Functional properties of primary afferent units probably related to pain mechanisms in primate glabrous skin

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Abstract

High threshold primary afferent units were selected from the population of axons functionally isolated in fine filaments dissected from the median and ulnar nerves of macaque monkeys. In 47 experiments, 536 such units were studied. They comprised 345 A delta and 191 C fiber units; 90 low threshold mechanoreceptive afferents were also studied for comparison. The high threshold units were categorized by observing their responses to mechanical and thermal (53 and 8°C) stimuli applied to their receptive fields in the glabrous skin of the hand. One hundred sixty A delta and 19 C fiber units responded only to mechanical stimulation. One hundred seventy seven A deltas and 164 Cs responded both to mechanical and to thermal stimuli: 79 A deltas and 75 Cs to mechanical and to heat stimuli; 35 A deltas and 13 Cs to mechanical and to cold stimuli; and 63 A deltas and 76 Cs to mechanical, heat, and cold stimulation. Sixteen units responded only to strong thermal stimuli: seven A deltas and five Cs to heat, and one A delta and three Cs to heat and cold. No pure high threshold cold fiber units were encountered. No low threshold mechanoreceptive C afferent units were identified. Mechanical pressure thresholds (determined using calibrated nylon filaments) were, for most units, above 3.97 log mbars (that is, above 9.4 bars). Thermal thresholds (for a response of 3 impulses above background activity in the first 3 s of stimulation) ranged for heat from 41 to over 53°C, and for cold from 30 to below 6°C. Receptive fields for about two thirds of the units were small, graded, usually with a single peak of maximal sensitivity; the remainder had fields of larger size with three or more sensitive spots. For each unit, each of the sensitive loci was responsive to all kinds of stimuli to which that particular unit responded. Virtually all the high threshold units responded better to pointed rather than to blunt mechanical stimuli. Low threshold mechanoreceptive afferents had significantly lower mechanical thresholds than either of the other two populations; innervated receptive fields, with usually a single locus of maximal sensitivity, gave grossly similar responses to either pointed or blunt mechanical stimuli and did not respond to heat stimulation; their condition velocities fell within the A beta range. There was an overlap of conduction velocities between the A beta and A delta fiber groups, but the separation of the two populations on the basis of functional properties was as clear in this overlapping range as between the nonoverlapping range. It is suggested that the dividing line between A beta and A delta fiber groups need not be rigid; a limited but flexible demarcation zone (roughly between 30 and 40 m/s) would include the overlapping tails of the two populations. These experiments demonstrate that there exists a rich diversity of response properties in high threshold A delta and C fiber units. These two fiber groups may serve the dual sensation of pain felt during noxious mechanical or heat stimulation; however, these dual sensations must be attributed to central connections of each group and cannot be explained on the basis of different properties of the primary afferents.

Original languageEnglish (US)
Pages (from-to)71-83
Number of pages13
JournalJournal of Neurophysiology
Volume39
Issue number1
DOIs
StatePublished - Jan 1 1976

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Primates
Hot Temperature
Pain
Skin
Unmyelinated Nerve Fibers
Population
Ulnar Nerve
Median Nerve
Nylons
Macaca
Haplorhini
Axons
Hand
Pressure

Cite this

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title = "Functional properties of primary afferent units probably related to pain mechanisms in primate glabrous skin",
abstract = "High threshold primary afferent units were selected from the population of axons functionally isolated in fine filaments dissected from the median and ulnar nerves of macaque monkeys. In 47 experiments, 536 such units were studied. They comprised 345 A delta and 191 C fiber units; 90 low threshold mechanoreceptive afferents were also studied for comparison. The high threshold units were categorized by observing their responses to mechanical and thermal (53 and 8°C) stimuli applied to their receptive fields in the glabrous skin of the hand. One hundred sixty A delta and 19 C fiber units responded only to mechanical stimulation. One hundred seventy seven A deltas and 164 Cs responded both to mechanical and to thermal stimuli: 79 A deltas and 75 Cs to mechanical and to heat stimuli; 35 A deltas and 13 Cs to mechanical and to cold stimuli; and 63 A deltas and 76 Cs to mechanical, heat, and cold stimulation. Sixteen units responded only to strong thermal stimuli: seven A deltas and five Cs to heat, and one A delta and three Cs to heat and cold. No pure high threshold cold fiber units were encountered. No low threshold mechanoreceptive C afferent units were identified. Mechanical pressure thresholds (determined using calibrated nylon filaments) were, for most units, above 3.97 log mbars (that is, above 9.4 bars). Thermal thresholds (for a response of 3 impulses above background activity in the first 3 s of stimulation) ranged for heat from 41 to over 53°C, and for cold from 30 to below 6°C. Receptive fields for about two thirds of the units were small, graded, usually with a single peak of maximal sensitivity; the remainder had fields of larger size with three or more sensitive spots. For each unit, each of the sensitive loci was responsive to all kinds of stimuli to which that particular unit responded. Virtually all the high threshold units responded better to pointed rather than to blunt mechanical stimuli. Low threshold mechanoreceptive afferents had significantly lower mechanical thresholds than either of the other two populations; innervated receptive fields, with usually a single locus of maximal sensitivity, gave grossly similar responses to either pointed or blunt mechanical stimuli and did not respond to heat stimulation; their condition velocities fell within the A beta range. There was an overlap of conduction velocities between the A beta and A delta fiber groups, but the separation of the two populations on the basis of functional properties was as clear in this overlapping range as between the nonoverlapping range. It is suggested that the dividing line between A beta and A delta fiber groups need not be rigid; a limited but flexible demarcation zone (roughly between 30 and 40 m/s) would include the overlapping tails of the two populations. These experiments demonstrate that there exists a rich diversity of response properties in high threshold A delta and C fiber units. These two fiber groups may serve the dual sensation of pain felt during noxious mechanical or heat stimulation; however, these dual sensations must be attributed to central connections of each group and cannot be explained on the basis of different properties of the primary afferents.",
author = "Georgopoulos, {A. P.}",
year = "1976",
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T1 - Functional properties of primary afferent units probably related to pain mechanisms in primate glabrous skin

