Skip to main content
Erschienen in: Journal of Neural Transmission 4/2020

09.08.2019 | Neurology and Preclinical Neurological Studies - Review Article

The development of pain circuits and unique effects of neonatal injury

verfasst von: Chelsie L. Brewer, Mark L. Baccei

Erschienen in: Journal of Neural Transmission | Ausgabe 4/2020

Einloggen, um Zugang zu erhalten

Abstract

Pain is a necessary sensation that prevents further tissue damage, but can be debilitating and detrimental in daily life under chronic conditions. Neuronal activity strongly regulates the maturation of the somatosensory system, and aberrant sensory input caused by injury or inflammation during critical periods of early postnatal development can have prolonged, detrimental effects on pain processing. This review will outline the maturation of neuronal circuits responsible for the transmission of nociceptive signals and the generation of pain sensation—involving peripheral sensory neurons, the spinal cord dorsal horn, and brain—in addition to the influences of the neuroimmune system on somatosensation. This summary will also highlight the unique effects of neonatal tissue injury on the maturation of these systems and subsequent consequences for adult somatosensation. Ultimately, this review emphasizes the need to account for age as an independent variable in basic and clinical pain research, and importantly, to consider the distinct qualities of the pediatric population when designing novel strategies for pain management.
Literatur
Zurück zum Zitat Abraira VE, Ginty DD (2013) The sensory neurons of touch Neuron 79:618–639PubMed Abraira VE, Ginty DD (2013) The sensory neurons of touch Neuron 79:618–639PubMed
Zurück zum Zitat Andrews K, Fitzgerald M (1994) The cutaneous withdrawal reflex in human neonates: sensitization, receptive fields, and the effects of contralateral stimulation. Pain 56:95–101PubMed Andrews K, Fitzgerald M (1994) The cutaneous withdrawal reflex in human neonates: sensitization, receptive fields, and the effects of contralateral stimulation. Pain 56:95–101PubMed
Zurück zum Zitat Antal M, Petko M, Polgar E, Heizmann C, Storm-Mathisen J (1996) Direct evidence of an extensive GABAergic innervation of the spinal dorsal horn by fibres descending from the rostral ventromedial medulla. Neuroscience 73:509–518PubMed Antal M, Petko M, Polgar E, Heizmann C, Storm-Mathisen J (1996) Direct evidence of an extensive GABAergic innervation of the spinal dorsal horn by fibres descending from the rostral ventromedial medulla. Neuroscience 73:509–518PubMed
Zurück zum Zitat Baccei ML, Bardoni R, Fitzgerald M (2003) Development of nociceptive synaptic inputs to the neonatal rat dorsal horn: glutamate release by capsaicin and menthol. J Physiol 549:231–242PubMedPubMedCentral Baccei ML, Bardoni R, Fitzgerald M (2003) Development of nociceptive synaptic inputs to the neonatal rat dorsal horn: glutamate release by capsaicin and menthol. J Physiol 549:231–242PubMedPubMedCentral
Zurück zum Zitat Bao J, Li JJ, Perl ER (1998) Differences in Ca2+ channels governing generation of miniature and evoked excitatory synaptic currents in spinal laminae I and II. J Neurosci 18:8740–8750PubMedPubMedCentral Bao J, Li JJ, Perl ER (1998) Differences in Ca2+ channels governing generation of miniature and evoked excitatory synaptic currents in spinal laminae I and II. J Neurosci 18:8740–8750PubMedPubMedCentral
Zurück zum Zitat Beggs S, Torsney C, Drew LJ, Fitzgerald M (2002) The postnatal reorganization of primary afferent input and dorsal horn cell receptive fields in the rat spinal cord is an activity-dependent process. Eur J Neurosci 16:1249–1258PubMed Beggs S, Torsney C, Drew LJ, Fitzgerald M (2002) The postnatal reorganization of primary afferent input and dorsal horn cell receptive fields in the rat spinal cord is an activity-dependent process. Eur J Neurosci 16:1249–1258PubMed
Zurück zum Zitat Beggs S, Alvares D, Moss A, Currie G, Middleton J, Salter MW, Fitzgerald M (2012a) A role for NT-3 in the hyperinnervation of neonatally wounded skin. PAIN® 153:2133–2139 Beggs S, Alvares D, Moss A, Currie G, Middleton J, Salter MW, Fitzgerald M (2012a) A role for NT-3 in the hyperinnervation of neonatally wounded skin. PAIN® 153:2133–2139
Zurück zum Zitat Benn SC, Costigan M, Tate S, Fitzgerald M, Woolf CJ (2001) Developmental expression of the TTX-resistant voltage-gated sodium channels Nav1. 8 (SNS) and Nav1. 9 (SNS2) in primary sensory neurons. J Neurosci 21:6077–6085PubMedPubMedCentral Benn SC, Costigan M, Tate S, Fitzgerald M, Woolf CJ (2001) Developmental expression of the TTX-resistant voltage-gated sodium channels Nav1. 8 (SNS) and Nav1. 9 (SNS2) in primary sensory neurons. J Neurosci 21:6077–6085PubMedPubMedCentral
Zurück zum Zitat Bird CM, Burgess N (2008) The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 9:182PubMed Bird CM, Burgess N (2008) The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 9:182PubMed
Zurück zum Zitat Bourane S et al (2015) Gate control of mechanical itch by a subpopulation of spinal cord interneurons. Science 350:550–554PubMedPubMedCentral Bourane S et al (2015) Gate control of mechanical itch by a subpopulation of spinal cord interneurons. Science 350:550–554PubMedPubMedCentral
Zurück zum Zitat Bremner LR, Fitzgerald M (2008) Postnatal tuning of cutaneous inhibitory receptive fields in the rat. J Physiol 586:1529–1537PubMed Bremner LR, Fitzgerald M (2008) Postnatal tuning of cutaneous inhibitory receptive fields in the rat. J Physiol 586:1529–1537PubMed
