Slowly Adapting Afferents Research Articles

Tactile sensitivity in the rat: a correlation between receptor structure and function

Single cutaneous fibers were recorded in the median nerve of the deeply anesthetized rat and the receptor morphology in the forelimb glabrous skin was analyzed to establish a probable correlation between receptor anatomy and physiology. Receptor complexes in the glabrous skin of the rat forelimb were stained immunologically with antibodies NF-200 and PGP-9.5, confirming the presence of Meissner corpuscles and Merkel complexes within the dermal papilla similar to other mammals including primates. Both the Meissner corpuscles and Merkel cell complexes were sparse and located in the pyramidal-shaped palmer pads and the apex of the digit extremities. They were almost totally absent elsewhere in the glabrous skin. No Ruffini receptors or Pacinian corpuscles were found in our samples. A total of 92 cutaneous fibers were retained long enough for analysis. Thirty-five (38%) were characterized as rapidly adapting fibers (RA) and 57 (62%) were slowly adapting afferents (SA). Despite the very limited number of receptors at the tip of the digit, RA receptors outnumbered SA fibers 3.2/1.0. In contrast, SA fibers on the thenar pad outnumbered RA receptors by a ratio of 3–1. Despite the very limited number of low threshold mechanoreceptors in the glabrous skin of the rat forelimb, the prevalence of SA afferents in the palm and more frequent occurrence of RA afferents in the digit extremity suggest differences in functionality both for locomotion and object manipulation.

Fast-adapting mechanoreceptors are important for force control in precision grip but not for sensorimotor memory.

Sensory feedback from cutaneous mechanoreceptors in the fingertips is important in effective object manipulation, allowing appropriate scaling of grip and load forces during precision grip. However, the role of mechanoreceptor subtypes in these tasks remains incompletely understood. To address this issue, psychophysical tasks that may specifically assess function of type I fast-adapting (FAI) and slowly adapting (SAI) mechanoreceptors were used with object manipulation experiments to examine the regulation of grip force control in an experimental model of graded reduction in tactile sensitivity (healthy volunteers wearing 2 layers of latex gloves). With gloves, tactile sensitivity decreased significantly from 1.9 ± 0.4 to 12.3 ± 2.2 μm in the Bumps task assessing function of FAI afferents but not in a grating orientation task assessing SAI afferents (1.6 ± 0.1 to 1.8 ± 0.2 mm). Six axis force/torque sensors measured peak grip (PGF) and load (PLF) forces generated by the fingertips during a grip-lift task. With gloves there was a significant increase of PGF (14 ± 6%), PLF (17 ± 5%), and grip and load force rates (26 ± 8%, 20 ± 8%). A variable-weight series task was used to examine sensorimotor memory. There was a 20% increase in PGF when the lift of a light object was preceded by a heavy relative to a light object. This relationship was not significantly altered when lifting with gloves, suggesting that the addition of gloves did not change sensorimotor memory effects. We conclude that FAI fibers may be important for the online force scaling but not for the buildup of a sensorimotor memory.

Tangential torque tunes touch

Tangential torque tunes touch

GABA and glycine in synaptic microcircuits associated with physiologically characterized primary afferents of cat trigeminal principal nucleus

