Precision and variability of hindlimb representation in cat dorsal horn and implications for tactile localization

1993 ◽  
Vol 70 (6) ◽  
pp. 2489-2501 ◽  
Author(s):  
H. R. Koerber ◽  
G. Hobbs ◽  
P. B. Brown

1. One hundred fifty-eight cells were recorded extracellularly in rows of tracks spanning both left and right dorsal horns, at segmental boundaries and midsegment in segments L5-S1, in six anesthetized cats. For each cell the low-threshold cutaneous mechano-receptive field was determined with the use of hand-held probes, and the recording site was marked with a microlesion. Recording sites were reconstructed, and the mediolateral (ML) and rostrocaudal (RC) locations of each cell were recorded along with the location of the cell's receptive field, expressed as distance from tips of toes (D). 2. Ninety-five percent of pairs of cells recorded from bilaterally symmetric locations (+/- 10%) in the same animal had receptive fields on opposite legs that had components that were mirror symmetric. Only 42% of cell pairs deviating from bilateral symmetry by approximately +/- 240 microns had receptive fields with overlapping components. This indicated that there was a substantial bilateral symmetry that was not simply due to large receptive fields. 3. The trajectories of receptive fields of cells in a single row of tracks were plotted in order of mediolateral recording site, going from medial to lateral, combining both sides. These trajectories followed a distoproximal course on the leg. Of 144 adjacent cells used to plot these trajectories, with an average spacing of approximately 120 microns, only 6 reversals of the distoproximal gradient polarity were observed within animals. 4. Data from individual animals were shifted rostrally and caudally, to obtain best agreement of mediolateral somatotopic gradients with the combined data from the other animals in the sample. Best agreement was obtained with shifts ranging from 0.3 segment rostral to 0.4 segment caudal, with an average absolute value shift of 0.22 segment. 5. By comparing cell pairs within the same dorsal horn, on opposite sides of the same animal, and across animals, variability in cell placement given the average map and the receptive field could be calculated. Interanimal variability and bilateral asymmetry were approximately +/- 60 microns, and within-dorsal horn variability was approximately +/- 35 microns. The interanimal variability is equivalent to a variability of distoproximal receptive-field location on the leg of +/- 13 mm, with a smaller variability in areas of high magnification (e.g., the toes), and a larger variability in areas with small magnification (e.g., the thigh). This degree of variability is consistent with the ability of animals with transected dorsal columns to localize tactile stimuli with a normal degree of precision.

1982 ◽  
Vol 48 (2) ◽  
pp. 481-489 ◽  
Author(s):  
H. R. Koerber ◽  
P. B. Brown

1. The dorsal horn lamina III-IV projections of 10 hindlimb nerves innervating most of the hindlimb have been studied in the cat using transganglionic transport of horseradish peroxidase (HRP). The somatotopic organization of whole cutaneous nerve projections was largely in register with the somatotopic organization of dorsal horn cells. That is, nerves projected to areas of dorsal horn where their innervation fields overlap the receptive fields of dorsal horn cells. 2. However, long-ranging projections were observed that were more extensive than predicted from the somatotopy of dorsal horn cells: these long-ranging projections may reflect the presence of normally ineffective synapses (synapses that do not cause postsynaptic discharge during receptive-field mapping of dorsal horn cells,) or a misconception of dorsal horn cell somatotopy in S2 and caudal segments, or the existence of a functionally separate cell group in ventral lamina IV and lamina V of these segments. 3. The cutaneous innervation fields of homologous nerves possessed high bilateral symmetry, as did their lamina III-IV projection fields. The degree of separation or overlap of two cutaneous nerves' projection fields was predictable from the degree of separation or overlap of their cutaneous innervation fields.


