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Pain and Nociception

Edward R. Perl

10.1002/cphy.cp010320

Source: Supplement 3: Handbook of Physiology, The Nervous System, Sensory Processes

Originally published: 1984

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Concepts and Theories
2 Pain as A Physiological Reaction
3 Aberrant Pain
3.1 Inflammation and Hyperalgesia
3.2 Referred Pain
3.3 Pain Associated With Pathology of Nervous System
4 Primary Afferent Neurons
4.1 Afferent Fiber Size and Quality of Pain
4.2 Identity of Receptive Units
4.3 Noxious Stimulation of Low‐Threshold Sense Organs
4.4 Relationship of Nociceptor Activity to Pain
4.5 Chemical Mediators
4.6 Central Terminations of Primary Afferent Fibers
5 Ascending Sensory Pathways
5.1 Defining Pathways for Pain Sensation
5.2 Selectively Nociceptive Neurons of Spinal Cord and Trigeminal Nuclei
5.3 Nonselectively Nociceptive Excitation
5.4 Origins of Spinothalamic and Related Systems
5.5 Functional Attributes of Neurons Projecting Over Ventral Quadrant Tracts
5.6 Projection Pathways for the Face
5.7 Other Ascending Pathways
5.8 Brain Stem, Hypothalamic, and Thalamic Components
5.9 Cerebral Cortex
6 Modulation of Nociceptive Neurons
6.1 Afferent Modulation
6.2 Descending Effects
6.3 Opiate Receptors, Opioids, and Endorphins
6.4 Cellular Mechanisms of Modulation
6.5 Higher Level Interactions
6.6 Functional Significance of Modulatory Mechanisms
7 Recapitulation
Figure 1. Figure 1.

Recordings from cutaneous nerve of a man. A: response evoked by stimulus strength sufficient to activate all myelinated (A) and unmyelinated (C) nerve fibers. Deflections are marked for calculated conduction velocity in m/s: 100 is equivalent to A‐α,β‐fiber activity, 25 to A‐δ‐fiber activity and 1.5 to C‐fiber activity. B: response evoked by stimulus strong enough to elicit report of pain by conscious subject; this intensity activated only myelinated fibers contributing to deflections marked 100 (A‐α,β‐fiber) and 25 (A‐δ‐fiber).

From Heinbecker et al. Arch. Neurol. Psychiatry 29: 771–789, 1933. Copyright 1933, American Medical Association
Figure 2. Figure 2.

Responses of cutaneous mechanical nociceptor (highthreshold mechanoreceptor) of cat. Upper traces record action potentials and lower trace inflections indicate magnitude and timing, or both, of the stimulus. A: skin pinch with blunt forceps. B: pressure with needle tip. C: pinch with serrated forceps. D: padded clip pinched center of receptive field with maintained pressure of 35 g/mm2. Afferent fiber's conduction velocity, 29 m/s. Strain gauge calibrations of stimulus force (in g) appear at right in A and B. Time calibration, 0.5 s in A, B, and C; 8.0 s in D.

From Burgess and Perl 84
Figure 3. Figure 3.

Typical receptive fields for individual mechanical nociceptors (high‐threshold mechanoreceptors) of monkey, determined for units of the posterior femoral cutaneous nerve (A‐C) or radial nerve (D‐G).

From Perl 478
Figure 4. Figure 4.

Responses of polymodal nociceptor in hairy skin of monkey. Lower traces: sharp probe displaced the skin at 10‐s intervals by increasing amounts. Upper traces: each dot represents an impulse; the reciprocal of the interval between each impulse and its antecedent (vertical axis) is plotted at the time of the impulse (horizontal axis). B: stimulation became noxious; in C and D skin was penetrated.

From Kumazawa and Perl 348
Figure 5. Figure 5.

