Subthreshold components of the cutaneous mechanoreceptive fields of dorsal horn neurons in the rat lumbar spinal cord

1989 ◽  
Vol 62 (4) ◽  
pp. 907-916 ◽  
Author(s):  
C. J. Woolf ◽  
A. E. King

1. Intracellular recordings have been made from 76 neurons in the dorsal horn of the fourth and fifth lumbar segments of the spinal cord in decerebrate-spinal rats. The locations of the neurons were identified after horseradish peroxidase (HRP) ionophoresis (n = 18) or calculated from depth readings (n = 58). Sixty-nine of the neurons were found or estimated to lie within the deep dorsal horn (laminae III-V), with the remaining 7 in laminae I and II. 2. Background excitatory activity was present in all the neurons in the absence of peripheral mechanical stimuli. In 22 neurons, this consisted only of subthreshold excitatory postsynaptic potentials (EPSPs), but in 54, a proportion of the EPSPs reached threshold, producing a spontaneous spike discharge (frequency 0.2-50 Hz) that had a rhythmic component in six cells. Spontaneous hyperpolarizations occurred but were uncommon (n = 10). 3. All the neurons had excitatory cutaneous mechanoreceptive fields on the ipsilateral hindlimb. The receptive fields, defined in terms of action-potential discharge, could be subdivided into two areas: a high-probability "firing zone," where skin stimulation elicited an action-potential discharge above the mean + 1 SD of the background activity; and a low-probability firing fringe, where the stimulus elicited a distinct subthreshold depolarization, but the action-potential response fell within the variability of the background discharge. 4. Mechanical stimulation in the middle of the firing zone in all cells generated both supra- and subthreshold excitatory responses, with the former predominating. As the stimuli were applied progressively farther away from the center of the firing zone, the subthreshold component became relatively more prominent. 5. Fifty percent of the 15 neurons that were recorded from for sufficient time (greater than 30 min) to enable the presence, extent, and characteristics of subthreshold responses to be examined in detail were found to have a low-probability firing fringe to their receptive fields. The response to stimulation within this fringe typically consisted of high-frequency, low-amplitude PSPs riding on a sustained depolarization, with an action-potential discharge that could not readily be distinguished from the spontaneous activity. The size of the fringe ranged from a small area adjacent to the firing zone to almost the entire hindlimb. 6. The firing zones of 20 neurons were low-threshold only and in 5 cells were high-threshold only. The majority of neurons were multireceptive, responding both to low- and high-intensity stimuli (n = 51).(ABSTRACT TRUNCATED AT 400 WORDS)

1996 ◽  
Vol 75 (6) ◽  
pp. 2606-2628 ◽  
Author(s):  
J. T. Katter ◽  
R. J. Dado ◽  
E. Kostarczyk ◽  
G. J. Giesler