Zurück zum Zitat Bremner L, Fitzgerald M, Baccei M (2006) Functional GABAA-receptor-mediated inhibition in the neonatal dorsal horn. J Neurophysiol 95:3893–3897PubMed Bremner L, Fitzgerald M, Baccei M (2006) Functional GABAA-receptor-mediated inhibition in the neonatal dorsal horn. J Neurophysiol 95:3893–3897PubMed
Zurück zum Zitat Chang P, Fabrizi L, Olhede S, Fitzgerald M (2016) The development of nociceptive network activity in the somatosensory cortex of freely moving rat pups. Cerebral Cortex 26(12):1–11 Chang P, Fabrizi L, Olhede S, Fitzgerald M (2016) The development of nociceptive network activity in the somatosensory cortex of freely moving rat pups. Cerebral Cortex 26(12):1–11
Zurück zum Zitat Chevalier M, Toporikova N, Simmers J, Thoby-Brisson M (2016) Development of pacemaker properties and rhythmogenic mechanisms in the mouse embryonic respiratory network. eLife 5:e16125PubMedPubMedCentral Chevalier M, Toporikova N, Simmers J, Thoby-Brisson M (2016) Development of pacemaker properties and rhythmogenic mechanisms in the mouse embryonic respiratory network. eLife 5:e16125PubMedPubMedCentral
Zurück zum Zitat Clancy B, Darlington R, Finlay B (2001) Translating developmental time across mammalian species. Neuroscience 105:7–17PubMed Clancy B, Darlington R, Finlay B (2001) Translating developmental time across mammalian species. Neuroscience 105:7–17PubMed
Zurück zum Zitat Coetzee WA et al (1999) Molecular diversity of K+ channels. Ann N Y Acad Sci 868:233–255PubMed Coetzee WA et al (1999) Molecular diversity of K+ channels. Ann N Y Acad Sci 868:233–255PubMed
Zurück zum Zitat Corder G et al (2013) Constitutive μ-opioid receptor activity leads to long-term endogenous analgesia and dependence. Science 341:1394–1399PubMedPubMedCentral Corder G et al (2013) Constitutive μ-opioid receptor activity leads to long-term endogenous analgesia and dependence. Science 341:1394–1399PubMedPubMedCentral
Zurück zum Zitat Cornelissen L et al (2013) Postnatal temporal, spatial and modality tuning of nociceptive cutaneous flexion reflexes in human infants. PloS One 8:e76470PubMedPubMedCentral Cornelissen L et al (2013) Postnatal temporal, spatial and modality tuning of nociceptive cutaneous flexion reflexes in human infants. PloS One 8:e76470PubMedPubMedCentral
Zurück zum Zitat Cunha J, Cunha F, Poole S, Ferreira S (2000) Cytokine-mediated inflammatory hyperalgesia limited by interleukin-1 receptor antagonist. Br J Pharmacol 130:1418–1424PubMedPubMedCentral Cunha J, Cunha F, Poole S, Ferreira S (2000) Cytokine-mediated inflammatory hyperalgesia limited by interleukin-1 receptor antagonist. Br J Pharmacol 130:1418–1424PubMedPubMedCentral
Zurück zum Zitat De Lima J, Alvares D, Hatch DJ, Fitzgerald M (1999) Sensory hyperinnervation after neonatal skin wounding: effect of bupivacaine sciatic nerve block. Br J Anaesth 83:662–664PubMed De Lima J, Alvares D, Hatch DJ, Fitzgerald M (1999) Sensory hyperinnervation after neonatal skin wounding: effect of bupivacaine sciatic nerve block. Br J Anaesth 83:662–664PubMed
Zurück zum Zitat Dickenson AH, Sullivan AF (1987) Evidence for a role of the NMDA receptor in the frequency dependent potentiation of deep rat dorsal horn nociceptive neurones following C fibre stimulation. Neuropharmacology 26:1235–1238PubMed Dickenson AH, Sullivan AF (1987) Evidence for a role of the NMDA receptor in the frequency dependent potentiation of deep rat dorsal horn nociceptive neurones following C fibre stimulation. Neuropharmacology 26:1235–1238PubMed
Zurück zum Zitat Duan B et al (2014) Identification of spinal circuits transmitting and gating mechanical pain. Cell 159:1417–1432PubMedPubMedCentral Duan B et al (2014) Identification of spinal circuits transmitting and gating mechanical pain. Cell 159:1417–1432PubMedPubMedCentral
Zurück zum Zitat Fabrizi L, Slater R, Worley A, Meek J, Boyd S, Olhede S, Fitzgerald M (2011) A shift in sensory processing that enables the developing human brain to discriminate touch from pain. Curr Biol 21:1552–1558PubMedPubMedCentral Fabrizi L, Slater R, Worley A, Meek J, Boyd S, Olhede S, Fitzgerald M (2011) A shift in sensory processing that enables the developing human brain to discriminate touch from pain. Curr Biol 21:1552–1558PubMedPubMedCentral
Zurück zum Zitat Fields H (2004) State-dependent opioid control of pain. Nat Rev Neurosci 5:565PubMed Fields H (2004) State-dependent opioid control of pain. Nat Rev Neurosci 5:565PubMed
Zurück zum Zitat Fitzgerald M (1985) The post-natal development of cutaneous afferent fibre input and receptive field organization in the rat dorsal horn. J Physiol 364:1–18PubMedPubMedCentral Fitzgerald M (1985) The post-natal development of cutaneous afferent fibre input and receptive field organization in the rat dorsal horn. J Physiol 364:1–18PubMedPubMedCentral
Zurück zum Zitat Fitzgerald M, Gibson S (1984) The postnatal physiological and neurochemical development of peripheral sensory C fibres. Neuroscience 13:933–944PubMed Fitzgerald M, Gibson S (1984) The postnatal physiological and neurochemical development of peripheral sensory C fibres. Neuroscience 13:933–944PubMed