Responses of single polymodal nociceptor in conscious man. Activity recorded from peroneal nerve at knee during cutaneous stimulation of receptive field on big toe. Lines below records and deflections in strain gauge signals (lowermost traces in D and E) indicate time course of stimuli. A: response to single electric shock. B: 2 g of sustained force (von Frey hair) reported as “itch” after 2 s. C: repeated, firm stroking with small stick provoked “slight aching.” D: 15 g of force from blunt probe perceived as “pressure.” E: 5 g of force from pointed probe elicited “slight pain.” F: needle prick evoked “pricking and delayed pain.” G: itching powder applied to receptive field reported as “burning itch.” H: nettle contacting skin caused “pain followed by itch.” I: hot probe touched to skin described as initial “pricking” sensation that became “burning pain.”

From Torebjörk 601
Figure 6. Figure 6.

Responses of polymodal nociceptor in hairy skin of monkey. Receptive field heated by small contact thermode every 200 s as illustrated; > 48°C was judged noxious. Discharge plotted as in Figure 4. A, B, and C represent first, third, and fifth heating cycles, respectively. Note successively lower thresholds and increased activity with each repetition.

From Kumazawa and Perl 348
Figure 7. Figure 7.

Subjective judgments of heat intensity by human observers. Perceived sensation (vertical axis) scaled from 1 (background) to 7 (very strong pain); faint pain rated 4. Stimulus was an infrared laser beam that repeatedly heated 7.5‐mm diam. spot on skin of thenar eminence at 28‐s intervals. Category ratings for each intensity of stimulation averaged across all three subjects; mean ratings plotted for each of six trials.

Adapted from LaMotte and Campbell 358
Figure 8. Figure 8.

Levels of substance P in feline spinal cord for segments L5 to S1. Left: 11 days after unilateral sectioning of dorsal roots caudal to L5. Right: intact side. Concentrations are stated as 10−10 mol/g wet wt.

From Takahashi and Otsuka 593
Figure 9. Figure 9.

Immunofluorescent staining of neurons binding antibodies to somatostatin (upper) and substance P (lower) in consecutive sections of dorsal horn of spinal cord in rat; thoracic level. DR, dorsal root. Arrow points dorsally. Although immunoreactivity was distributed similarly, different cell bodies were involved in each case and substance P staining concentrated more superficially. × 160.

From Hökfelt et al. 259
Figure 10. Figure 10.

Superficial dorsal horn loci of unitary electrophysiological recordings for cutaneously excited elements in monkey. Units grouped according to most effective type of primary afferent excitatory input. The dominant excitation was from mechanical nociceptors with fine myelinated fibers for A; from low‐threshold thermoreceptors with fine myelinated fibers for B; from C‐fiber polymodal nociceptors for C; and from low‐threshold mechanoreceptors with A‐δ‐ and C‐fibers for D. SG, substantia gelatinosa Rolandi.

From Kumazawa and Perl 349
Figure 11. Figure 11.

Superficial spinal dorsal horn: summary of observations and deductions on patterns of primary afferent termination and associated dendritic arborization of certain neurons. A: diagram showing zones of primary afferent termination. Marginal zone (MZ, Rexed's lamina I) indicated by fine dots (outermost layer): region of termination for myelinated fiber nociceptors and myelinated fiber thermoreceptors. Outer substantia gelatinosa (SGo, outer lamina II of Rexed) indicated by closely spaced coarse dots: a region of termination for unmyelinated fiber nociceptors and unmyelinated fiber thermoreceptors. Inner substantia gelatinosa (SGi, inner lamina II of Rexed) indicated by less dense coarse dots: a region of termination for unmyelinated low‐threshold mechanoreceptors, and, at its inner border, also for thinly myelinated low‐threshold mechanoreceptors. Outer nucleus proprius (Rexed's lamina III) indicated by sparse dots: a principal region of terminals from thinly myelinated, low‐threshold mechanoreceptors of skin. Note: borders between zones are not smooth; substantial irregularities are the rule for marginal zone and at interface between substantia gelatinosa and nucleus proprius. B: schematic representation of neuronal dendritic patterns for cells readily excited by primary afferent input. Region depicted corresponds to the bracketed region in A. (All variations not indicated; neurons of region receiving major excitation from other sources have not been considered.) a, Neuron with large receptive field showing excitatory convergence from both rapidly and slowly conducting afferent fibers from a variety of receptor types; b, nociceptive neuron or innocuous thermoreceptive neuron with excitation dominated by thinly myelinated primary afferent units. Neurons of the type illustrated by b have major dendritic arborizations slightly more deeply located (in SGo) when primary afferent excitation is largely derived from unmyelinated dorsal root fibers; c, nociceptive neuron with excitation by unmyelinated and thinly myelinated fibers; d, low‐threshold mechanoreceptive neuron typically showing marked habituation; excitation may be principally or partially from unmyelinated primary fibers; e, low‐threshold mechanoreceptive neuron of the nucleus proprius.
Figure 12. Figure 12.