1. A goal of this study was to determine whether neurons in the sacral spinal cord that project to the diencephalon are involved in the processing and transmission of sensory information that arises in the perineum and pelvis. Therefore, 58 neurons in segments L6-S2 were activated antidromically with currents < or = 30 microA from points in the contralateral diencephalon in rats that were anesthetized with urethan. 2. Responses to mechanical stimuli applied to the cutaneous receptive fields of these neurons were used to classify them as low-threshold (LT), wide dynamic range (WDR) or high-threshold (HT) neurons. Twenty-two neurons (38%) responded preferentially to brushing (LT neurons). Eighteen neurons (31%) responded to brushing but responded with higher firing frequencies to noxious mechanical stimuli (WDR neurons). Eighteen neurons (31%) responded only to noxious intensities of mechanical stimulation (HT neurons). LT neurons were recorded predominantly in nucleus proprius of the dorsal horn. Nociceptive neurons (WDR and HT) were recorded throughout the dorsal horn. 3. Cutaneous receptive fields were mapped for 56 neurons. Forty-five (80%) had receptive fields that included at least two of the following regions ipsilaterally: the rump, perineum, or tail. Eleven neurons (20%) had receptive fields that were restricted to one of these areas or to the ipsilateral hind limb. Thirty-eight neurons (68%) had cutaneous receptive fields that also included regions of the contralateral tail or perineum. On the perineum, receptive fields usually encompassed perianal and perivaginal areas including the clitoral sheath. There were no statistically significant differences in the locations or sizes of receptive fields for LT neurons compared with nociceptive (WDR and HT) neurons. 4. Thirty-seven LT, WDR, and HT neurons were tested for their responsiveness to heat stimuli. Five (14%) responded to increasing intensities of heat with graded increases in their firing frequencies. Thirty-two LT, WDR, and HT neurons also were tested with cold stimuli. None responded with graded increases in their firing frequencies to increasingly colder stimuli. There were no statistically significant differences among the responses of LT, WDR, and HT neurons to either heat or cold stimuli. 5. Forty LT, WDR, and HT neurons were tested for their responsiveness to visceral stimuli by distending a balloon placed into the rectum and colon with a series of increasing pressures. Seventeen (43%) exhibited graded increases in their firing frequencies in response to increasing pressures of colorectal distention (CrD). None of the responsive neurons responded reproducibly to CrD at an intensity of 20 mmHg, and all responded at intensities of > or = 80 mmHg. More than 90% responded abruptly at stimulus onset, responded continuously throughout the stimulus period, and stopped responding immediately after termination of the stimulus. 6. Thirty-one neurons were tested for their responsiveness to distention of a balloon placed inside the vagina. Eleven (35%) exhibited graded increases in their firing frequencies in response to increasing pressures of vaginal distention (VaD). The thresholds and temporal profiles of the responses to VaD were similar to those for CrD. Twenty-nine neurons were tested with both CrD and VaD. Thirteen (45%) were excited by both stimuli, four (14%) responded to CrD but not VaD, and one (3%) was excited by VaD but not CrD. Neurons excited by CrD, VaD, or both were recorded throughout the dorsal horn. 7. As a population, WDR neurons, but not LT or HT neurons, encoded increasing pressures of CrD and VaD with graded increases in their firing frequencies. The responses of WDR neurons to CrD differed significantly from those of either LT or HT neurons. Regression analyses of the stimulus-response functions of responsive WDR neurons to CrD and VaD were described by power functions with exponents of 1.6 and 2.4, respectively.(ABSTRACT TRUNCATED)


1984 ◽  
Vol 52 (4) ◽  
pp. 595-611 ◽  
Author(s):  
D. Menetrey ◽  
J. de Pommery ◽  
J. M. Besson

Spinal neurons antidromically activated from either the lateral reticular nucleus (LRN) or immediately adjacent areas were identified in the rat lumbar spinal cord. In agreement with previous anatomical work (60), these neurons were widely distributed in both the dorsal and ventral horns of the spinal cord and could be subdivided into three main groups according to their location: a) deep ventromedial (DVM) cells, which project more substantially to the LRN than to other supraspinal targets; b) cells of the median portion of the neck of the dorsal horn (mNDH), which project exclusively to the LRN; c) cells lying in other parts of the dorsal horn (superficial layers, nucleus proprius, reticular extension of the neck), by their location, they are indistinguishable from cells projecting to other supraspinal targets. The probability is high that the DVM and mNDH cells contribute exclusively, or at least preferentially, to the lateral component of the spinoreticular tract (lSRT), defined as the direct spinal pathway to the LRN. Although electrophysiological properties of cells were clearly related to their spinal location, several subpopulations could be recognized in each of the three main groups. The majority of DVM neurons were in lamina VII, with some in laminae VI, VIII, and X. With the exception of a few lamina X cells, the DVM neurons had high conduction velocities. Four subpopulations of these neurons were recognized. a) Innocuous proprioceptive cells responded to small changes in joint position, some showing convergence of nonnoxious cutaneous inputs. b) High-threshold cells (approximately 50% of DVM cells). Seventy-five percent of these cells were excited from bilateral receptive fields (mostly symmetric) with noxious cutaneous pinching that extended to subcutaneous tissues. Their evoked responses had long-lasting postdischarges that continued up to several minutes after cessation of the stimulus. c) Inhibited cells had no demonstrable excitatory receptive fields and a high ongoing activity that was tonically depressed by pressure or pinch; poststimulus effects of long duration were observed. d) Cells with no resting discharge and demonstrable excitatory peripheral receptive fields. mNDH cells had recording sites at the medial border of the internal portion of the reticular area of the neck of the dorsal horn.(ABSTRACT TRUNCATED AT 400 WORDS)