Zurück zum Zitat Fitzgerald M, Butcher T, Shortland P (1994) Developmental changes in the laminar termination of A fibre cutaneous sensory afferents in the rat spinal cord dorsal horn. J Comp Neurol 348:225–233PubMed Fitzgerald M, Butcher T, Shortland P (1994) Developmental changes in the laminar termination of A fibre cutaneous sensory afferents in the rat spinal cord dorsal horn. J Comp Neurol 348:225–233PubMed
Zurück zum Zitat Gaskin DJ, Richard P (2012) The economic costs of pain in the United States. J Pain 13:715–724PubMed Gaskin DJ, Richard P (2012) The economic costs of pain in the United States. J Pain 13:715–724PubMed
Zurück zum Zitat Gentile LF et al (2014) Protective immunity and defects in the neonatal and elderly immune response to sepsis. J Immunol 192:3156–3165PubMedPubMedCentral Gentile LF et al (2014) Protective immunity and defects in the neonatal and elderly immune response to sepsis. J Immunol 192:3156–3165PubMedPubMedCentral
Zurück zum Zitat Goksan S et al (2018) The influence of the descending pain modulatory system on infant pain-related brain activity. Elife 7:e37125PubMedPubMedCentral Goksan S et al (2018) The influence of the descending pain modulatory system on infant pain-related brain activity. Elife 7:e37125PubMedPubMedCentral
Zurück zum Zitat Gonzalez DL, Fuchs JL, Droge MH (1993) Distribution of NMDA receptor binding in developing mouse spinal cord. Neurosci Lett 151:134–137PubMed Gonzalez DL, Fuchs JL, Droge MH (1993) Distribution of NMDA receptor binding in developing mouse spinal cord. Neurosci Lett 151:134–137PubMed
Zurück zum Zitat Grahn JA, Parkinson JA, Owen AM (2008) The cognitive functions of the caudate nucleus. Prog Neurobiol 86:141–155PubMed Grahn JA, Parkinson JA, Owen AM (2008) The cognitive functions of the caudate nucleus. Prog Neurobiol 86:141–155PubMed
Zurück zum Zitat Granmo M, Petersson P, Schouenborg J (2008) Action-based body maps in the spinal cord emerge from a transitory floating organization. J Neurosci 28:5494–5503PubMedPubMedCentral Granmo M, Petersson P, Schouenborg J (2008) Action-based body maps in the spinal cord emerge from a transitory floating organization. J Neurosci 28:5494–5503PubMedPubMedCentral
Zurück zum Zitat Hartley C et al (2018) Analgesic efficacy and safety of morphine in the Procedural Pain in Premature Infants (Poppi) study: randomised placebo-controlled trial. Lancet 392:2595–2605PubMedPubMedCentral Hartley C et al (2018) Analgesic efficacy and safety of morphine in the Procedural Pain in Premature Infants (Poppi) study: randomised placebo-controlled trial. Lancet 392:2595–2605PubMedPubMedCentral
Zurück zum Zitat Hasegawa-Ishii S, Inaba M, Umegaki H, Unno K, Wakabayashi K, Shimada A (2016) Endotoxemia-induced cytokine-mediated responses of hippocampal astrocytes transmitted by cells of the brain–immune interface. Sci Rep 6:25457PubMedPubMedCentral Hasegawa-Ishii S, Inaba M, Umegaki H, Unno K, Wakabayashi K, Shimada A (2016) Endotoxemia-induced cytokine-mediated responses of hippocampal astrocytes transmitted by cells of the brain–immune interface. Sci Rep 6:25457PubMedPubMedCentral
Zurück zum Zitat Hathway G, Koch S, Low L, Fitzgerald M (2009) The changing balance of brainstem–spinal cord modulation of pain processing over the first weeks of rat postnatal life. J Physiol 587:2927–2935PubMedPubMedCentral Hathway G, Koch S, Low L, Fitzgerald M (2009) The changing balance of brainstem–spinal cord modulation of pain processing over the first weeks of rat postnatal life. J Physiol 587:2927–2935PubMedPubMedCentral
Zurück zum Zitat Hathway GJ, Vega-Avelaira D, Fitzgerald M (2012) A critical period in the supraspinal control of pain: opioid-dependent changes in brainstem rostroventral medulla function in preadolescence. PAIN® 153:775–783 Hathway GJ, Vega-Avelaira D, Fitzgerald M (2012) A critical period in the supraspinal control of pain: opioid-dependent changes in brainstem rostroventral medulla function in preadolescence. PAIN® 153:775–783
Zurück zum Zitat Hermann C, Hohmeister J, Demirakça S, Zohsel K, Flor H (2006) Long-term alteration of pain sensitivity in school-aged children with early pain experiences. Pain 125:278–285PubMed Hermann C, Hohmeister J, Demirakça S, Zohsel K, Flor H (2006) Long-term alteration of pain sensitivity in school-aged children with early pain experiences. Pain 125:278–285PubMed
Zurück zum Zitat Hohmeister J, Demirakça S, Zohsel K, Flor H, Hermann C (2009) Responses to pain in school-aged children with experience in a neonatal intensive care unit: cognitive aspects and maternal influences. Eur J Pain 13:94–101PubMed Hohmeister J, Demirakça S, Zohsel K, Flor H, Hermann C (2009) Responses to pain in school-aged children with experience in a neonatal intensive care unit: cognitive aspects and maternal influences. Eur J Pain 13:94–101PubMed
Zurück zum Zitat Hohmeister J, Kroll A, Wollgarten-Hadamek I, Zohsel K, Demirakça S, Flor H, Hermann C (2010) Cerebral processing of pain in school-aged children with neonatal nociceptive input: an exploratory fMRI study. Pain 150:257–267PubMed Hohmeister J, Kroll A, Wollgarten-Hadamek I, Zohsel K, Demirakça S, Flor H, Hermann C (2010) Cerebral processing of pain in school-aged children with neonatal nociceptive input: an exploratory fMRI study. Pain 150:257–267PubMed
Zurück zum Zitat Holmberg H, Schouenborg J (1996) Postnatal development of the nociceptive withdrawal reflexes in the rat: a behavioural and electromyographic study. J Physiol 493:239–252PubMedPubMedCentral Holmberg H, Schouenborg J (1996) Postnatal development of the nociceptive withdrawal reflexes in the rat: a behavioural and electromyographic study. J Physiol 493:239–252PubMedPubMedCentral