Soma locations of spinothalamic tract neurons stained retrogradely by horseradish peroxidase injected into thalamus. Neurons found throughout L7 segment of monkey (upper) and cat (lower) plotted on representative cross‐section with lamination as proposed by Rexed. Left side is contralateral to injection site.

Adapted from Trevino and Carstens 608
Figure 13. Figure 13.

Locations of recording sites for functionally characterized units of trigeminal nucleus caudalis and reticular formation of monkey; all antidromically activated from contralateral thalamus. Distance caudal to obex shown (in mm) above each section. Broken lines separate substantia gelatinosa (SG) from marginal zone (MAR) and magnocellular layer (MAG) and mark boundary between ventral MAG and lateral reticular formation. RF, receptive field. Classes 1 and 2: no thermal responsiveness; vigorously excited by gentle mechanical stimulation of face with no additional response to noxious stimulation. Class 3: warming sometimes effective; noxious heat often effective; incremental response to mechanical stimulation graded from gentle to noxious intensities. Class 4: some response to warming or noxious heat; noxious mechanical stimulation most effective. Class 5: noxious mechanical stimulation solely excitatory.

From Price et al. 503
Figure 14. Figure 14.

Observations made during three penetrations through ventralis posterior lateralis (VPL) hindlimb region in one experiment. Numbers shown refer to stereotaxic coordinates in millimeters. Grid represents horizontal zero plane, 10 mm above interaural line. A, anterior; R, right in lateral axis; H, vertical. Approximate location and size of receptive fields of units encountered in vertical penetrations appear on outline drawings. Solid black is used for highthreshold (HT) units and shading for lowthreshold mechanoreceptive (LTM) units.

From Honda et al. 707
Figure 15. Figure 15.

Inhibition of nociceptive spinal unit by peripheral afferent volleys. Impulses/s (ordinate) are plotted as a function of time for a neural element of the L6‐L7 feline dorsal horn. Discharge evoked by noxious heating of skin (bar above graph). Ipsilateral tibial nerve stimulated at A‐α,β‐fiber intensity (Ti 2.6T) and at A‐α (Ti 1.4T) for period indicated by the shorter bars. Ti, tibial nerve; T, threshold.

From Cervero et al. 100
Figure 16. Figure 16.

Effect of dorsal column lesion on inhibition of selectively nociceptive spinal neuron antidromically excited from contralateral thalamus. A: response of unit to electrical shock applied to skin of receptive field. B: electrical stimulation of dorsal column at C7‐C8 20 ms before cutaneous stimulation. C: varying interval between dorsal column and cutaneous stimuli altered number of discharges relative to control response (% on ordinate), as shown by curve through open circles; lesion of dorsal column eliminated inhibition (crosses); moving stimulus electrode caudal to lesion restored inhibition (filled circles). Each point graphed is mean number of discharges for ten trials; bars represent standard deviation. D: maximal extent of dorsal column lesion.

From Foreman et al. 172. In: Advances in Pain Research and Therapy, edited by J. J. Bonica and D. Albe‐Fessard. © 1976, with permission of Raven Press, New York
Figure 17. Figure 17.