2003 ◽  
Vol 90 (1) ◽  
pp. 73-80 ◽  
Author(s):  
Yuan Bo Peng ◽  
Qing Dong Ling ◽  
M. A. Ruda ◽  
Daniel R. Kenshalo

Neonatal peripheral inflammation has been shown to produce profound anatomical changes in the dorsal horn of adult rats. In this study, we explored whether parallel physiological changes exist. Neonatal rats were injected with complete Freund's adjuvant (CFA) into the left hind paw. At 8–10 wk of age, single dorsal horn neurons were recorded in response to graded intensities of mechanical stimuli delivered to the receptive field. In addition, cord dorsum potentials, produced by electrical stimuli delivered to the left sciatic nerve at 2.5× threshold, were recorded bilaterally from L2 to S3. There were significant increases in background activity and responses to brush and pinch in neonatal rats that were treated with CFA, as compared with control rats. Further analysis showed similar significant changes when dorsal horn neurons were categorized into wide dynamic range (WDR), high-threshold (HT), and low-threshold (LT) groups. The receptive field was significantly larger in neonatally treated rats as compared with control rats. Additionally, there was a significant increase in the response to a 49°C heat stimulus in neonatally treated rats as compared with control rats. There was also a trend for the amplitudes of N1, N2, and P waves of the cord dorsum potential to increase and latencies to decrease in neonatally treated rats, but no significant differences were detected between different levels of the spinal cord (L2 to S3). These data further support the notion that anatomical and physiological plasticity changes occurred in the spinal cord following early neonatal CFA treatment.


1990 ◽  
Vol 64 (1) ◽  
pp. 299-311 ◽  
Author(s):  
V. Neugebauer ◽  
H. G. Schaible

1. In the spinalized cat, nociceptive spinal neurons with knee input show enhanced responses to mechanical stimulation of that joint once an inflammation has developed in the knee. Enhanced responses may result from increased afferent inflow as well as from modifications of the nociceptive processing within the spinal cord. To examine the significance of these components, we tested in 30 chloralose-anesthetized, spinalized cats whether, during development of arthritis, changes of responsiveness in spinal neurons are restricted to stimulation of the inflamed joint or whether responsiveness in these neurons is altered in general. While continuously recording from a neuron, we injected kaolin and carrageenan into one knee and tested the responses to mechanical stimuli applied to the joint and to regions adjacent to and remote from the knee during the developing arthritis. In addition, in six cats we monitored the neurons' responses to electrical stimulation of the sural nerves and the rostral lumbar spinal cord. 2. Of 32 neurons in laminae VI, VII, and VIII of the lumbar spinal cord, 15 ascending and eight nonascending cells were driven by mechanical stimulation of one or both knee joint(s). Nine of these were nociceptive specific (NS), responding exclusively or predominantly to noxious compression of the knee and other deep tissue, and 12 were wide-dynamic-range (WDR) cells with graded responses to gentle and noxious stimuli applied to the knee joint(s), deep tissue, and skin. Two neurons with high ongoing discharges had some excitatory joint input but showed marked inhibition by most stimuli used (INH neurons). The majority of the neurons had receptive fields on both legs. Nine of the 32 neurons had no input from the knee(s). 3. All 23 neurons with joint input became sensitive or more responsive to movements and gentle compression of the inflamed knee once the inflammation had developed. In general, these neurons also showed enhanced responses to compression of the adjacent muscles in thigh and lower leg. In 20 neurons, response properties were even altered for stimuli applied to regions remote from the inflamed joint, including the contralateral leg in 18 cases. We found expansion of initially restricted receptive fields (mainly in NS cells), enhancement of preexisting responses, and/or lowering of threshold to mechanical stimuli applied to these regions; few neurons developed inhibitory reactions.(ABSTRACT TRUNCATED AT 400 WORDS)