Previous studies suggest that sensory information conveyed through trigeminal afferents is more strongly controlled at the level of the first synapse by GABA-mediated presynaptic mechanisms in the trigeminal principal sensory nucleus (Vp) than other sensory nuclei. However, it is unknown if such a mechanism is common to functionally different classes of primary afferent in the same nucleus or across the nuclei. To address these issues, the present study focused on synaptic microcircuits associated with slowly adapting (SA) mechanosensory afferents innervating the periodontal ligaments in the cat Vp and attempted to examine GABA, glycine, and glutamate immunoreactivity in axon terminals involved in the circuits. Afferents were physiologically characterized before injection of horseradish peroxidase (HRP) and preparation for electron microscopy. HRP-labeled afferent boutons were serially sectioned and immunostained with antibodies against GABA, glycine, and glutamate using a postembedding immunogold method. All the afferent boutons examined contacted non-primary dendrites and they were frequently postsynaptic to unlabeled axons (p-endings). Axodendritic and axoaxonic contacts per afferent bouton were 1.3 (46/35) and 2.0 (70/35), respectively. Most p-endings were immunoreactive for GABA (63/70) and also glycine was co-stained in the majority of the p-endings (49/63). Thirty percent of p-endings with the colocalization of GABA and glycine participated in synaptic triads where a p-ending formed a synapse with the same dendrite as the afferent bouton. None of the p-endings was immunoreactive for glutamate. Most afferent boutons were enriched with glutamate but were immunonegative for GABA and glycine. This study provides evidence suggesting that transmission from SA afferents is strongly controlled presynaptically by GABAergic interneurons with colocalized glycine, and that a proportion of these interneurons, involved in synaptic triads, may also have postsynaptic inhibitory actions on target neurons of the SA afferents.

Morphological differences between fast and slowly adapting lingual afferent terminations in the principal and oral nuclei in the cat.

Previous studies indicated that fast-adapting (FA) and slowly adapting (SA) mechanoreceptive afferents innervating the facial or intraoral structures give rise to morphologically distinct terminal arbors in the individual subdivisions of the trigeminal sensory nuclear complex. The present study examined the collateral morphologies of lingual afferents in the nuclei principalis (Vp) and oralis (Vo) of the cat. Seven FA and six SA lingual afferents were physiologically characterized and stained by the intra-axonal horseradish peroxidase (HRP) injection technique. The two types of afferents established terminal arbors in the dorsomedial subdivision (Vpd) of the Vp, and the rostrodorsomedial (Vo.r) and dorsomedial subdivisions (Vo.dm) of the Vo, but the collateral morphologies are different between the two types. The FA afferents gave rise to mediolaterally extended oblong arbors in each subdivision, but the arbors were better developed in the Vo.r than in the Vpd and Vo.dm. The number of collaterals, intercollateral distance, number of boutons per collateral, and bouton size were also different among the subdivisions. The SA afferents were divided into two subtypes; one had a preferential projection into the Vpd or the Vo.r and Vo.dm, and others lacked a selected projection. Although the shape of their arbors varied from a stringy form to a roundish form, the general profile was denser, better developed, and rounder than that of FA afferents in each subdivision. The intercollateral distance and bouton size were different among the subdivisions. The number of boutons per collateral, bouton density, and bouton size were larger in SA than FA afferents in each subdivision. The present study demonstrated that two functionally distinct lingual afferents manifest unique morphological differences in the Vpd and Vo.

Ultrastructural observations of synaptic connections of vibrissa afferent terminals in cat principal sensory nucleus and morphometry of related synaptic elements.

Previous work suggests that slowly adapting (SA) periodontal afferents have different synaptic arrangements in the principal (Vp) and oral trigeminal nuclei and that the synaptic structure associated with transmitter release may be related directly to bouton size. The present study examined the ultrastructures of SA and fast adapting (FA) vibrissa afferents and their associated unlabeled axonal endings in the cat Vp by using intra-axonal labeling with horseradish peroxidase and a morphometric analysis. All SA and FA afferent boutons contained clear, round, synaptic vesicles. All the FA and most SA boutons were presynaptic to dendrites, but a few SA boutons were axosomatic. Both types of bouton were frequently postsynaptic to unlabeled axonal ending(s) containing pleomorphic, synaptic vesicles (P-ending). The size of labeled boutons was larger in FA than SA afferents, but the size of dendrites postsynaptic to labeled boutons was larger for SA than FA afferents. Large-sized FA and SA boutons made synaptic contacts with small-diameter dendrites. The size of FA and SA boutons was larger than that of their associated P-endings. A morphometric analysis made on the pooled data of SA and FA boutons indicated that apposed surface area, active zone number, total active zone area, vesicle number, and mitochondrial volume were highly correlated in a positive linear manner with labeled bouton volume. These relationships were also applicable to unlabeled P-endings, but the range of each parameter was smaller than that of the labeled boutons. These observations provide evidence that the two functionally distinct types of vibrissa afferent manifest unique differences but share certain structural features in the synaptic organization and that the ultrastructural "size principle" proposed by Pierce and Mendell ([1993] J. Neurosci. 13:4748-4763) for Ia-motoneuron synapses is applicable to the somatosensory system.