Cross sections of three levels of lower brain stem (A‐C) and spinal cord (D) showing distributions of some enkephalin‐positive (left side) and substance P‐positive (right) cell bodies (asterisks) and nerve terminals (dots). AF, anterior funiculus; cod, n. cochlearis dorsalis; DF, dorsal funiculus; FLM, fasciculus longitudinalis medialis; gr, n. gracilis; io, n. olivaris inferior; LF, lateral funiculus; LL, lemniscus lateralis; LM, lemniscus medialis; nrv, n. reticularis medullae oblongatae pars ventralis; nts, n. tractus solitarii; ntV, spinal trigeminal nucleus; ntVd, same, pars dorsomedialis; nVII, n. originis nervi facialis; P, tractus corticospinalis; PCI, pedunculus cerebellaris inferior; PCS, pedunculus cerebellaris superior; rd, n. raphe dorsalis; rgi, n. reticularis gigantocellularis; rl, n. reticularis lateralis; rm, n. raphe magnus; rp, n. raphe pallidus; SGC, substantia grisea centralis; TSV, tractus spinalis nervi trigemini; vm, n. vestibularis medialis.

From Hökfelt et al. 262


Figure 1.

Recordings from cutaneous nerve of a man. A: response evoked by stimulus strength sufficient to activate all myelinated (A) and unmyelinated (C) nerve fibers. Deflections are marked for calculated conduction velocity in m/s: 100 is equivalent to A‐α,β‐fiber activity, 25 to A‐δ‐fiber activity and 1.5 to C‐fiber activity. B: response evoked by stimulus strong enough to elicit report of pain by conscious subject; this intensity activated only myelinated fibers contributing to deflections marked 100 (A‐α,β‐fiber) and 25 (A‐δ‐fiber).

From Heinbecker et al. Arch. Neurol. Psychiatry 29: 771–789, 1933. Copyright 1933, American Medical Association


Figure 2.

Responses of cutaneous mechanical nociceptor (highthreshold mechanoreceptor) of cat. Upper traces record action potentials and lower trace inflections indicate magnitude and timing, or both, of the stimulus. A: skin pinch with blunt forceps. B: pressure with needle tip. C: pinch with serrated forceps. D: padded clip pinched center of receptive field with maintained pressure of 35 g/mm2. Afferent fiber's conduction velocity, 29 m/s. Strain gauge calibrations of stimulus force (in g) appear at right in A and B. Time calibration, 0.5 s in A, B, and C; 8.0 s in D.

From Burgess and Perl 84


Figure 3.

Typical receptive fields for individual mechanical nociceptors (high‐threshold mechanoreceptors) of monkey, determined for units of the posterior femoral cutaneous nerve (A‐C) or radial nerve (D‐G).

From Perl 478


Figure 4.

Responses of polymodal nociceptor in hairy skin of monkey. Lower traces: sharp probe displaced the skin at 10‐s intervals by increasing amounts. Upper traces: each dot represents an impulse; the reciprocal of the interval between each impulse and its antecedent (vertical axis) is plotted at the time of the impulse (horizontal axis). B: stimulation became noxious; in C and D skin was penetrated.

From Kumazawa and Perl 348


Figure 5.

Responses of single polymodal nociceptor in conscious man. Activity recorded from peroneal nerve at knee during cutaneous stimulation of receptive field on big toe. Lines below records and deflections in strain gauge signals (lowermost traces in D and E) indicate time course of stimuli. A: response to single electric shock. B: 2 g of sustained force (von Frey hair) reported as “itch” after 2 s. C: repeated, firm stroking with small stick provoked “slight aching.” D: 15 g of force from blunt probe perceived as “pressure.” E: 5 g of force from pointed probe elicited “slight pain.” F: needle prick evoked “pricking and delayed pain.” G: itching powder applied to receptive field reported as “burning itch.” H: nettle contacting skin caused “pain followed by itch.” I: hot probe touched to skin described as initial “pricking” sensation that became “burning pain.”

From Torebjörk 601


Figure 6.

Responses of polymodal nociceptor in hairy skin of monkey. Receptive field heated by small contact thermode every 200 s as illustrated; > 48°C was judged noxious. Discharge plotted as in Figure 4. A, B, and C represent first, third, and fifth heating cycles, respectively. Note successively lower thresholds and increased activity with each repetition.

From Kumazawa and Perl 348


Figure 7.