2006 ◽  
Vol 96 (2) ◽  
pp. 661-670 ◽  
Author(s):  
Esther Garcia-Nicas ◽  
Jennifer M. A. Laird ◽  
Fernando Cervero

Single-unit electrical activity was recorded from 80 nociceptor-specific (NS) neurons in the dorsal horn of the lumbar spinal cord of pentobarbital anesthetized rats. Their responses to low- and high-intensity mechanical stimulation of their receptive fields (RFs) were recorded before and after the application of irritant agents [capsaicin (CAP) or mustard oil (MO)] to the RF. Before the applications of the irritants the neurons responded only to high-intensity stimuli, but after this procedure 20 of 28 neurons tested were sensitized, i.e., gave increased responses to high-intensity stimuli and showed novel responses to low-intensity mechanical stimulation as well as an Aβ-fiber afferent drive. CAP was more likely to induce sensitization than MO and the majority of sensitized neurons were located in the superficial dorsal horn. No relationship was found between the magnitude of the response to the sensitizing agent and the presence or absence of sensitization. Cumulative doses of two γ-aminobutyric acid type A (GABAA)–receptor antagonists, picrotoxin and bicuculline, were administered systemically or applied directly over the spinal cord. The GABAA antagonists reversed the sensitization of the neurons by reducing the novel low-threshold responses. These results show that NS neurons in the spinal dorsal horn can be sensitized by a sustained afferent discharge in peripheral nociceptors and that this sensitization can be reduced or reversed by low doses of GABAA-receptor antagonists. This provides evidence for a mechanism in which an enhanced GABAergic transmission can lead to hyperexcitability and sensitization of NS neurons in the dorsal horn.


1994 ◽  
Vol 71 (3) ◽  
pp. 981-1002 ◽  
Author(s):  
R. J. Dado ◽  
J. T. Katter ◽  
G. J. Giesler

1. The goal of this study was to gather data that would increase our understanding of nociceptive processing by spinothalamic tract (STT) neurons that receive inputs from the hand and arm. Fifty neurons in the cervical enlargement of urethan-anesthetized rats were antidromically activated from the contralateral posterior thalamus. A stimulating electrode was moved systematically within an anterior-posterior plane in the thalamus until a point was located where the smallest amount of current antidromically activated the neuron. The antidromic thresholds at each of these lowest threshold points was < or = 30 microA; the mean antidromic threshold was 15.4 +/- 1.0 (SE) microA. Lowest threshold points were found primarily in the posterior thalamic group (Po), zona incerta, and in or near the supraoptic decussation. 2. The recording sites of 47 neurons were marked and recovered. Recording sites were located in the superficial dorsal horn (SDH, n = 15), deep dorsal horn (DDH, n = 31), and ventral horn (n = 1). Recording sites were located across the mediolateral extent of the SDH. Within the DDH, recording sites were concentrated laterally in nucleus proprius and dorsally in the lateral reticulated area. The locations of the recording points confirm previous anatomic descriptions of STT neurons in the cervical enlargement. 3. Cutaneous excitatory receptive fields were restricted to the ipsilateral forepaw or forelimb in 67% (10/15) of the neurons recorded in the SDH and 42% (13/31) of the neurons recorded in the DDH. Neurons having larger, more complex receptive fields were also commonly encountered. Thirty-three percent (5/15) of the neurons recorded in the SDH and 58% (18/31) recorded in the DDH had receptive fields that were often discontinuous and included areas of the ipsilateral shoulder, thorax, and head, including the face. 4. Innocuous and noxious mechanical stimuli were applied to the receptive field of each neuron. Fifty percent (25/50) responded to innocuous mechanical stimuli but responded at higher frequencies to noxious stimuli (wide dynamic range, WDR). Forty-four percent (22/50) responded only to noxious stimuli (high threshold, HT). Six percent (3/50) responded preferentially to innocuous stimuli (low threshold, LT). WDR and HT neurons were recorded in both the SDH and DDH, including nucleus proprius, an area not typically associated with nociceptive transmission at other levels of the cord. Sixty percent (9/15) of the units recorded in the SDH were classified as WDR neurons; the other 40% (6/15) were classified HT. Forty-eight percent (15/31) of the units recorded in the DDH were classified as WDR neurons and 42% (13/31) as HT.(ABSTRACT TRUNCATED AT 400 WORDS)


