensory neurone respond differently to lesions of their axons. Cutting the axons of high-threshold units responding to noxious stimulation of the skin elicits sprouting of additional processes from the axon hillock region within the central nervous system (CNS), whereas cutting or crushing the axons of low-threshold cells responding to light touch of the skin elicits sprouting at the site of the lesion only, and not within the CNS. 4. In addition to the new growth directed into the peripheral nerve, damaged nociceptive neurones also form new processes that wrap the somata of particular cells within the ganglion. 5. Sprouted processes of axotomized neurones are retained for long periods after the lesion (up to 425 days). 6. The electrical properties of touch and nociceptive cells were studied between 1 and 60 days after axotomy, by intracellular recording from the centrally located cell bodies. The amplitude, width and maximum dV/dt of the action potential and after-hyperpolarization, as well as the resting potential and input resistance, did not change significantly after axotomy, despite the considerable process sprouting known to occur during this time.


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.


1980 ◽  
Vol 43 (6) ◽  
pp. 1673-1699 ◽  
Author(s):  
V. Golovchinsky

1. The responses of single cuneate neurons to controled mechanical stimulation of skin were recorded in cats lightly anesthetized with a nitrous oxide-halothane mixture. The discharge patterns and peripheral receptive-field characteristics were studied in neurons driven by sensitive cutaneous mechanoreceptors, including slowly adapting skin mechanoreceptors. Virtually all cuneate neurons display maximum discharge during the velocity component of displacement. 2. Among cuneate neurons encountered in this study, approximately 46% were driven by guard hair mechanoreceptors, 15% were driven by field receptors, and 13% were driven by slowly adapting skin receptors. Neurons responding to stimulation of deep tissues (including claws) were not studied with controlled mechanical stimulation and accounted for 19%. The rest of the neurons were driven by Pacinian corpuscles, received afferent inputs from several different first-order afferents, or were not definitely identified. There was no clear evidence of down hair or high-threshold mechanoreceptor representation. 3. The discharge pattern in response to a constant-velocity stimulus proved most valuable in describing submodality classes of neurons driven by hair and field receptors since sensitivity of these neurons to dynamic and to static phases of stimulation constitute respective continua and, thus, preclude sharp separation into distinct groups. 4. The majority of neurons displayed response properties and receptive fields similar to those of first-order afferents. A minority of cells had receptive fields that were larger than those of primary afferents, with nearly identical modality and velocity characteristics throughout the receptive field. 5. Approximately 2% of recorded neurons displayed convergent properties not encountered in first-order afferents, including neurons driven from receptors of different modalities or from discontinuous receptive fields. 6. Inhibition of neuronal firing generated from outside the receptive field was rarely seen, possibly due to anesthetic conditions. In a small number of neurons, irregularities in the discharge were observed that might indicate inhibitory influences originating from within the receptive field.


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)


1985 ◽  
Vol 54 (3) ◽  
pp. 491-501 ◽  
Author(s):  
V. K. Shea ◽  
E. R. Perl

The cutaneous receptive properties of unmyelinated (C) fibers of the rabbit's great auricular nerve were determined by single-unit recordings. The majority of C-fiber units could be excited by cutaneous stimulation, and such sensory units fell into three major categories on the basis of responses to mechanical and thermal stimulation of their cutaneous receptive fields: low-threshold mechanoreceptors, nociceptors, or specific thermoreceptors. The majority of afferent elements were nociceptive, and all nociceptors responded to strong mechanical stimulation. Three types of nociceptors could be distinguished by their responses to thermal stimuli. Polymodal nociceptors responded to heat with thresholds of 40-55 degrees C and typically displayed enhanced responses or sensitization after noxious heating of their receptive fields. High-threshold mechanoreceptors failed to respond promptly to heat before noxious cutaneous stimulation which, however, elicited subsequent back-ground activity or sensitivity to heat. A third type of nociceptor responded to cold but not to heat. Low-threshold mechanoreceptors were identified by their brisk responses to very gentle, slowly moving mechanical stimulation of their receptive fields, and were readily distinguished from any element classified as nociceptive by their lower mechanical thresholds. Rapid innocuous warming or cooling excited some of the low-threshold mechanoreceptors. Specific thermoreceptors, both warming and cooling types, were rare, insensitive to mechanical stimulation, and responded to very slight changes in temperature. In contrast to the sensitization to heat, which was characteristic of most nociceptors, specific warming receptors displayed depressed thermal responses after noxious heating of their receptive fields. These results provide further evidence of the similarity of C-fiber receptors innervating hairy skin of different species. Some differences from past reports and additional features are described.


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.


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.


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)


1980 ◽  
Vol 238 (1) ◽  
pp. R57-R64 ◽  
Author(s):  
J. Ciriello ◽  
F. R. Calaresu

Experiments were done in cats anesthetized with chloralose, paralyzed and artificially ventilated cats to obtain electrophysiological evidence on the medullary site of origin of vagal cardioinhibitory fibers. The regions of the nucleus ambiguus (AMB), dorsal motor nucleus of the vagus (DMV), nucleus tractus solitarius (NTS), and external cuneate nucleus (ECN) were systematically explored for units responding both to antidromic stimulation of the cardiac branches of the vagus (CBV) and to orthodromic stimulation of the carotid sinus and aortic depressor nerves. Eighty-six single units conforming to these criteria were found in the medulla: 30 in the AMB, 26 in the DMV, 12 in the NTS, 8 in the NTS-DMV border region, and 10 in the ECN. Antidromically evoked spikes had durations of 0.5--2.5 ms and followed stimulation frequencies of 20--500 Hz. The axons of these units conducted at velocities of 3.3--20.8 m/s. The specificity of activation of medullary units by cardioinhibitory fibers was tested in 11 units, which were found to respond consistently with an antidromic spike to stimulation of CBV but not to stimulation of the thoracic vagus. In eight spinal animals low threshold (less than 15 microA) sites eliciting vagal bradycardia were found in the same medullary nuclei where cardioinhibitory units had been located. These results indicate that vagal cardioinhibitory axons, originate in at least three medullary nuclei, the AMB, DMV, and NTS. Unit activity from the ECN may have been recorded from carioinhibitory fibers because of the short duration of the spike potentials.


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