Roughness coding in the somatosensory system

Roughness perception is coded in the somatosensory system by neurons in the type I slowly adapting (SAI) system. When the fingers scan a surface, an isomorphic representation of the surface is encoded in the discharge patterns of SAI afferents. Central neurons in area 3b of primary somatosensory (SI) cortex spatially filter the peripheral image to compute local spatial variation. The outputs from these neurons converge onto neurons in area 1 and onto neurons in secondary somatosensory (SII) cortex which we believe is the critical processing pathway underlying roughness perception.

Central terminations of periodontal mechanoreceptive and tooth pulp afferents in the trigeminal principal and oral nuclei of the cat

Intra-axonal recording and horseradish peroxidase (HRP) injection techniques were employed to define the response properties of low-threshold mechanoreceptive periodontal afferents and of the tooth pulp afferents and the morphological characteristics of their axon arbors in the nucleus principalis (Vp) and rostrodorsomedial (Vo.r) and dorsomedial parts (Vo.dm) of the nucleus oralis (Vo). The central terminals of 3 fast adapting (FA) and 4 slowly adapting (SA) periodontal afferents and 4 tooth pulp (TP) afferents were recovered for detailed analyses. Stained axons in the trigeminal sensory tract ascended and descended (bifurcating fibers), or descended without bifurcation (descending non-bifurcating fibers). The ratio of the bifurcating fibers to the descending non-bifurcating fibers was about three to one for each type of afferents. The main collaterals given off from the ascending branches terminated in the Vp. Most collaterals given off from the descending branches terminated in the Vo with the exception of few instances. In case of the FA afferents, the ascending branches gave off all main collaterals into the Vp with rostrocaudal and dorsoventral continuities in their arbors, whereas the descending branches gave off all main collaterals, except two collaterals, into the Vo with rostrocaudal discontinuities. The projections from the FA afferents to the Vo.dm was predominant in terms of the number of boutons and the length of preterminal and terminal branches. In case of the SA afferents, the collaterals from the ascending and descending branches formed rostrocaudally and dorsoventrally discontinuous terminal arbors. In terms of the density of boutons the SA afferents were divided into two subtypes. One had a preferential projection into the Vp or Vo, whereas others lacked a selective projection. In case of the TP afferents, the main collaterals of the ascending branches formed partially overlapping terminal arbors, but the terminal arbors formed by the collateral of the descending branches did not overlap. The frequency of collaterals of the TP afferents was less than of the other types of afferents. The terminal arbors including the density of boutons of the pulpal afferents were less extensive than those of the other types of afferents. The average size of varicosities became smaller in the following subdivisions, Vp, Vo.r and Vo.dm for SA and TP afferents. The size of varicosities of the TP afferents was smaller and that of the FA afferents was larger than that of the SA afferents. This study demonstrates that a distinctive morphology in the terminal arborizations has a good correlation with a functional segregation among the cytoarchitectonically different zones of the trigeminal sensory nuclear complex (TSNC).