2008 ◽  
Vol 99 (6) ◽  
pp. 3144-3150 ◽  
Author(s):  
Rachel A. Ingram ◽  
Maria Fitzgerald ◽  
Mark L. Baccei

The lower thresholds and increased excitability of dorsal horn neurons in the neonatal rat suggest that inhibitory processing is less efficient in the immature spinal cord. This is unlikely to be explained by an absence of functional GABAergic inhibition because antagonism of γ-aminobutyric acid (GABA) type A receptors augments neuronal firing in vivo from the first days of life. However, it is possible that more subtle deficits in GABAergic signaling exist in the neonate, such as decreased reliability of transmission or greater depression during repetitive stimulation, both of which could influence the relative excitability of the immature spinal cord. To address this issue we examined monosynaptic GABAergic inputs onto superficial dorsal horn neurons using whole cell patch-clamp recordings made in spinal cord slices at a range of postnatal ages (P3, P10, and P21). The amplitudes of evoked inhibitory postsynaptic currents (IPSCs) were significantly lower and showed greater variability in younger animals, suggesting a lower fidelity of GABAergic signaling at early postnatal ages. Paired-pulse ratios were similar throughout the postnatal period, whereas trains of stimuli (1, 5, 10, and 20 Hz) revealed frequency-dependent short-term depression (STD) of IPSCs at all ages. Although the magnitude of STD did not differ between ages, the recovery from depression was significantly slower at immature GABAergic synapses. These properties may affect the integration of synaptic inputs within developing superficial dorsal horn neurons and thus contribute to their larger receptive fields and enhanced afterdischarge.


1984 ◽  
Vol 52 (3) ◽  
pp. 449-458 ◽  
Author(s):  
A. R. Light ◽  
R. G. Durkovic

Single-unit recordings from 312 units of lamina I-VII of the lumbar spinal cord of unanesthetized, decerebrate, T8 spinal cats were used to determine the somatotopic and laminar organization of spinal neurons responding to cutaneous stimulation of the hindlimb. Properties of cells confined to different Rexed laminae (I-VII) were shown to differ in several respects, including responses to variations in stimulus intensity, receptive-field areas, spontaneous frequencies, and central delays. Spinal cord neurons with similarly localized cutaneous receptive fields were found to be organized in sagittally oriented rectangular columns. These columns were 7 to at least 20 mm long (rostral-caudal axis), 0.5-1.0 mm wide, and could encompass laminae I-VII in depth. Touch, pressure, and pinch were effective excitatory inputs into each column subserving a given receptive-field location. A map of the somatotopic organization of units in the horizontal plane is presented, which in general confirms previous reports and in particular deals with the organization of units with receptive fields on the plantar cushion and individual toes.


Sign in / Sign up

Export Citation Format

Share Document