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Activity evoked by A- and C-afferent fibers in rat dorsal horn neurons and its relation to a flexion reflex

Schouenborg, J. LU orcid and Sjolund, B. H. (1983) In Journal of Neurophysiology 50(5). p.1108-1121
Abstract

The responses of 56 neurons recorded in the lumbosacral spinal cord of halothane-anesthetized rats were studied following the application of mechanical stimuli to the skin on the lateral aspect of the paw or electrical stimulation of the sural nerve. Only neurons driven by A- and C-fiber stimulation were considered. The evoked activity in a nerve supplying flexor muscles, the common peroneal nerve, was also recorded to evaluate possible relations between neuronal events and reflex discharges. To quantify the reflex output we also recorded the activity of 12 motoneurons. Four different populations of dorsal horn neurons activated by C-fibers could be distinguished. The neurons were classified on the basis of their responses to mechanical... (More)

The responses of 56 neurons recorded in the lumbosacral spinal cord of halothane-anesthetized rats were studied following the application of mechanical stimuli to the skin on the lateral aspect of the paw or electrical stimulation of the sural nerve. Only neurons driven by A- and C-fiber stimulation were considered. The evoked activity in a nerve supplying flexor muscles, the common peroneal nerve, was also recorded to evaluate possible relations between neuronal events and reflex discharges. To quantify the reflex output we also recorded the activity of 12 motoneurons. Four different populations of dorsal horn neurons activated by C-fibers could be distinguished. The neurons were classified on the basis of their responses to mechanical stimuli and of their location in the dorsal horn. Class 1 neurons were driven by nonnoxious stimulation only. Neurons driven by nonnoxious stimuli and noxious stimuli were denoted class 2S (superficial to the location of the maximal A-β-fiber-evoked field potentials) or class 2D (deep to the same potential). Class 3 neurons were driven by noxious stimuli only. The functional characteristics of these four classes of neurons differed in many respects. The latency for the A-β-fiber-evoked discharge was, on average, 2 ms longer in class 2S than in class 2D neurons, indicating a polysynaptic A-β input to the former class of neurons. The C-fiber-evoked neuronal discharge often showed time-locked peaks of activity during the interval 120-170 ms. Such peaks of activity occurred, in general, later in class 2D neurons (mean, 157 ms) than in class 2S (mean, 137 ms) or in class 3 mean, 140 ms), suggesting that the different classes received C-fiber input via partially different routes. The responses to repeated C-fiber stimulation also differed markedly among the four classes. After 16 single electrical stimulations (100 T (T = threshold strength for activating A-β-afferents), 1 Hz), the C-fiber-evoked discharge in class 2D neurons was increased by 196%, whereas the corresponding value for those in classes 2S, 3, and 1 was 41, 24 and 38%, respectively. Ten of 14 class 2D neurons showed a simultaneous increase of the A-fiber-evoked discharge, indicating an increased excitability of these neurons after repeated impulses in C-fiber afferents. An early reflex discharge (latency, 6-10 ms) was evoked in the common peroneal nerve by electrical stimulation of the sural nerve. The magnitude was maximal at a strength of 2 T and was not potentiated by repetitive intense stimulation (100 T, 1 Hz). Electrical stimulation of the sural nerve at a strength higher than 30 T regularly evoked a prolonged late (latency, 160-200 ms) reflex discharge in the common peroneal nerve. The magnitude but not the latency of this late reflex was dependent on the frequency of stimulation, being remarkably potentiated when the frequency was higher than 0.3 Hz. The total reflex output, as measured from 12 motoneurons belonging to the common nerve, was increased by 165% after 16 stimulations (100 T, 1 Hz). Ten of 14 class 2D neurons and 3 of 10 class 2S neurons exhibited a late C-fiber-evoked peak activity (145-170 ms), which preceded and overlapped with the onset of the late reflex discharge. Furthermore, these neurons also gave a prolonged C-fiber-evoked discharge, which was strongly potentiated by repetitive stimulation (100 T, 1 Hz). None of the neurons belonging to class 1 or class 3 displayed this combination of characteristics. On the basis of differences in response characteristics, it is suggested that the four classes of neurons studied are intercalated in different local neuronal circuits and subserve different functions. It is suggested that some of the class 2D and/or 2S neurons were, in fact, intercalated in the neuronal circuit responsible for the late reflex discharge. Evidence that the neurons studied were not intercalated in the reflex pathway serving the early reflex discharge was also presented.