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N2 - High threshold primary afferent units were selected from the population of axons functionally isolated in fine filaments dissected from the median and ulnar nerves of macaque monkeys. In 47 experiments, 536 such units were studied. They comprised 345 A delta and 191 C fiber units; 90 low threshold mechanoreceptive afferents were also studied for comparison. The high threshold units were categorized by observing their responses to mechanical and thermal (53 and 8°C) stimuli applied to their receptive fields in the glabrous skin of the hand. One hundred sixty A delta and 19 C fiber units responded only to mechanical stimulation. One hundred seventy seven A deltas and 164 Cs responded both to mechanical and to thermal stimuli: 79 A deltas and 75 Cs to mechanical and to heat stimuli; 35 A deltas and 13 Cs to mechanical and to cold stimuli; and 63 A deltas and 76 Cs to mechanical, heat, and cold stimulation. Sixteen units responded only to strong thermal stimuli: seven A deltas and five Cs to heat, and one A delta and three Cs to heat and cold. No pure high threshold cold fiber units were encountered. No low threshold mechanoreceptive C afferent units were identified. Mechanical pressure thresholds (determined using calibrated nylon filaments) were, for most units, above 3.97 log mbars (that is, above 9.4 bars). Thermal thresholds (for a response of 3 impulses above background activity in the first 3 s of stimulation) ranged for heat from 41 to over 53°C, and for cold from 30 to below 6°C. Receptive fields for about two thirds of the units were small, graded, usually with a single peak of maximal sensitivity; the remainder had fields of larger size with three or more sensitive spots. For each unit, each of the sensitive loci was responsive to all kinds of stimuli to which that particular unit responded. Virtually all the high threshold units responded better to pointed rather than to blunt mechanical stimuli. Low threshold mechanoreceptive afferents had significantly lower mechanical thresholds than either of the other two populations; innervated receptive fields, with usually a single locus of maximal sensitivity, gave grossly similar responses to either pointed or blunt mechanical stimuli and did not respond to heat stimulation; their condition velocities fell within the A beta range. There was an overlap of conduction velocities between the A beta and A delta fiber groups, but the separation of the two populations on the basis of functional properties was as clear in this overlapping range as between the nonoverlapping range. It is suggested that the dividing line between A beta and A delta fiber groups need not be rigid; a limited but flexible demarcation zone (roughly between 30 and 40 m/s) would include the overlapping tails of the two populations. These experiments demonstrate that there exists a rich diversity of response properties in high threshold A delta and C fiber units. These two fiber groups may serve the dual sensation of pain felt during noxious mechanical or heat stimulation; however, these dual sensations must be attributed to central connections of each group and cannot be explained on the basis of different properties of the primary afferents.

AB - High threshold primary afferent units were selected from the population of axons functionally isolated in fine filaments dissected from the median and ulnar nerves of macaque monkeys. In 47 experiments, 536 such units were studied. They comprised 345 A delta and 191 C fiber units; 90 low threshold mechanoreceptive afferents were also studied for comparison. The high threshold units were categorized by observing their responses to mechanical and thermal (53 and 8°C) stimuli applied to their receptive fields in the glabrous skin of the hand. One hundred sixty A delta and 19 C fiber units responded only to mechanical stimulation. One hundred seventy seven A deltas and 164 Cs responded both to mechanical and to thermal stimuli: 79 A deltas and 75 Cs to mechanical and to heat stimuli; 35 A deltas and 13 Cs to mechanical and to cold stimuli; and 63 A deltas and 76 Cs to mechanical, heat, and cold stimulation. Sixteen units responded only to strong thermal stimuli: seven A deltas and five Cs to heat, and one A delta and three Cs to heat and cold. No pure high threshold cold fiber units were encountered. No low threshold mechanoreceptive C afferent units were identified. Mechanical pressure thresholds (determined using calibrated nylon filaments) were, for most units, above 3.97 log mbars (that is, above 9.4 bars). Thermal thresholds (for a response of 3 impulses above background activity in the first 3 s of stimulation) ranged for heat from 41 to over 53°C, and for cold from 30 to below 6°C. Receptive fields for about two thirds of the units were small, graded, usually with a single peak of maximal sensitivity; the remainder had fields of larger size with three or more sensitive spots. For each unit, each of the sensitive loci was responsive to all kinds of stimuli to which that particular unit responded. Virtually all the high threshold units responded better to pointed rather than to blunt mechanical stimuli. Low threshold mechanoreceptive afferents had significantly lower mechanical thresholds than either of the other two populations; innervated receptive fields, with usually a single locus of maximal sensitivity, gave grossly similar responses to either pointed or blunt mechanical stimuli and did not respond to heat stimulation; their condition velocities fell within the A beta range. There was an overlap of conduction velocities between the A beta and A delta fiber groups, but the separation of the two populations on the basis of functional properties was as clear in this overlapping range as between the nonoverlapping range. It is suggested that the dividing line between A beta and A delta fiber groups need not be rigid; a limited but flexible demarcation zone (roughly between 30 and 40 m/s) would include the overlapping tails of the two populations. These experiments demonstrate that there exists a rich diversity of response properties in high threshold A delta and C fiber units. These two fiber groups may serve the dual sensation of pain felt during noxious mechanical or heat stimulation; however, these dual sensations must be attributed to central connections of each group and cannot be explained on the basis of different properties of the primary afferents.

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