Subjective judgments of heat intensity by human observers. Perceived sensation (vertical axis) scaled from 1 (background) to 7 (very strong pain); faint pain rated 4. Stimulus was an infrared laser beam that repeatedly heated 7.5‐mm diam. spot on skin of thenar eminence at 28‐s intervals. Category ratings for each intensity of stimulation averaged across all three subjects; mean ratings plotted for each of six trials.

Adapted from LaMotte and Campbell 358


Figure 8.

Levels of substance P in feline spinal cord for segments L5 to S1. Left: 11 days after unilateral sectioning of dorsal roots caudal to L5. Right: intact side. Concentrations are stated as 10−10 mol/g wet wt.

From Takahashi and Otsuka 593


Figure 9.

Immunofluorescent staining of neurons binding antibodies to somatostatin (upper) and substance P (lower) in consecutive sections of dorsal horn of spinal cord in rat; thoracic level. DR, dorsal root. Arrow points dorsally. Although immunoreactivity was distributed similarly, different cell bodies were involved in each case and substance P staining concentrated more superficially. × 160.

From Hökfelt et al. 259


Figure 10.

Superficial dorsal horn loci of unitary electrophysiological recordings for cutaneously excited elements in monkey. Units grouped according to most effective type of primary afferent excitatory input. The dominant excitation was from mechanical nociceptors with fine myelinated fibers for A; from low‐threshold thermoreceptors with fine myelinated fibers for B; from C‐fiber polymodal nociceptors for C; and from low‐threshold mechanoreceptors with A‐δ‐ and C‐fibers for D. SG, substantia gelatinosa Rolandi.

From Kumazawa and Perl 349


Figure 11.

Superficial spinal dorsal horn: summary of observations and deductions on patterns of primary afferent termination and associated dendritic arborization of certain neurons. A: diagram showing zones of primary afferent termination. Marginal zone (MZ, Rexed's lamina I) indicated by fine dots (outermost layer): region of termination for myelinated fiber nociceptors and myelinated fiber thermoreceptors. Outer substantia gelatinosa (SGo, outer lamina II of Rexed) indicated by closely spaced coarse dots: a region of termination for unmyelinated fiber nociceptors and unmyelinated fiber thermoreceptors. Inner substantia gelatinosa (SGi, inner lamina II of Rexed) indicated by less dense coarse dots: a region of termination for unmyelinated low‐threshold mechanoreceptors, and, at its inner border, also for thinly myelinated low‐threshold mechanoreceptors. Outer nucleus proprius (Rexed's lamina III) indicated by sparse dots: a principal region of terminals from thinly myelinated, low‐threshold mechanoreceptors of skin. Note: borders between zones are not smooth; substantial irregularities are the rule for marginal zone and at interface between substantia gelatinosa and nucleus proprius. B: schematic representation of neuronal dendritic patterns for cells readily excited by primary afferent input. Region depicted corresponds to the bracketed region in A. (All variations not indicated; neurons of region receiving major excitation from other sources have not been considered.) a, Neuron with large receptive field showing excitatory convergence from both rapidly and slowly conducting afferent fibers from a variety of receptor types; b, nociceptive neuron or innocuous thermoreceptive neuron with excitation dominated by thinly myelinated primary afferent units. Neurons of the type illustrated by b have major dendritic arborizations slightly more deeply located (in SGo) when primary afferent excitation is largely derived from unmyelinated dorsal root fibers; c, nociceptive neuron with excitation by unmyelinated and thinly myelinated fibers; d, low‐threshold mechanoreceptive neuron typically showing marked habituation; excitation may be principally or partially from unmyelinated primary fibers; e, low‐threshold mechanoreceptive neuron of the nucleus proprius.



Figure 12.

Soma locations of spinothalamic tract neurons stained retrogradely by horseradish peroxidase injected into thalamus. Neurons found throughout L7 segment of monkey (upper) and cat (lower) plotted on representative cross‐section with lamination as proposed by Rexed. Left side is contralateral to injection site.

Adapted from Trevino and Carstens 608


Figure 13.