Spatial and temporal factors determining afferent fiber responses to a grating moving sinusoidally over the monkey's fingerpad

Gratings of alternating grooves and ridges were moved sinusoidally across the fingerpads of anesthetized monkeys, while responses were recorded from individual slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs) in the median nerve. The stimulus comprised 2 spatial variables, namely, groove width (G) and ridge width (W), and 2 temporal variables, namely, the peak speed of movement (S) and the peak temporal frequency (F) at which successive spatial cycles of the grating pass over a point in the receptive field. The responses of all 3 fiber types were determined by only 1 spatial variable, G, and only 1 temporal variable, F. Changes in W or S affected responses only if there was a concomitant change in either G or F. Responses were phase-locked to the occurrence of successive spatial cycles of the grating, and we have used the number of impulses elicited by a single spatial cycle as the fundamental measure of response. An equation of the form I = cGaexp(-b square root of F) describes the responses of all 3 fiber types. For SAs, the effect of groove width was greater (a = 2.64) than for RAs and PCs (a = 0.924 and 1.05, respectively). The reduction in response with frequency was most marked for SAs (b = 0.262), and greater for PCs (b = 0.167) than for RAs (b = 0.130). From the equation, the instantaneous response during the entire sinusoidal cycle was reconstructed as well as a second measure, the mean cyclic response. These 2 measures behaved differently with changes in the stimulus parameters. The temporal properties of the fibers, as revealed by gratings, may appear to be in conflict with those established by vibratory threshold studies; in fact, they are compatible with suprathreshold responses to vibrating probes.

Perceived roughness of a grating: correlation with responses of mechanoreceptive afferents innervating the monkey's fingerpad

Human subjects scaled gratings of alternating grooves and ridges for perceived roughness. Roughness increased with an increase in groove width and decreased with an increase in ridge width, but the effect of groove width was much greater than the effect of ridge width. In corresponding neurophysiological experiments, the gratings were moved sinusoidally across the receptive fields of single mechano-receptive afferents innervating the fingerpads of anesthetized monkeys. The measure of response used was the mean cyclic discharge rate (averaged over one cycle of the sinusoid). Slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs) all showed a marked increase in response when groove width increased. An increase in ridge width had no consistent effect on the responses of SAs or RAs but resulted in a small decrease in the response of PCs. The response to a smooth surface differed significantly from the responses to the finer gratings only for the RAs. An alternative measure of response (the number of impulses elicited by each spatial cycle of the grating) increased with an increase in ridge width for all 3 fiber types. Thus, the large effect of groove width on perceived roughness can be accounted for by the mean cyclic discharge rate in the active afferent fibers. The smaller effect of ridge width can be accounted for by the number of impulses per spatial cycle of the grating.

Chapter 2 Segmental influence of slowly-adapting cutaneous mechanoreceptors on γ motoneurones revealed by cross-correlation of unit discharges in the cat

Cross-correlations between the discharges of individual cutaneous afferents and gamma motoneurones have been constructed in the spinal, decerebrated cat. The discharges of single receptors in the sural nerve field from the heel were recorded in dorsal root ganglia. Background discharges of gamma motoneurones and the responses to heel stimulation were recorded from cut filaments of the muscle nerve to gastrocnemius medialis of the same leg. Slowly-adapting afferents were stimulated by steady application of a probe to the receptive field whereas rapidly-adapting afferents required continuous movement to sustain discharge of a receptor. Cross-correlation between the discharges of 17 out of 39 slowly-adapting, type-1 (SA1) mechanoreceptors and gamma motoneurones revealed sharp increases in probability of gamma motoneurone discharge that were delayed with respect to the afferent discharge. The peaks were of short duration with widths at half maximum in the range 2-7 ms and rise times of 1 to 4 ms. Deducting peripheral conduction times gave central delays of 3-6.5 ms for gamma motoneurone facilitation. These delays were comparable to those of gamma motoneurone excitation seen in response to electrical stimulation of the sural nerve at 1.5 to 4 times threshold. No short duration peaks were seen in correlograms between hair follicle (n = 29) or slowly-adapting type-2 (SA2) (n = 11) afferents and gamma motoneurones. It is concluded that a single impulse from a SA1 afferent from the hairy skin of the heel is able to facilitate the discharge of gamma motoneurones to the ipsilateral gastrocnemius muscle.(ABSTRACT TRUNCATED AT 250 WORDS)

Sinusoidal movement of a grating across the monkey's fingerpad: temporal patterns of afferent fiber responses