1979 ◽  
Vol 42 (4) ◽  
pp. 954-974 ◽  
Author(s):  
S. C. Rosen ◽  
K. R. Weiss ◽  
I. Kupfermann

1. The cells of two clusters of small neurons on the ventrocaudal surface of each hemicerebral ganglion of Aplysia were found to exhibit action potentials following tactile stimuli applied to the skin of the head. These neurons appear to be mechanosensory afferents since they possess axons in the nerves innervating the skin and tactile stimulation evokes spikes with no prepotentials, even when the cell bodies are sufficiently hyperpolarized to block some spikes. The mechanosensory afferents may be primary afferents since the sensory response persists after chemical synaptic transmission is blocked by bathing the ganglion and peripheral structures in seawater with a high-Mg2+ and low-Ca2+ content. 2. The mechanosensory afferents are normally silent and are insensitive to photic, thermal, and chemical stimuli. A punctate tactile stimulus applied to a circumscribed region of skin can evoke a burst of spikes. If the stimulus is maintained at a constant forces, the mechanosensory response slowly adapts over a period of seconds. Repeated brief stimuli have little or no effect on spike frequency within a burst. 3. Approximately 81% of the mechanoafferent neurons have a single ipsilateral receptive field. The fields are located on the lips, the anterior tentacles, the dorsal portion of the head, the neck, or the perioral zone. Because many cells have collateral axons in the cerebral connectives, receptive fields elsewhere on the body are a possibility. The highest receptive-field density was associated with the lips. Within each area, receptive fields vary in size and shape. Adjacent fields overlap and larger fields frequently encompass several smaller ones. The features of some fields appear invariant from one animal to the next. A loose form of topographic organization of the mechanoafferent cells was observed. For example, cells located in the medial cluster have lip receptive fields, and most cells in the posterolateral portion of the lateral clusters have tentacle receptive fields. 4. Intracellular stimulation of individual mechanoafferents evokes short and constant-latency EPSPs in putative motor neurons comprising the identified B-cell clusters of the cerebral ganglion. On the basis of several criteria, these EPSPs appear to be several criteria, these EPSPs appear to be chemically mediated and are monosynaptic. 5. Repetitive intracellular stimulation of individual mechanoafferent neurons at low rates results in a gradual decrement in the amplitude of the EPSPs evoked in B cluster neurons. EPSP amplitude can be restored following brief periods of rest, but subsequent stimulation leads to further diminution of the response. 6. A decremented response cannot be restored by strong mechanical stimulation outside the receptive field of the mechanoafferent or by electrical stimulation of the cerebral nerves or connectives...


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.


1997 ◽  
Vol 78 (5) ◽  
pp. 2296-2308 ◽  
Author(s):  
Stephen E. Sherman ◽  
Lei Luo ◽  
Jonathan O. Dostrovsky

Sherman, Stephen E., Lei Luo, and Jonathan O. Dostrovsky. Altered receptive fields and sensory modalities of rat VPL thalamic neurons during spinal strychnine-induced allodynia. J. Neurophysiol. 78: 2296–2308, 1997. Allodynia is an unpleasant sequela of neural injury or neuropathy that is characterized by the inappropriate perception of light tactile stimuli as pain. This condition may be modeled experimentally in animals by the intrathecal (i.t.) administration of strychnine, a glycine receptor antagonist. Thus after i.t. strychnine, otherwise innocuous tactile stimuli evoke behavioral and autonomic responses that normally are elicited only by noxious stimuli. The current study was undertaken to determine how i.t. strychnine alters the spinal processing of somatosensory input by examining the responses of neurons in the ventroposterolateral thalamic nucleus. Extracellular, single-unit recordings were conducted in the lateral thalamus of 19 urethan-anaesthetized, male, Wistar rats (342 ± 44 g; mean ± SD). Receptive fields and responses to noxious and innocuous cutaneous stimuli were determined for 19 units (1 per animal) before and immediately after i.t. strychnine (40 μg). Eighteen of the animals developed allodynia as evidenced by the ability of otherwise innocuous brush or air jet stimuli to evoke cardiovascular and/or motor reflexes. All (3) of the nociceptive-specific units became responsive to brush stimulation after i.t. strychnine, and one became sensitive to brushing over an expanded receptive field. Expansion of the receptive field, as determined by brush stimulation, also was exhibited by all of the low-threshold mechanoreceptive units (14) and wide dynamic range units (2) after i.t. strychnine. The use of air jet stimuli at fixed cutaneous sites also provided evidence of receptive field expansion, because significant unit responses to air jet developed at 13 cutaneous sites (on 7 animals) where an identical stimulus was ineffective in evoking a unit response before i.t. strychnine. However, the magnitude of the unit response to cutaneous air jet stimulation was not changed at sites that already had been sensitive to this stimulus before i.t. strychnine. The onset of allodynia corresponded with the onset of the altered unit responses (i.e., lowered threshold/receptive field expansion) for the majority of animals (9), but the altered unit response either terminated concurrently with symptoms of allodynia (6) or, more frequently, outlasted the symptoms of allodynia (10) as the effects of strychnine declined. The present results demonstrate that the direct, receptor-mediated actions of strychnine on the spinal processing of sensory information are reflected by changes in the receptive fields and response properties of nociceptive and nonnociceptive thalamic neurons. These changes are consistent with the involvement of thalamocortical mechanisms in the expression of strychnine-induced allodynia and, moreover, suggest that i.t. strychnine also produces changes in innocuous tactile sensation.


