Temporal summation of the nociceptive withdrawal reflex involves deactivation of posterior cingulate cortex

A Perrotta, P Chiacchiaretta, M G Anastasio, L Pavone, G Grillea, M Bartolo, E Siravo, C Colonnese, R De Icco, M Serrao, G Sandrini, F Pierelli, A Ferretti

Research output: Contribution to journalArticle

Abstract

BACKGROUND: Temporal summation of pain sensation is pivotal both in physiological and pathological nociception. In humans, it develops in parallel with temporal summation of the nociceptive withdrawal reflex (NWR) of the lower limb, an objective representation of the temporal processing of nociceptive signals into the spinal cord.

METHODS: To study the contribution of cortical and subcortical structures in temporal summation of pain reflex responses, we compared the fMRI signal changes related to the temporal summation threshold (TST) of the NWR with that related to the single NWR response. We studied 17 healthy subjects using a stimulation paradigm previously determined to evoke both the TST of the NWR (SUMM) and the NWR single response (SING).

RESULTS: We found a significant activation in left (contralateral) primary somatosensory cortex (SI), bilateral secondary somatosensory cortex (SII), bilateral insula, anterior cingulate cortex (ACC) and bilateral thalamus during both SUMM and SING conditions. The SUMM versus SING contrast revealed a significant deactivation in the posterior cingulate cortex (PCC) and bilateral middle occipital gyrus in SUMM when compared to SING condition.

CONCLUSIONS: Our data support the hypothesis that temporal summation of nociceptive reflex responses is driven through a switch between activation and deactivation of a specific set of brain areas linked to the default mode network. This behaviour could be explained in view of the relevance of the pain processing induced by temporal summation, recognized as a more significant potential damaging condition with respect to a single, isolated, painful stimulation of comparable pain intensity.

SIGNIFICANCE: The study demonstrated that TST of the NWR involves a selective deactivation of PCC.

Original languageEnglish
Pages (from-to)289-301
Number of pages13
JournalEUR.J.PAIN
Volume21
Issue number2
DOIs
Publication statusPublished - Feb 2017

Fingerprint

Gyrus Cinguli
Reflex
Pain
Somatosensory Cortex
Occipital Lobe
Nociception
Thalamus
Lower Extremity
Spinal Cord
Healthy Volunteers
Magnetic Resonance Imaging
Brain

Keywords

  • Adult
  • Female
  • Gyrus Cinguli
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Nociception
  • Pain
  • Pain Measurement
  • Reflex
  • Young Adult
  • Journal Article

Cite this

Temporal summation of the nociceptive withdrawal reflex involves deactivation of posterior cingulate cortex. / Perrotta, A; Chiacchiaretta, P; Anastasio, M G; Pavone, L; Grillea, G; Bartolo, M; Siravo, E; Colonnese, C; De Icco, R; Serrao, M; Sandrini, G; Pierelli, F; Ferretti, A.

In: EUR.J.PAIN, Vol. 21, No. 2, 02.2017, p. 289-301.

Research output: Contribution to journalArticle

Perrotta, A ; Chiacchiaretta, P ; Anastasio, M G ; Pavone, L ; Grillea, G ; Bartolo, M ; Siravo, E ; Colonnese, C ; De Icco, R ; Serrao, M ; Sandrini, G ; Pierelli, F ; Ferretti, A. / Temporal summation of the nociceptive withdrawal reflex involves deactivation of posterior cingulate cortex. In: EUR.J.PAIN. 2017 ; Vol. 21, No. 2. pp. 289-301.
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abstract = "BACKGROUND: Temporal summation of pain sensation is pivotal both in physiological and pathological nociception. In humans, it develops in parallel with temporal summation of the nociceptive withdrawal reflex (NWR) of the lower limb, an objective representation of the temporal processing of nociceptive signals into the spinal cord.METHODS: To study the contribution of cortical and subcortical structures in temporal summation of pain reflex responses, we compared the fMRI signal changes related to the temporal summation threshold (TST) of the NWR with that related to the single NWR response. We studied 17 healthy subjects using a stimulation paradigm previously determined to evoke both the TST of the NWR (SUMM) and the NWR single response (SING).RESULTS: We found a significant activation in left (contralateral) primary somatosensory cortex (SI), bilateral secondary somatosensory cortex (SII), bilateral insula, anterior cingulate cortex (ACC) and bilateral thalamus during both SUMM and SING conditions. The SUMM versus SING contrast revealed a significant deactivation in the posterior cingulate cortex (PCC) and bilateral middle occipital gyrus in SUMM when compared to SING condition.CONCLUSIONS: Our data support the hypothesis that temporal summation of nociceptive reflex responses is driven through a switch between activation and deactivation of a specific set of brain areas linked to the default mode network. This behaviour could be explained in view of the relevance of the pain processing induced by temporal summation, recognized as a more significant potential damaging condition with respect to a single, isolated, painful stimulation of comparable pain intensity.SIGNIFICANCE: The study demonstrated that TST of the NWR involves a selective deactivation of PCC.",
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T1 - Temporal summation of the nociceptive withdrawal reflex involves deactivation of posterior cingulate cortex