Zurück zum Zitat Hori Y, Kanda K (1994) Developmental alterations in NMDA receptor-mediated [Ca2+]i elevation in substantia gelatinosa neurons of neonatal rat spinal cord. Brain Res Dev Brain Res 80:141–148PubMed Hori Y, Kanda K (1994) Developmental alterations in NMDA receptor-mediated [Ca2+]i elevation in substantia gelatinosa neurons of neonatal rat spinal cord. Brain Res Dev Brain Res 80:141–148PubMed
Zurück zum Zitat Huang H-W, Wang W-C, Lin C-CK (2010) Influence of age on thermal thresholds, thermal pain thresholds, and reaction time. J Clin Neurosci 17:722–726PubMed Huang H-W, Wang W-C, Lin C-CK (2010) Influence of age on thermal thresholds, thermal pain thresholds, and reaction time. J Clin Neurosci 17:722–726PubMed
Zurück zum Zitat Huang T et al (2019) Identifying the pathways required for coping behaviours associated with sustained pain. Nature 565:86PubMed Huang T et al (2019) Identifying the pathways required for coping behaviours associated with sustained pain. Nature 565:86PubMed
Zurück zum Zitat Hubner CA, Stein V, Hermans-Borgmeyer I, Meyer T, Ballanyi K, Jentsch TJ (2001) Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30:515–524PubMed Hubner CA, Stein V, Hermans-Borgmeyer I, Meyer T, Ballanyi K, Jentsch TJ (2001) Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30:515–524PubMed
Zurück zum Zitat Jackman A, Fitzgerald M (2000) Development of peripheral hindlimb and central spinal cord innervation by subpopulations of dorsal root ganglion cells in the embryonic rat. J Comp Neurol 418:281–298PubMed Jackman A, Fitzgerald M (2000) Development of peripheral hindlimb and central spinal cord innervation by subpopulations of dorsal root ganglion cells in the embryonic rat. J Comp Neurol 418:281–298PubMed
Zurück zum Zitat Kardon AP et al (2014) Dynorphin acts as a neuromodulator to inhibit itch in the dorsal horn of the spinal cord. Neuron 82:573–586PubMedPubMedCentral Kardon AP et al (2014) Dynorphin acts as a neuromodulator to inhibit itch in the dorsal horn of the spinal cord. Neuron 82:573–586PubMedPubMedCentral
Zurück zum Zitat Koch SC, Fitzgerald M (2014) The selectivity of rostroventral medulla descending control of spinal sensory inputs shifts postnatally from A fibre to C fibre evoked activity. J Physiol 592:1535–1544PubMedPubMedCentral Koch SC, Fitzgerald M (2014) The selectivity of rostroventral medulla descending control of spinal sensory inputs shifts postnatally from A fibre to C fibre evoked activity. J Physiol 592:1535–1544PubMedPubMedCentral
Zurück zum Zitat Kollmann TR et al (2009) Neonatal innate TLR-mediated responses are distinct from those of adults. J Immunol 183:7150–7160PubMedPubMedCentral Kollmann TR et al (2009) Neonatal innate TLR-mediated responses are distinct from those of adults. J Immunol 183:7150–7160PubMedPubMedCentral
Zurück zum Zitat Kwok CH, Devonshire IM, Bennett AJ, Hathway GJ (2014) Postnatal maturation of endogenous opioid systems within the periaqueductal grey and spinal dorsal horn of the rat. PAIN® 155:168–178 Kwok CH, Devonshire IM, Bennett AJ, Hathway GJ (2014) Postnatal maturation of endogenous opioid systems within the periaqueductal grey and spinal dorsal horn of the rat. PAIN® 155:168–178
Zurück zum Zitat LaPrairie JL, Murphy AZ (2007) Female rats are more vulnerable to the long-term consequences of neonatal inflammatory injury. Pain 132:S124–S133PubMedPubMedCentral LaPrairie JL, Murphy AZ (2007) Female rats are more vulnerable to the long-term consequences of neonatal inflammatory injury. Pain 132:S124–S133PubMedPubMedCentral
Zurück zum Zitat LaPrairie J, Murphy AZ (2009) Neonatal injury alters adult pain sensitivity by increasing opioid tone in the periaqueductal gray. Front Behav Neurosci 3:31PubMedPubMedCentral LaPrairie J, Murphy AZ (2009) Neonatal injury alters adult pain sensitivity by increasing opioid tone in the periaqueductal gray. Front Behav Neurosci 3:31PubMedPubMedCentral
Zurück zum Zitat LaPrairie JL, Murphy AZ (2010) Long-term impact of neonatal injury in male and female rats: sex differences, mechanisms and clinical implications. Front Neuroendocrinol 31:193–202PubMedPubMedCentral LaPrairie JL, Murphy AZ (2010) Long-term impact of neonatal injury in male and female rats: sex differences, mechanisms and clinical implications. Front Neuroendocrinol 31:193–202PubMedPubMedCentral
Zurück zum Zitat LaPrairie JL, Johns ME, Murphy AZ (2008) Preemptive morphine analgesia attenuates the long-term consequences of neonatal inflammation in male and female rats. Pediatr Res 64:625PubMedPubMedCentral LaPrairie JL, Johns ME, Murphy AZ (2008) Preemptive morphine analgesia attenuates the long-term consequences of neonatal inflammation in male and female rats. Pediatr Res 64:625PubMedPubMedCentral
Zurück zum Zitat Lawson S (2002) Phenotype and function of somatic primary afferent nociceptive neurones with C-Aδ- or Aα/β-fibres. Exp Physiol 87:239–244PubMed Lawson S (2002) Phenotype and function of somatic primary afferent nociceptive neurones with C-Aδ- or Aα/β-fibres. Exp Physiol 87:239–244PubMed
Zurück zum Zitat Legrain V, Iannetti GD, Plaghki L, Mouraux A (2011) The pain matrix reloaded: a salience detection system for the body. Prog Neurobiol 93:111–124PubMed Legrain V, Iannetti GD, Plaghki L, Mouraux A (2011) The pain matrix reloaded: a salience detection system for the body. Prog Neurobiol 93:111–124PubMed