1997 ◽  
Vol 78 (3) ◽  
pp. 1691-1706 ◽  
Author(s):  
Miguel A. L. Nicolelis ◽  
Rick C. S. Lin ◽  
John K. Chapin

Nicolelis, Miguel A. L., Rick C. S. Lin, and John K. Chapin. Neonatal whisker removal reduces the discrimination of tactile stimuli by thalamic ensembles in adult rats. J. Neurophysiol. 78: 1691–1706, 1997. Simultaneous recordings of up to 48 single neurons per animal were used to characterize the long-term functional effects of sensory plastic modifications in the ventral posterior medial nucleus (VPM) of the thalamus following unilateral removal of facial whiskers in newborn rats. One year after this neonatal whisker deprivation, neurons in the contralateral VPM responded to cutaneous stimulation of the face at much longer minimal latencies (15.2 ± 8.2 ms, mean ± SD) than did normal cells (8.8 ± 5.3 ms) in the same subregion of the VPM. In 69% of these neurons, the initial sensory responses to stimulus offset were followed for up to 700 ms by reverberant trains of bursting discharge, alternating in 100-ms cycles with inhibition. Receptive fields in the deafferented VPM were also atypical in that they extended over the entire face, shoulder, forepaw, hindpaw, and even ipsilateral whiskers. Discriminant analysis (DA) was then used to statistically evaluate how this abnormal receptive field organization might affect the ability of thalamocortical neuronal populations to “discriminate” somatosensory stimulus location. To standardize this analysis, three stimulus targets (“groups”) were chosen in all animals such that they triangulated the central region of the “receptive field” of the recorded multineuronal ensemble. In the normal animals these stimulus targets were whiskers or perioral hairs; in the deprived animals the targets typically included hairy skin of the body as well as face. The measured variables consisted of each neuron's spiking response to each stimulus differentiated into three poststimulus response epochs (0–15, 15–30, and 30–45 ms). DA quantified the statistical contribution of each of these variables to its overall discrimination between the three stimulus sites. In the normal animals, the stimulus locations were correctly classified in 88.2 ± 3.7% of trials on the basis of the spatiotemporal patterns of ensemble activity derived from up to 18 single neurons. In the deprived animals, the stimulus locations were much less consistently discriminated (reduced to 73.5 ± 12.6%; difference from controls significant at P < 0.01) despite the fact that much more widely spaced stimulus targets were used and even when up to 20 neurons were included in the ensemble. Overall, these results suggest that neonatal damage to peripheral sense organs may produce marked changes in the physiology of individual neurons in the somatosensory thalamus. Moreover, the present demonstration that these changes can profoundly alter sensory discrimination at the level of neural populations in the thalamus provides important evidence that the well-known perceptual effects of chronic peripheral deprivation may be partially attributable to plastic reorganization at subcortical levels.


1980 ◽  
Vol 44 (5) ◽  
pp. 862-877 ◽  
Author(s):  
D. Menetrey ◽  
A. Chaouch ◽  
J. M. Besson

