Organization and receptive fields of primate spinothalamic tract neurons

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.

1995 ◽  
Vol 74 (5) ◽  
pp. 2065-2076 ◽  
Author(s):  
H. R. Koerber ◽  
P. B. Brown

1. To test the hypothesis that subtotal deafferentation of dorsal horn cells can stimulate plastic changes in their receptive fields (RFs), diffuse deafferentation of the cat hindlimb dorsal horn was produced by transection of L7 or L6 and L7 dorsal roots. The following single-unit cutaneous low-threshold mechanoreceptor RF properties were compared between operated and control dorsal horns: 1) distance of RF center from tips of toes, 2) RF length-width ratio; and 3) RF area. 2. In both L7 and L6-L7 rhizotomized animals there was an increased incidence of silent electrode tracks in the most deafferented portion of the hindlimb map (the foot and toe representation). In the rhizotomized L6-L7 animals, there was also an increased incidence of symmetrically placed tracks in deafferented and control dorsal horns, in which cell RFs had no mirror-symmetrical components. In addition, cells in the lateral half of the L6 and L7 dorsal horns exhibited a proximal shift in the location of their RFs. In the rhizotomized L7 animals there was a distal shift of RFs in the L5 segment at long survival times. RFs had lower length-width ratios in L5 and L6 at short survival times and in L6 at long survival times. 3. In intact preparations, dorsal horn cells normally respond to inputs via single or small numbers of low-threshold cutaneous mechanoreceptors. Because these rhizotomies do not remove all inputs from any given area of skin, the deafferentations would produce only patchy loss of input from individual receptors. Therefore observed changes cannot be accounted for entirely by loss of afferent input, suggesting that some reorganization of dorsal horn cell RFs occurred. We conclude that the threshold stimulus for plastic change is less than total deafferentation of dorsal horn cells. At least some of the mechanisms underlying these changes may be active in normal animals in the maintenance of the somatotopic map or in conditioning.


1978 ◽  
Vol 41 (2) ◽  
pp. 260-267 ◽  
Author(s):  
P. B. Brown ◽  
H. R. Koerber

1. Single-unit recording from dorsal root ganglia was used to determine the dermatomes of L4-S2 segments in the cat. Dermatomes for low-threshold myelinated mechanoreceptor afferents are smaller than those reported in earlier studies of whole-root dermatomes. There are also sufficient discrepancies among earlier studies and with the present data to merit reexamination of hindlimb whole-root dermatomes. 2. Receptive-field size varies directly with distance from toes. Length/width ratio is essentially constant for different parts of the hindlimb. 3. Estimates of innervation density verify the long-standing assumption that innervation density is greater for foot and toes than for proximal hindlimb, at least for low-threshold cutaneous myelinated afferents.


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)


1987 ◽  
Vol 57 (3) ◽  
pp. 835-868 ◽  
Author(s):  
R. Desimone ◽  
S. J. Schein

Area V4, a visuotopically organized area in prestriate cortex of the macaque, is the major source of visual input to the inferior temporal cortex, known to be crucial for object recognition. To examine the selectivity of cells in V4 for stimulus form, we quantitatively measured the responses of 322 cells to bars varying in length, width, orientation, and polarity of contrast, and sinusoidal gratings varying in spatial frequency, phase, orientation, and overall size. All of the cells recorded in V4 were located on the lower portion of the prelunate gyrus. Receptive fields were located almost exclusively within the representation of the central 5 degrees of the lower visual field, and receptive field size, in linear dimension, was 4-7 times greater than that in the corresponding representation of striate cortex (V1). Nearly all receptive fields consisted of overlapping dark and light zones, like “classic” complex fields in V1, but the relative strengths of the dark and light zones often differed. A few cells responded exclusively to light or dark stimuli. Many cells in V4 were selective for stimulus orientation, and a few were selective for direction of motion as well. Although the median orientation bandwidth of the orientation-selective cells (52 degrees) was wider than that reported for oriented cells in V1, approximately 8% of the oriented cells had bandwidths of less than 30 degrees, which is nearly as narrow as the most narrowly tuned cells in V1. The proportion of cells selective for direction of motion (13%) was not markedly different from that reported in V1. The large majority of V4 cells were tuned to the length and width of bars, and the “shape” of the optimal bar varied from cell to cell, as has been reported for cells in the dorsolateral visual area (DL) of the owl monkey, a possible homologue of V4 in the macaque. Preferred lengths and widths varied independently from approximately 0.05 to 6 degrees, with the smallest preferred bars about the size of the smallest receptive fields in V1 and the largest preferred bars larger than any fields in V1. The relationship between the size of the optimal bar and the size of the receptive field varied from cell to cell. Some cells, for example, responded best to bars much narrower or shorter than the field, whereas other cells responded best to bars that filled (but did not extend beyond) the excitatory field in the length, width, or both dimensions.(ABSTRACT TRUNCATED AT 400 WORDS)


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

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


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.


1993 ◽  
Vol 90 (23) ◽  
pp. 11142-11146 ◽  
Author(s):  
S Bisti ◽  
C Trimarchi

Prenatal unilateral enucleation in mammals causes an extensive anatomical reorganization of visual pathways. The remaining eye innervates the entire extent of visual subcortical and cortical areas. Electrophysiological recordings have shown that the retino-geniculate connections are retinotopically organized and geniculate neurones have normal receptive field properties. In area 17 all neurons respond to stimulation of the remaining eye and retinotopy, orientation columns, and direction selectivity are maintained. The only detectable change is a reduction in receptive field size. Are these changes reflected in the visual behavior? We studied visual performance in cats unilaterally enucleated 3 weeks before birth (gestational age at enucleation, 39-42 days). We tested behaviorally the development of visual acuity and, in the adult, the extension of the visual field and the contrast sensitivity. We found no difference between prenatal monocularly enucleated cats and controls in their ability to orient to targets in different positions of the visual field or in their visual acuity (at any age). The major difference between enucleated and control animals was in contrast sensitivity:prenatal enucleated cats present a loss in sensitivity for gratings of low spatial frequency (below 0.5 cycle per degree) as well as a slight increase in sensitivity at middle frequencies. We conclude that prenatal unilateral enucleation causes a selective change in the spatial performance of the remaining eye. We suggest that this change is the result of a reduction in the number of neurones with large receptive fields, possibly due to a severe impairment of the Y system.


2005 ◽  
Vol 93 (6) ◽  
pp. 3537-3547 ◽  
Author(s):  
Chong Weng ◽  
Chun-I Yeh ◽  
Carl R. Stoelzel ◽  
Jose-Manuel Alonso

Each point in visual space is encoded at the level of the thalamus by a group of neighboring cells with overlapping receptive fields. Here we show that the receptive fields of these cells differ in size and response latency but not at random. We have found that in the cat lateral geniculate nucleus (LGN) the receptive field size and response latency of neighboring neurons are significantly correlated: the larger the receptive field, the faster the response to visual stimuli. This correlation is widespread in LGN. It is found in groups of cells belonging to the same type (e.g., Y cells), and of different types (i.e., X and Y), within a specific layer or across different layers. These results indicate that the inputs from the multiple geniculate afferents that converge onto a cortical cell (approximately 30) are likely to arrive in a sequence determined by the receptive field size of the geniculate afferents. Recent studies have shown that the peak of the spatial frequency tuning of a cortical cell shifts toward higher frequencies as the response progresses in time. Our results are consistent with the idea that these shifts in spatial frequency tuning arise from differences in the response time course of the thalamic inputs.


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.


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