Zurück zum Zitat Levy WB, Steward O (1983) Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience 8:791–797PubMed Levy WB, Steward O (1983) Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience 8:791–797PubMed
Zurück zum Zitat Li J, Baccei ML (2014) Neonatal tissue injury reduces the intrinsic excitability of adult mouse superficial dorsal horn neurons. Neuroscience 256:392–402PubMed Li J, Baccei ML (2014) Neonatal tissue injury reduces the intrinsic excitability of adult mouse superficial dorsal horn neurons. Neuroscience 256:392–402PubMed
Zurück zum Zitat Li G-L, Qiao Z-M, Han J-S, Luo F (2010) Dissociated behavior of low-frequency responses and high-frequency oscillations after systemic morphine administration in conscious rats. NeuroReport 21:2–7PubMed Li G-L, Qiao Z-M, Han J-S, Luo F (2010) Dissociated behavior of low-frequency responses and high-frequency oscillations after systemic morphine administration in conscious rats. NeuroReport 21:2–7PubMed
Zurück zum Zitat Li J, Blankenship ML, Baccei ML (2013) Inward-rectifying potassium (Kir) channels regulate pacemaker activity in spinal nociceptive circuits during early life. J Neurosci 33:3352–3362PubMedPubMedCentral Li J, Blankenship ML, Baccei ML (2013) Inward-rectifying potassium (Kir) channels regulate pacemaker activity in spinal nociceptive circuits during early life. J Neurosci 33:3352–3362PubMedPubMedCentral
Zurück zum Zitat Li J, Kritzer E, Craig PE, Baccei ML (2015) Aberrant synaptic integration in adult lamina I projection neurons following neonatal tissue damage. J Neurosci 35:2438–2451PubMedPubMedCentral Li J, Kritzer E, Craig PE, Baccei ML (2015) Aberrant synaptic integration in adult lamina I projection neurons following neonatal tissue damage. J Neurosci 35:2438–2451PubMedPubMedCentral
Zurück zum Zitat Lu Y, Sweitzer SM, Laurito CE, Yeomans DC (2004) Differential opioid inhibition of C- and Aδ-fiber mediated thermonociception after stimulation of the nucleus raphe magnus. Anesth Analg 98:414–419PubMed Lu Y, Sweitzer SM, Laurito CE, Yeomans DC (2004) Differential opioid inhibition of C- and Aδ-fiber mediated thermonociception after stimulation of the nucleus raphe magnus. Anesth Analg 98:414–419PubMed
Zurück zum Zitat Mendell LM, Wall PD (1965) Responses of single dorsal cord cells to peripheral cutaneous unmyelinated fibres. Nature 206:97–99PubMed Mendell LM, Wall PD (1965) Responses of single dorsal cord cells to peripheral cutaneous unmyelinated fibres. Nature 206:97–99PubMed
Zurück zum Zitat Morgan MM, Christie MJ (2011) Analysis of opioid efficacy, tolerance, addiction and dependence from cell culture to human. Br J Pharmacol 164:1322–1334PubMedPubMedCentral Morgan MM, Christie MJ (2011) Analysis of opioid efficacy, tolerance, addiction and dependence from cell culture to human. Br J Pharmacol 164:1322–1334PubMedPubMedCentral
Zurück zum Zitat Morgan M, Heinricher M, Fields H (1992) Circuitry linking opioid-sensitive nociceptive modulatory systems in periaqueductal gray and spinal cord with rostral ventromedial medulla. Neuroscience 47:863–871PubMed Morgan M, Heinricher M, Fields H (1992) Circuitry linking opioid-sensitive nociceptive modulatory systems in periaqueductal gray and spinal cord with rostral ventromedial medulla. Neuroscience 47:863–871PubMed
Zurück zum Zitat Moriarty O, Harrington L, Beggs S, Walker S (2018) Opioid analgesia and the somatosensory memory of neonatal surgical injury in the adult rat. Br J Anaesth 121:314–324PubMedPubMedCentral Moriarty O, Harrington L, Beggs S, Walker S (2018) Opioid analgesia and the somatosensory memory of neonatal surgical injury in the adult rat. Br J Anaesth 121:314–324PubMedPubMedCentral
Zurück zum Zitat Moriarty O, Tu Y, Sengar AS, Salter MW, Beggs S, Walker SM (2019) Priming of adult incision response by early life injury: neonatal microglial inhibition has persistent but sexually dimorphic effects in adult rats. J Neurosci 39(16):1786–1798 Moriarty O, Tu Y, Sengar AS, Salter MW, Beggs S, Walker SM (2019) Priming of adult incision response by early life injury: neonatal microglial inhibition has persistent but sexually dimorphic effects in adult rats. J Neurosci 39(16):1786–1798
Zurück zum Zitat Moss A, Beggs S, Vega-Avelaira D, Costigan M, Hathway GJ, Salter MW, Fitzgerald M (2007) Spinal microglia and neuropathic pain in young rats. Pain 128:215–224PubMed Moss A, Beggs S, Vega-Avelaira D, Costigan M, Hathway GJ, Salter MW, Fitzgerald M (2007) Spinal microglia and neuropathic pain in young rats. Pain 128:215–224PubMed
Zurück zum Zitat Nahin RL, Sayer B, Stussman BJ, Feinberg TM (2019) 18-Year trends in the prevalence of, and health care use for, non-cancer pain in the United States: data from the medical expenditure panel survey. J Pain 20(7):796–809PubMed Nahin RL, Sayer B, Stussman BJ, Feinberg TM (2019) 18-Year trends in the prevalence of, and health care use for, non-cancer pain in the United States: data from the medical expenditure panel survey. J Pain 20(7):796–809PubMed
Zurück zum Zitat Nakatsuka T, Ataka T, Kumamoto E, Tamaki T, Yoshimura M (2000) Alteration in synaptic inputs through C-afferent fibers to substantia gelatinosa neurons of the rat spinal dorsal horn during postnatal development. Neuroscience 99:549–556PubMed Nakatsuka T, Ataka T, Kumamoto E, Tamaki T, Yoshimura M (2000) Alteration in synaptic inputs through C-afferent fibers to substantia gelatinosa neurons of the rat spinal dorsal horn during postnatal development. Neuroscience 99:549–556PubMed