1. Spinoreticular tract neurons at the rat lumbar cord level were identified by antidromic activation following stimulation at mainly pontine and mesencephalic levels. These units, which were found in the dorsal half of the cord, could be separated into two groups according to their spinal location, electrophysiological properties, and their central projections. 2. Units in the dorsolateral funiculus nucleus projected mainly to the cuneiformis area and adjacent structures with frequent bilateral projections. They had the slowest conduction velocities, sometimes in the unmyelinated range. Generally, they were driven only by stimulation of subcutaneous and/or deep structures. 3. Neurons located in the dorsal horn mainly projected contralaterally to pontine and mesencephalic levels. their conduction velocities and the electrophysiological properties were identical to those observed for the rat spinothalamic tract (22). Almost all (86%) had clear cutaneous sensitivity and generally large receptive fields: 40% responded to nonnoxious and noxious mechanical cutaneous stimuli and frequently to noxious radiant heat, 26% were exclusively excited by light tactile stimuli, and 20% required noxious cutaneous mechanical stimulation for activation. There was a good correlation between responses to natural and transcutaneous electrical stimulation: units driven by noxious mechanical stimuli received A-delta- and/or C-fiber inputs. The remaining units (14%) had more complex receptive fields associated with both excitatory and inhibitory inputs originating from a single peripheral area. 4. The functional heterogeneity of the rat spinoreticular tract is reminiscent of that demonstrated for the rat and monkey spinothalamic tracts. Similarly, the rat spinoreticular neurons are under the influence of descending inhibitory controls originating from the nucleus raphe magnus and bulbar reticular formation. 5. Responses of the rat spinoreticular tract neurons are consistent with the involvement of this pathway in the transmission of messages of both innocuous and noxious origins.


2008 ◽  
Vol 109 (4) ◽  
pp. 698-706 ◽  
Author(s):  
Douglas G. Ririe ◽  
Lindsay R. Bremner ◽  
Maria Fitzgerald

Background Pain behavior in response to skin incision is developmentally regulated, but little is known about the underlying neuronal mechanisms. The authors hypothesize that the spatial activation and intensity of dorsal horn neuron responses to skin incision differ in immature and adult spinal cord. Methods Single wide-dynamic-range dorsal horn cell spike activity was recorded for a minimum of 2 h from anesthetized rat pups aged 7 and 28 days. Cutaneous pinch and brush receptive fields were mapped and von Frey hair thresholds were determined on the plantar hind paw before and 1 h after a skin incision was made. Results Baseline receptive field areas for brush and pinch were larger and von Frey thresholds lower in the younger animals. One hour after the incision, brush and pinch receptive field area, spontaneous firing, and evoked spike activity had significantly increased in the 7-day-old animals but not in the 28-day-old animals. Von Frey hair thresholds decreased at both ages. Conclusions Continuous recording from single dorsal horn cells both before and after injury shows that sensitization of receptive fields and of background and afferent-evoked spike activity at 1 h is greater in younger animals. This difference is not reflected in von Frey mechanical thresholds. These results highlight the importance of studying the effects of injury on sensory neuron physiology. Injury in young animals induces a marked and rapid increase in afferent-evoked activity in second-order sensory neurons, which may be important when considering long-term effects and analgesic interventions.


1995 ◽  
Vol 74 (2) ◽  
pp. 763-769 ◽  
Author(s):  
K. Kishikawa ◽  
H. Uchida ◽  
Y. Yamamori ◽  
J. G. Collins

1. Cats were prepared for chronic recordings from the lumbar enlargement of the spinal dorsal horn. At the beginning of each recording session, a tungsten microelectrode was advanced through the dura in a physiologically intact, awake, drug-free animal, until amplitude discrimination provided a single neuron with a receptive field on the hindquarters. 2. Extracellular recordings of activity of each neuron were made during receptive field stimulation with tactile and thermal nonnoxious and noxious stimuli. 3. Baseline responses obtained in the awake state were compared with responses of the same neurons during slow-wave or rapid-eye-movement (REM) sleep. In a subpopulation of neurons, the effects of anesthesia (propofol, 7.5 mg/kg iv) were observed after the completion of sleep studies. 4. The low-threshold receptive fields of the seven neurons studied during REM sleep were all increased in size when compared with the baseline value. The average increase was 52.6% (range 26.2–96.7%). 5. The low-threshold receptive fields of the seven neurons studied during REM sleep were reduced by propofol anesthesia by an average of 49.1% (range 29–74%). 6. Neuronal response to receptive field brushing was observed in 15 neurons during REM sleep. The effect of propofol on receptive field brushing was observed in 8 of those neurons. In only one of those eight neurons were the effects of REM sleep and anesthesia in the same direction. 7. Changes in neuronal responses were less consistent during slow-wave sleep but still differed from changes induced by propofol.(ABSTRACT TRUNCATED AT 250 WORDS)