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published
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in
Journal of Neurophysiology
volume
50
issue
5
pages
1108 - 1121
publisher
American Physiological Society
external identifiers
  • pmid:6644362
  • scopus:0021072543
ISSN
0022-3077
DOI
10.1152/jn.1983.50.5.1108
language
English
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yes
id
0673cd5d-59d2-4a67-a5bd-03b6b10b88ba
date added to LUP
2019-06-25 16:12:29
date last changed
2024-04-02 10:22:22
@article{0673cd5d-59d2-4a67-a5bd-03b6b10b88ba,
  abstract     = {{<p>The responses of 56 neurons recorded in the lumbosacral spinal cord of halothane-anesthetized rats were studied following the application of mechanical stimuli to the skin on the lateral aspect of the paw or electrical stimulation of the sural nerve. Only neurons driven by A- and C-fiber stimulation were considered. The evoked activity in a nerve supplying flexor muscles, the common peroneal nerve, was also recorded to evaluate possible relations between neuronal events and reflex discharges. To quantify the reflex output we also recorded the activity of 12 motoneurons. Four different populations of dorsal horn neurons activated by C-fibers could be distinguished. The neurons were classified on the basis of their responses to mechanical stimuli and of their location in the dorsal horn. Class 1 neurons were driven by nonnoxious stimulation only. Neurons driven by nonnoxious stimuli and noxious stimuli were denoted class 2S (superficial to the location of the maximal A-β-fiber-evoked field potentials) or class 2D (deep to the same potential). Class 3 neurons were driven by noxious stimuli only. The functional characteristics of these four classes of neurons differed in many respects. The latency for the A-β-fiber-evoked discharge was, on average, 2 ms longer in class 2S than in class 2D neurons, indicating a polysynaptic A-β input to the former class of neurons. The C-fiber-evoked neuronal discharge often showed time-locked peaks of activity during the interval 120-170 ms. Such peaks of activity occurred, in general, later in class 2D neurons (mean, 157 ms) than in class 2S (mean, 137 ms) or in class 3 mean, 140 ms), suggesting that the different classes received C-fiber input via partially different routes. The responses to repeated C-fiber stimulation also differed markedly among the four classes. After 16 single electrical stimulations (100 T (T = threshold strength for activating A-β-afferents), 1 Hz), the C-fiber-evoked discharge in class 2D neurons was increased by 196%, whereas the corresponding value for those in classes 2S, 3, and 1 was 41, 24 and 38%, respectively. Ten of 14 class 2D neurons showed a simultaneous increase of the A-fiber-evoked discharge, indicating an increased excitability of these neurons after repeated impulses in C-fiber afferents. An early reflex discharge (latency, 6-10 ms) was evoked in the common peroneal nerve by electrical stimulation of the sural nerve. The magnitude was maximal at a strength of 2 T and was not potentiated by repetitive intense stimulation (100 T, 1 Hz). Electrical stimulation of the sural nerve at a strength higher than 30 T regularly evoked a prolonged late (latency, 160-200 ms) reflex discharge in the common peroneal nerve. The magnitude but not the latency of this late reflex was dependent on the frequency of stimulation, being remarkably potentiated when the frequency was higher than 0.3 Hz. The total reflex output, as measured from 12 motoneurons belonging to the common nerve, was increased by 165% after 16 stimulations (100 T, 1 Hz). Ten of 14 class 2D neurons and 3 of 10 class 2S neurons exhibited a late C-fiber-evoked peak activity (145-170 ms), which preceded and overlapped with the onset of the late reflex discharge. Furthermore, these neurons also gave a prolonged C-fiber-evoked discharge, which was strongly potentiated by repetitive stimulation (100 T, 1 Hz). None of the neurons belonging to class 1 or class 3 displayed this combination of characteristics. On the basis of differences in response characteristics, it is suggested that the four classes of neurons studied are intercalated in different local neuronal circuits and subserve different functions. It is suggested that some of the class 2D and/or 2S neurons were, in fact, intercalated in the neuronal circuit responsible for the late reflex discharge. Evidence that the neurons studied were not intercalated in the reflex pathway serving the early reflex discharge was also presented.</p>}},
  author       = {{Schouenborg, J. and Sjolund, B. H.}},
  issn         = {{0022-3077}},
  language     = {{eng}},
  month        = {{01}},
  number       = {{5}},
  pages        = {{1108--1121}},
  publisher    = {{American Physiological Society}},
  series       = {{Journal of Neurophysiology}},
  title        = {{Activity evoked by A- and C-afferent fibers in rat dorsal horn neurons and its relation to a flexion reflex}},
  url          = {{http://dx.doi.org/10.1152/jn.1983.50.5.1108}},
  doi          = {{10.1152/jn.1983.50.5.1108}},
  volume       = {{50}},
  year         = {{1983}},
}