Zurück zum Zitat Oberlander TF, Grunau RE, Whitfield MF, Fitzgerald C, Pitfield S, Saul JP (2000) Biobehavioral pain responses in former extremely low birth weight infants at four months 9 corrected age. Pediatrics 105:e6PubMed Oberlander TF, Grunau RE, Whitfield MF, Fitzgerald C, Pitfield S, Saul JP (2000) Biobehavioral pain responses in former extremely low birth weight infants at four months 9 corrected age. Pediatrics 105:e6PubMed
Zurück zum Zitat Park J-S, Nakatsuka T, Nagata K, Higashi H, Yoshimura M (1999) Reorganization of the primary afferent termination in the rat spinal dorsal horn during post-natal development. Dev Brain Res 113:29–36 Park J-S, Nakatsuka T, Nagata K, Higashi H, Yoshimura M (1999) Reorganization of the primary afferent termination in the rat spinal dorsal horn during post-natal development. Dev Brain Res 113:29–36
Zurück zum Zitat Petitjean H et al (2015) Dorsal horn parvalbumin neurons are gate-keepers of touch-evoked pain after nerve injury. Cell Rep 13:1246–1257PubMedPubMedCentral Petitjean H et al (2015) Dorsal horn parvalbumin neurons are gate-keepers of touch-evoked pain after nerve injury. Cell Rep 13:1246–1257PubMedPubMedCentral
Zurück zum Zitat Pinto JG, Jones DG, Williams CK, Murphy KM (2015) Characterizing synaptic protein development in human visual cortex enables alignment of synaptic age with rat visual cortex. Front Neural Circuits 9:3PubMedPubMedCentral Pinto JG, Jones DG, Williams CK, Murphy KM (2015) Characterizing synaptic protein development in human visual cortex enables alignment of synaptic age with rat visual cortex. Front Neural Circuits 9:3PubMedPubMedCentral
Zurück zum Zitat Ray P et al (2018) Comparative transcriptome profiling of the human and mouse dorsal root ganglia: an RNA-seq-based resource for pain and sensory neuroscience research. Pain 159:1325–1345PubMedPubMedCentral Ray P et al (2018) Comparative transcriptome profiling of the human and mouse dorsal root ganglia: an RNA-seq-based resource for pain and sensory neuroscience research. Pain 159:1325–1345PubMedPubMedCentral
Zurück zum Zitat Ren K et al (2004) Characterization of basal and re-inflammation-associated long-term alteration in pain responsivity following short-lasting neonatal local inflammatory insult. Pain 110:588–596PubMed Ren K et al (2004) Characterization of basal and re-inflammation-associated long-term alteration in pain responsivity following short-lasting neonatal local inflammatory insult. Pain 110:588–596PubMed
Zurück zum Zitat Reynolds ML, Fitzgerald M, Benowitz LI (1991) GAP-43 expression in developing cutaneous and muscle nerves in the rat hindlimb. Neuroscience 41:201–211PubMed Reynolds ML, Fitzgerald M, Benowitz LI (1991) GAP-43 expression in developing cutaneous and muscle nerves in the rat hindlimb. Neuroscience 41:201–211PubMed
Zurück zum Zitat Sandkühler J, Liu X (1998) Induction of long-term potentiation at spinal synapses by noxious stimulation or nerve injury. Eur J Neurosci 10:2476–2480PubMed Sandkühler J, Liu X (1998) Induction of long-term potentiation at spinal synapses by noxious stimulation or nerve injury. Eur J Neurosci 10:2476–2480PubMed
Zurück zum Zitat Schaffner AE, Behar T, Nadi S, Barker JL (1993) Quantitative analysis of transient GABA expression in embryonic and early postnatal rat spinal cord neurons. Dev Brain Res 72:265–276 Schaffner AE, Behar T, Nadi S, Barker JL (1993) Quantitative analysis of transient GABA expression in embryonic and early postnatal rat spinal cord neurons. Dev Brain Res 72:265–276
Zurück zum Zitat Scheffel J et al (2012) Toll-like receptor activation reveals developmental reorganization and unmasks responder subsets of microglia. Glia 60:1930–1943PubMed Scheffel J et al (2012) Toll-like receptor activation reveals developmental reorganization and unmasks responder subsets of microglia. Glia 60:1930–1943PubMed
Zurück zum Zitat Scheible KM et al (2015) Developmentally determined reduction in CD31 during gestation is associated with CD8+ T cell effector differentiation in preterm infants. Clin Immunol 161:65–74PubMedPubMedCentral Scheible KM et al (2015) Developmentally determined reduction in CD31 during gestation is associated with CD8+ T cell effector differentiation in preterm infants. Clin Immunol 161:65–74PubMedPubMedCentral
Zurück zum Zitat Schmelzle-Lubiecki B, Campbell KA, Howard R, Franck L, Fitzgerald M (2007) Long-term consequences of early infant injury and trauma upon somatosensory processing. Eur J Pain 11:799–809PubMed Schmelzle-Lubiecki B, Campbell KA, Howard R, Franck L, Fitzgerald M (2007) Long-term consequences of early infant injury and trauma upon somatosensory processing. Eur J Pain 11:799–809PubMed
Zurück zum Zitat Teichert RW, Smith NJ, Raghuraman S, Yoshikami D, Light AR, Olivera BM (2012) Functional profiling of neurons through cellular neuropharmacology. Proc Natl Acad Sci 109:1388–1395PubMed Teichert RW, Smith NJ, Raghuraman S, Yoshikami D, Light AR, Olivera BM (2012) Functional profiling of neurons through cellular neuropharmacology. Proc Natl Acad Sci 109:1388–1395PubMed
Zurück zum Zitat Usoskin D et al (2015) Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat Neurosci 18:145PubMed Usoskin D et al (2015) Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat Neurosci 18:145PubMed