Responses were recorded from cutaneous afferents innervating mechanoreceptors in the monkey's fingerpad, while gratings of alternating grooves and ridges were moved sinusoidally across their receptive fields. The gratings were specified by their spatial period and the movement by its peak speed: together these determined the peak temporal frequency at which grating ridges passed over the receptive field. During the central 42 degrees of each half cycle of movement, the speed and thus the temporal frequency of the grating ridges remained constant to within 6.6% of their peak values. In this region the responses of all afferents were phase-locked to the temporal sequence of grating ridges. The number of impulses elicited by each grating ridge was a function of the stimulus variables. For all 3 afferent classes--namely, slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs)--the number of impulses per grating ridge increased as the spatial period of the grating increased (while the peak speed of movement was held constant). Similarly, for all 3 classes, the number of impulses per ridge decreased as the peak speed of movement increased (while the spatial period of the grating remained constant). When the peak temporal frequency of the grating ridges was held constant, for SAs and RAs the number of impulses per ridge increased with an increase in the spatial period of the grating and thus with an increase in the peak speed. These phase-locked responses provided information about the peak temporal frequency of the grating ridges independent of the grating spatial period and of the peak speed of movement. The shape of the response profile during a half cycle of movement was different for different afferents. Many of the RA response profiles were close to sinusoidal. The SA and PC profiles tended to have reduced peaks or raised troughs, resulting in flatter profiles. Other departures from sinusoidal profiles were also seen.

Sinusoidal movement of a grating across the monkey's fingerpad: representation of grating and movement features in afferent fiber responses

Gratings of alternating grooves and ridges were moved sinusoidally back and forth across the monkey's fingerpad. Each grating was completely specified by its spatial period and the movement by its peak speed: together these determined the peak temporal frequency at which grating ridges passed over the skin. Responses of cutaneous, mechanoreceptive afferents innervating the fingerpad were characterized in terms of these 3 parameters. Slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs) had different characteristics. The responses (mean cyclic discharge rates) of the SAs increased when the spatial period of the grating increased (and peak speed of movement remained constant) but did not change with changes in the peak speed of the movement (while the spatial period of the grating remained constant). Conversely, the responses of the PCs increased when the peak speed of movement increased (and the spatial period remained constant) but were relatively insensitive to changes in the spatial period of the grating (while the peak speed remained constant). The responses of the RAs increased as the spatial period of the grating increased (and peak speed remained constant) and also increased as the peak speed of movement increased (and the grating spatial period remained constant). When the peak temporal frequency of the grating ridges was held constant, the responses of all 3 afferent groups changed with changes in the grating spatial period or in the peak speed of movement. Information about the spatial features of the grating, independent of the peak speed of movement, was present in the SA population response and in the ratios of the RA and PC population responses. Information about the peak speed of movement, independent of the spatial period of the grating, was present in the PC population response and could be extracted from the RA population response.

Sinusoidal movement of a grating across the monkey's fingerpad: effect of contact angle and force of the grating on afferent fiber responses

Responses were recorded from cutaneous afferents innervating mechanoreceptors in the monkey's fingerpad. When gratings of alternating grooves and ridges were moved sinusoidally back and forth across the receptive field, the responses of the afferent were often not equal for the 2 directions of movement. To investigate this phenomenon, the position of the center of the afferent's receptive field, relative to the contact area between the grating and the finger, was varied systematically. For some afferents, regardless of these relative positions, the response was always greater for a particular direction of movement. For other afferents, regardless of these relative positions, the responses for the 2 directions of movement were always equal. For a minority of afferents, the response was greater for movement in one particular direction for some relative positions and greater for movement in the opposite direction for other relative positions. Slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs) exhibited all 3 types of response patterns. We could not relate these patterns to the afferent type or to the positions, in the fingerpad, of the receptive field center. The contact force between the grating and the finger was varied by varying the contact displacement (indentation). Two grating spatial periods were used. For SAs and PCs the response increased with increasing indentation for both gratings. For RAs the response to the finer grating increased with increasing indentation, but the response to the coarser grating did not.