Locations of recording sites for functionally characterized units of trigeminal nucleus caudalis and reticular formation of monkey; all antidromically activated from contralateral thalamus. Distance caudal to obex shown (in mm) above each section. Broken lines separate substantia gelatinosa (SG) from marginal zone (MAR) and magnocellular layer (MAG) and mark boundary between ventral MAG and lateral reticular formation. RF, receptive field. Classes 1 and 2: no thermal responsiveness; vigorously excited by gentle mechanical stimulation of face with no additional response to noxious stimulation. Class 3: warming sometimes effective; noxious heat often effective; incremental response to mechanical stimulation graded from gentle to noxious intensities. Class 4: some response to warming or noxious heat; noxious mechanical stimulation most effective. Class 5: noxious mechanical stimulation solely excitatory.

From Price et al. 503


Figure 14.

Observations made during three penetrations through ventralis posterior lateralis (VPL) hindlimb region in one experiment. Numbers shown refer to stereotaxic coordinates in millimeters. Grid represents horizontal zero plane, 10 mm above interaural line. A, anterior; R, right in lateral axis; H, vertical. Approximate location and size of receptive fields of units encountered in vertical penetrations appear on outline drawings. Solid black is used for highthreshold (HT) units and shading for lowthreshold mechanoreceptive (LTM) units.

From Honda et al. 707


Figure 15.

Inhibition of nociceptive spinal unit by peripheral afferent volleys. Impulses/s (ordinate) are plotted as a function of time for a neural element of the L6‐L7 feline dorsal horn. Discharge evoked by noxious heating of skin (bar above graph). Ipsilateral tibial nerve stimulated at A‐α,β‐fiber intensity (Ti 2.6T) and at A‐α (Ti 1.4T) for period indicated by the shorter bars. Ti, tibial nerve; T, threshold.

From Cervero et al. 100


Figure 16.

Effect of dorsal column lesion on inhibition of selectively nociceptive spinal neuron antidromically excited from contralateral thalamus. A: response of unit to electrical shock applied to skin of receptive field. B: electrical stimulation of dorsal column at C7‐C8 20 ms before cutaneous stimulation. C: varying interval between dorsal column and cutaneous stimuli altered number of discharges relative to control response (% on ordinate), as shown by curve through open circles; lesion of dorsal column eliminated inhibition (crosses); moving stimulus electrode caudal to lesion restored inhibition (filled circles). Each point graphed is mean number of discharges for ten trials; bars represent standard deviation. D: maximal extent of dorsal column lesion.

From Foreman et al. 172. In: Advances in Pain Research and Therapy, edited by J. J. Bonica and D. Albe‐Fessard. © 1976, with permission of Raven Press, New York


Figure 17.

Cross sections of three levels of lower brain stem (A‐C) and spinal cord (D) showing distributions of some enkephalin‐positive (left side) and substance P‐positive (right) cell bodies (asterisks) and nerve terminals (dots). AF, anterior funiculus; cod, n. cochlearis dorsalis; DF, dorsal funiculus; FLM, fasciculus longitudinalis medialis; gr, n. gracilis; io, n. olivaris inferior; LF, lateral funiculus; LL, lemniscus lateralis; LM, lemniscus medialis; nrv, n. reticularis medullae oblongatae pars ventralis; nts, n. tractus solitarii; ntV, spinal trigeminal nucleus; ntVd, same, pars dorsomedialis; nVII, n. originis nervi facialis; P, tractus corticospinalis; PCI, pedunculus cerebellaris inferior; PCS, pedunculus cerebellaris superior; rd, n. raphe dorsalis; rgi, n. reticularis gigantocellularis; rl, n. reticularis lateralis; rm, n. raphe magnus; rp, n. raphe pallidus; SGC, substantia grisea centralis; TSV, tractus spinalis nervi trigemini; vm, n. vestibularis medialis.

From Hökfelt et al. 262
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Article Title: Pain and Nociception
 

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Edward R. Perl. Pain and Nociception. Compr Physiol 2011, Supplement 3: Handbook of Physiology, The Nervous System, Sensory Processes: 915-975. First published in print 1984. doi: 10.1002/cphy.cp010320