1998 ◽  
Vol 80 (1) ◽  
pp. 120-129 ◽  
Author(s):  
Robert W. Dykes ◽  
A. D. Craig

Dykes, Robert W. and A. D. Craig. Control of size and excitability of mechanosensory receptive fields in dorsal column nuclei by homolateral dorsal horn neurons. J. Neurophysiol. 80: 120–129 1998. Both accidental and experimental lesions of the spinal cord suggest that neuronal processes occurring in the spinal cord modify the relay of information through the dorsal column-lemniscal pathway. How such interactions might occur has not been adequately explained. To address this issue, the receptive fields of mechanosensory neurons of the dorsal column nuclei were studied before and after manipulation of the spinal dorsal horn. After either a cervical or lumbar laminectomy and exposure of the dorsal column nuclei in anesthetized cats, the representation of the hindlimb or of the forelimb was defined by multiunit recordings in both the dorsal column nuclei and in the ipsilateral spinal cord. Next, a single cell was isolated in the dorsal column nuclei, and its receptive field carefully defined. Each cell could be activated by light mechanical stimuli from a well-defined cutaneous receptive field. Generally the adequate stimulus was movement of a few hairs or rapid skin indentation. Subsequently a pipette containing either lidocaine or cobalt chloride was lowered into the ipsilateral dorsal horn at the site in the somatosensory representation in the spinal cord corresponding to the receptive field of the neuron isolated in the dorsal column nuclei. Injection of several hundred nanoliters of either lidocaine or cobalt chloride into the dorsal horn produced an enlargement of the receptive field of the neuron being studied in the dorsal column nuclei. The experiment was repeated 16 times, and receptive field enlargements of 147–563% were observed in 15 cases. These data suggest that the dorsal horn exerts a tonic inhibitory control on the mechanosensory signals relayed through the dorsal column-lemniscal pathway. Because published data from other laboratories have shown that receptive field size is controlled by signals arising from the skin, we infer that the control of neuronal excitability, receptive field size and location for lemniscal neurons is determined by tonic afferent activity that is relayed through a synapse in the dorsal horn. This influence of dorsal horn neurons on the relay of mechanosensory information through the lemniscal pathways must modify our traditional views concerning the relative independence of these two systems.


1993 ◽  
Vol 69 (4) ◽  
pp. 1171-1180 ◽  
Author(s):  
N. L. Chiaia ◽  
W. R. Bauer ◽  
R. W. Rhoades

1. Extracellular single-unit recording and receptive-field mapping techniques were used to evaluate the response characteristics of trigeminal (V) ganglion cells in unanesthetized, decerebrate, fetal rats between the ages of embryonic (E-) day 15 and E-20 (E-0 is the day of conception). 2. The receptive-field properties of the cells (n = 282) recorded at all of these ages except E-15 were remarkably similar; V primary afferents were generally silent in the absence of peripheral stimulation (94.3%) and gave rapidly adapting responses to innocuous tactile stimuli (97.5%). Rapid response decrements to repeated stimuli were observed in 9 of the 14 cells (64%) tested. 3. None of the cells recorded were activated by either heat or cold. No attempt was made to evaluate responses to noxious mechanical stimuli. 4. Particular attention was paid to neurons whose receptive fields involved mystacial vibrissae follicles. At all ages, neurons were recorded that responded to indentation of the skin at the base of the vibrissae, but vibrissa deflection was not an adequate stimulus for any of the cells tested. At all ages, nearly all (89.0%) of the 127 cells with vibrissa-related receptive fields responded to indentation of one and only one follicle. 5. These results indicate that the response properties (e.g., adaptation characteristics, ability to respond to repeated stimuli) of V primary afferents in fetal rats differ substantially from those of V ganglion cells in adult animals, but that the receptive-field size for these neurons in prenatal rats is, with very rare exceptions, adult-like from the earliest age at which they can be recorded. 6. These results, when considered together with the results of previous retrograde tracing experiments in fetal animals, suggest that the initial projections of V primary afferents to their peripheral targets may be quite accurate.


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