Altered Receptive Fields and Sensory Modalities of Rat VPL Thalamic Neurons During Spinal Strychnine-Induced Allodynia

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.

1986 ◽  
Vol 55 (1) ◽  
pp. 76-96 ◽  
Author(s):  
R. P. Yezierski ◽  
R. H. Schwartz

Recordings were made from 90 identified spinomesencephalic tract (SMT) cells in the lumbosacral spinal cord of cats anesthetized with alpha-chloralose and pentobarbital sodium. Recording sites were located in laminae I-VIII. Antidromic stimulation sites were located in different regions of the rostral and caudal midbrain including the periaqueductal gray, midbrain reticular formation, and the deep layers of the superior colliculus. Twelve SMT cells were antidromically activated from more than one midbrain level or from sites in the medial thalamus. The mean conduction velocity for the population of cells sampled was 45.2 +/- 21.4 m/s. Cells were categorized based on their responses to graded intensities of mechanical stimuli and the location of excitatory and/or inhibitory receptive fields. Four major categories of cells were encountered: wide dynamic range (WDR); high threshold (HT); deep/tap; and nonresponsive. WDR and HT cells had excitatory and/or inhibitory receptive fields restricted to the ipsilateral hindlimb or extending to other parts of the body including the tail, forelimbs, and face. Some cells had long afterdischarges following noxious stimulation, whereas others had high rates of background activity that was depressed by nonnoxious and noxious stimuli. Deep/tap cells received convergent input from muscle, joint, or visceral primary afferent fibers. The placement of mechanical lesions at different rostrocaudal levels of the cervical spinal cord provided information related to the spinal trajectory of SMT axons. Six axons were located contralateral to the recording electrode in the ventrolateral/medial or lateral funiculi while two were located in the ventrolateral funiculus of the ipsilateral spinal cord. Stimulation at sites used to antidromically activate SMT cells resulted in the inhibition of background and evoked responses for 22 of 25 cells tested. Inhibitory effects were observed on responses evoked by low/high intensity cutaneous stimuli and by the activation of joint or muscle primary afferent fibers. Based on the response and receptive-field properties of SMT cells it is suggested that the SMT may have an important role in somatosensory mechanisms, particularly those related to nociception.


2010 ◽  
Vol 104 (2) ◽  
pp. 675-684 ◽  
Author(s):  
Yen-Chyi Liu ◽  
Jens Herberholz

Crayfish ( Procambarus clarkii ) have bilateral pairs of giant interneurons that control rapid escape movements in response to predatory threats. The medial giant neurons (MGs) can be made to fire an action potential by visual or tactile stimuli directed to the front of the animal and this leads to an escape tail-flip that thrusts the animal directly backward. The lateral giant neurons (LGs) can be made to fire an action potential by strong tactile stimuli directed to the rear of the animal, and this produces flexions of the abdomen that propel the crayfish upward and forward. These observations have led to the notion that the receptive fields of the giant neurons are locally restricted and do not overlap with each other. Using extra- and intracellular electrophysiology in whole animal preparations of juvenile crayfish, we found that the receptive fields of the LGs are far more extensive than previously assumed. The LGs receive excitatory inputs from descending interneurons originating in the brain; these interneurons can be activated by stimulation of the antenna II nerve or the protocerebral tract. In our experiments, descending inputs alone could not cause action potentials in the LGs, but when paired with excitatory postsynaptic potentials elicited by stimulation of tail afferents, the inputs summed to yield firing. Thus the LG escape neurons integrate sensory information received through both rostral and caudal receptive fields, and excitatory inputs that are activated rostrally can bring the LGs' membrane potential closer to threshold. This enhances the animal's sensitivity to an approaching predator, a finding that may generalize to other species with similarly organized escape systems.


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...


2002 ◽  
Vol 14 (7) ◽  
pp. 1669-1689 ◽  
Author(s):  
Richard H. R. Hahnloser ◽  
Rodney J. Douglas ◽  
Klaus Hepp

There is strong anatomical and physiological evidence that neurons with large receptive fields located in higher visual areas are recurrently connected to neurons with smaller receptive fields in lower areas. We have previously described a minimal neuronal network architecture in which top-down attentional signals to large receptive field neurons can bias and selectively read out the bottom-up sensory information to small receptive field neurons (Hahnloser, Douglas, Mahowald, & Hepp, 1999). Here we study an enhanced model, where the role of attention is to recruit specific inter-areal feedback loops (e.g., drive neurons above firing threshold). We first illustrate the operation of recruitment on a simple example of visual stimulus selection. In the subsequent analysis, we find that attentional recruitment operates by dynamical modulation of signal amplification and response multistability. In particular, we find that attentional stimulus selection necessitates increased recruitment when the stimulus to be selected is of small contrast and of small distance away from distractor stimuli. The selectability of a low-contrast stimulus is dependent on the gain of attentional effects; for example, low-contrast stimuli can be selected only when attention enhances neural responses. However, the dependence of attentional selection on stimulus-distractor distance is not contingent on whether attention enhances or suppresses responses. The computational implications of attentional recruitment are that cortical circuits can behave as winner-take-all mechanisms of variable strength and can achieve close to optimal signal discrimination in the presence of external noise.


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.


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.


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.


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.


2012 ◽  
Vol 24 (2) ◽  
pp. 276-286 ◽  
Author(s):  
Nadia Bolognini ◽  
Carlo Cecchetto ◽  
Carlo Geraci ◽  
Angelo Maravita ◽  
Alvaro Pascual-Leone ◽  
...  

Confronted with the loss of one type of sensory input, we compensate using information conveyed by other senses. However, losing one type of sensory information at specific developmental times may lead to deficits across all sensory modalities. We addressed the effect of auditory deprivation on the development of tactile abilities, taking into account changes occurring at the behavioral and cortical level. Congenitally deaf and hearing individuals performed two tactile tasks, the first requiring the discrimination of the temporal duration of touches and the second requiring the discrimination of their spatial length. Compared with hearing individuals, deaf individuals were impaired only in tactile temporal processing. To explore the neural substrate of this difference, we ran a TMS experiment. In deaf individuals, the auditory association cortex was involved in temporal and spatial tactile processing, with the same chronometry as the primary somatosensory cortex. In hearing participants, the involvement of auditory association cortex occurred at a later stage and selectively for temporal discrimination. The different chronometry in the recruitment of the auditory cortex in deaf individuals correlated with the tactile temporal impairment. Thus, early hearing experience seems to be crucial to develop an efficient temporal processing across modalities, suggesting that plasticity does not necessarily result in behavioral compensation.


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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