Zurück zum Zitat van Praag H, Frenk H (1991) The development of stimulation-produced analgesia (SPA) in the rat. Brain Res Dev Brain Res 64:71–76PubMed van Praag H, Frenk H (1991) The development of stimulation-produced analgesia (SPA) in the rat. Brain Res Dev Brain Res 64:71–76PubMed
Zurück zum Zitat Waldenstrom A, Thelin J, Thimansson E, Levinsson A, Schouenborg J (2003) Developmental learning in a pain-related system: evidence for a cross-modality mechanism. J Neurosci 23:7719–7725PubMedPubMedCentral Waldenstrom A, Thelin J, Thimansson E, Levinsson A, Schouenborg J (2003) Developmental learning in a pain-related system: evidence for a cross-modality mechanism. J Neurosci 23:7719–7725PubMedPubMedCentral
Zurück zum Zitat Walker SM, Fitzgerald M, Hathway GJ (2015) Surgical injury in the neonatal rat alters the adult pattern of descending modulation from the rostroventral medulla. Anesthesiol J Am Soc Anesthesiol 122:1391–1400 Walker SM, Fitzgerald M, Hathway GJ (2015) Surgical injury in the neonatal rat alters the adult pattern of descending modulation from the rostroventral medulla. Anesthesiol J Am Soc Anesthesiol 122:1391–1400
Zurück zum Zitat Walker S, Melbourne A, O’Reilly H, Beckmann J, Eaton-Rosen Z, Ourselin S, Marlow N (2018) Somatosensory function and pain in extremely preterm young adults from the UK EPICure cohort: sex-dependent differences and impact of neonatal surgery. Br J Anaesth 121:623–635PubMedPubMedCentral Walker S, Melbourne A, O’Reilly H, Beckmann J, Eaton-Rosen Z, Ourselin S, Marlow N (2018) Somatosensory function and pain in extremely preterm young adults from the UK EPICure cohort: sex-dependent differences and impact of neonatal surgery. Br J Anaesth 121:623–635PubMedPubMedCentral
Zurück zum Zitat Walwyn WM, Chen W, Kim H, Minasyan A, Ennes HS, McRoberts JA, Marvizón JCG (2016) Sustained suppression of hyperalgesia during latent sensitization by μ-, δ-, and κ-opioid receptors and α2A adrenergic receptors: role of constitutive activity. J Neurosci 36:204–221PubMedPubMedCentral Walwyn WM, Chen W, Kim H, Minasyan A, Ennes HS, McRoberts JA, Marvizón JCG (2016) Sustained suppression of hyperalgesia during latent sensitization by μ-, δ-, and κ-opioid receptors and α2A adrenergic receptors: role of constitutive activity. J Neurosci 36:204–221PubMedPubMedCentral
Zurück zum Zitat Watkins LR, Wiertelak EP, Goehler LE, Smith KP, Martin D, Maier SF (1994) Characterization of cytokine-induced hyperalgesia. Brain Res 654:15–26PubMed Watkins LR, Wiertelak EP, Goehler LE, Smith KP, Martin D, Maier SF (1994) Characterization of cytokine-induced hyperalgesia. Brain Res 654:15–26PubMed
Zurück zum Zitat Weiss KE, Hahn A, Wallace DP, Biggs B, Bruce BK, Harrison TE (2013) Acceptance of pain: associations with depression, catastrophizing, and functional disability among children and adolescents in an interdisciplinary chronic pain rehabilitation program. J Pediatr Psychol 38:756–765. https://doi.org/10.1093/jpepsy/jst028 CrossRefPubMed Weiss KE, Hahn A, Wallace DP, Biggs B, Bruce BK, Harrison TE (2013) Acceptance of pain: associations with depression, catastrophizing, and functional disability among children and adolescents in an interdisciplinary chronic pain rehabilitation program. J Pediatr Psychol 38:756–765. https://​doi.​org/​10.​1093/​jpepsy/​jst028 CrossRefPubMed
Zurück zum Zitat Xu XJ, Dalsgaard CJ, Wiesenfeld-Hallin Z (1992) Spinal substance P and N-methyl-d-aspartate receptors are coactivated in the induction of central sensitization of the nociceptive flexor reflex. Neuroscience 51:641–648PubMed Xu XJ, Dalsgaard CJ, Wiesenfeld-Hallin Z (1992) Spinal substance P and N-methyl-d-aspartate receptors are coactivated in the induction of central sensitization of the nociceptive flexor reflex. Neuroscience 51:641–648PubMed
Zurück zum Zitat Yang K, Kumamoto E, Furue H, Yoshimura M (1998) Capsaicin facilitates excitatory but not inhibitory synaptic transmission in substantia gelatinosa of the rat spinal cord. Neurosci Lett 255:135–138PubMed Yang K, Kumamoto E, Furue H, Yoshimura M (1998) Capsaicin facilitates excitatory but not inhibitory synaptic transmission in substantia gelatinosa of the rat spinal cord. Neurosci Lett 255:135–138PubMed
Zurück zum Zitat Yoon S-Y, Patel D, Dougherty PM (2012) Minocycline blocks lipopolysaccharide induced hyperalgesia by suppression of microglia but not astrocytes. Neuroscience 221:214–224PubMedPubMedCentral Yoon S-Y, Patel D, Dougherty PM (2012) Minocycline blocks lipopolysaccharide induced hyperalgesia by suppression of microglia but not astrocytes. Neuroscience 221:214–224PubMedPubMedCentral
Zurück zum Zitat Zhang Y-H, Wang X-M, Ennis M (2010) Effects of neonatal inflammation on descending modulation from the rostroventromedial medulla. Brain Res Bull 83:16–22PubMed Zhang Y-H, Wang X-M, Ennis M (2010) Effects of neonatal inflammation on descending modulation from the rostroventromedial medulla. Brain Res Bull 83:16–22PubMed
Metadaten
Titel
The development of pain circuits and unique effects of neonatal injury
verfasst von
Chelsie L. Brewer
Mark L. Baccei
Publikationsdatum
09.08.2019
Verlag
Springer Vienna
Erschienen in
Journal of Neural Transmission / Ausgabe 4/2020
Print ISSN: 0300-9564
Elektronische ISSN: 1435-1463
DOI
https://doi.org/10.1007/s00702-019-02059-z