AU - Perrotta, A

AU - Chiacchiaretta, P

AU - Anastasio, M G

AU - Pavone, L

AU - Grillea, G

AU - Bartolo, M

AU - Siravo, E

AU - Colonnese, C

AU - De Icco, R

AU - Serrao, M

AU - Sandrini, G

AU - Pierelli, F

AU - Ferretti, A

N1 - © 2016 European Pain Federation - EFIC®.

PY - 2017/2

Y1 - 2017/2

N2 - BACKGROUND: Temporal summation of pain sensation is pivotal both in physiological and pathological nociception. In humans, it develops in parallel with temporal summation of the nociceptive withdrawal reflex (NWR) of the lower limb, an objective representation of the temporal processing of nociceptive signals into the spinal cord.METHODS: To study the contribution of cortical and subcortical structures in temporal summation of pain reflex responses, we compared the fMRI signal changes related to the temporal summation threshold (TST) of the NWR with that related to the single NWR response. We studied 17 healthy subjects using a stimulation paradigm previously determined to evoke both the TST of the NWR (SUMM) and the NWR single response (SING).RESULTS: We found a significant activation in left (contralateral) primary somatosensory cortex (SI), bilateral secondary somatosensory cortex (SII), bilateral insula, anterior cingulate cortex (ACC) and bilateral thalamus during both SUMM and SING conditions. The SUMM versus SING contrast revealed a significant deactivation in the posterior cingulate cortex (PCC) and bilateral middle occipital gyrus in SUMM when compared to SING condition.CONCLUSIONS: Our data support the hypothesis that temporal summation of nociceptive reflex responses is driven through a switch between activation and deactivation of a specific set of brain areas linked to the default mode network. This behaviour could be explained in view of the relevance of the pain processing induced by temporal summation, recognized as a more significant potential damaging condition with respect to a single, isolated, painful stimulation of comparable pain intensity.SIGNIFICANCE: The study demonstrated that TST of the NWR involves a selective deactivation of PCC.

AB - BACKGROUND: Temporal summation of pain sensation is pivotal both in physiological and pathological nociception. In humans, it develops in parallel with temporal summation of the nociceptive withdrawal reflex (NWR) of the lower limb, an objective representation of the temporal processing of nociceptive signals into the spinal cord.METHODS: To study the contribution of cortical and subcortical structures in temporal summation of pain reflex responses, we compared the fMRI signal changes related to the temporal summation threshold (TST) of the NWR with that related to the single NWR response. We studied 17 healthy subjects using a stimulation paradigm previously determined to evoke both the TST of the NWR (SUMM) and the NWR single response (SING).RESULTS: We found a significant activation in left (contralateral) primary somatosensory cortex (SI), bilateral secondary somatosensory cortex (SII), bilateral insula, anterior cingulate cortex (ACC) and bilateral thalamus during both SUMM and SING conditions. The SUMM versus SING contrast revealed a significant deactivation in the posterior cingulate cortex (PCC) and bilateral middle occipital gyrus in SUMM when compared to SING condition.CONCLUSIONS: Our data support the hypothesis that temporal summation of nociceptive reflex responses is driven through a switch between activation and deactivation of a specific set of brain areas linked to the default mode network. This behaviour could be explained in view of the relevance of the pain processing induced by temporal summation, recognized as a more significant potential damaging condition with respect to a single, isolated, painful stimulation of comparable pain intensity.SIGNIFICANCE: The study demonstrated that TST of the NWR involves a selective deactivation of PCC.

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KW - Magnetic Resonance Imaging

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KW - Nociception

KW - Pain

KW - Pain Measurement

KW - Reflex

KW - Young Adult

KW - Journal Article

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DO - 10.1002/ejp.923

M3 - Article

C2 - 27452295

VL - 21

SP - 289

EP - 301

JO - EUR.J.PAIN

JF - EUR.J.PAIN

SN - 1090-3801

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