Weitere Artikel der Ausgabe 4/2020

Journal of Neural Transmission 4/2020 Zur Ausgabe

Neurology and Preclinical Neurological Studies - Review Article

Alleviating pain with delta opioid receptor agonists: evidence from experimental models

Neurology and Preclinical Neurological Studies - Review Article

Nocebo and the contribution of psychosocial factors to the generation of pain

Neurology and Preclinical Neurological Studies - Review Article

Neurostimulation methods in the treatment of chronic pain

Neurology and Preclinical Neurological Studies - Review Article

Reviewing the case for compromised spinal inhibition in neuropathic pain

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

25.04.2024 Hypotonie Nachrichten

Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.

Frühe Alzheimertherapie lohnt sich

25.04.2024 AAN-Jahrestagung 2024 Nachrichten

Ist die Tau-Last noch gering, scheint der Vorteil von Lecanemab besonders groß zu sein. Und beginnen Erkrankte verzögert mit der Behandlung, erreichen sie nicht mehr die kognitive Leistung wie bei einem früheren Start. Darauf deuten neue Analysen der Phase-3-Studie Clarity AD.

Viel Bewegung in der Parkinsonforschung

25.04.2024 Parkinson-Krankheit Nachrichten

Neue arznei- und zellbasierte Ansätze, Frühdiagnose mit Bewegungssensoren, Rückenmarkstimulation gegen Gehblockaden – in der Parkinsonforschung tut sich einiges. Auf dem Deutschen Parkinsonkongress ging es auch viel um technische Innovationen.

Demenzkranke durch Antipsychotika vielfach gefährdet

23.04.2024 Demenz Nachrichten

Wenn Demenzkranke aufgrund von Symptomen wie Agitation oder Aggressivität mit Antipsychotika behandelt werden, sind damit offenbar noch mehr Risiken verbunden als bislang angenommen.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.