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Colocalized structural and functional changes in the cortex of patients with trigeminal neuropathic pain.

DaSilva AF, Becerra L, Pendse G, Chizh B, Tully S, Borsook D - PLoS ONE (2008)

Bottom Line: Changes in cortical thickness of TNP patients were frequently colocalized and correlated with functional allodynic activations, and included both cortical thickening and thinning in sensorimotor regions, and predominantly thinning in emotional regions.Overall, such patterns of cortical thickness suggest a dynamic functionally-driven plasticity of the brain.These structural changes, which correlated with the pain duration, age-at-onset, pain intensity and cortical activity, may be specific targets for evaluating therapeutic interventions.

View Article: PubMed Central - PubMed

Affiliation: PAIN Group, Brain Imaging Center, Mclean Hospital, Harvard Medical School, Boston, MA, USA. adasilva@umich.edu

ABSTRACT

Background: Recent data suggests that in chronic pain there are changes in gray matter consistent with decreased brain volume, indicating that the disease process may produce morphological changes in the brains of those affected. However, no study has evaluated cortical thickness in relation to specific functional changes in evoked pain. In this study we sought to investigate structural (gray matter thickness) and functional (blood oxygenation dependent level - BOLD) changes in cortical regions of precisely matched patients with chronic trigeminal neuropathic pain (TNP) affecting the right maxillary (V2) division of the trigeminal nerve. The model has a number of advantages including the evaluation of specific changes that can be mapped to known somatotopic anatomy.

Methodology/principal findings: Cortical regions were chosen based on sensory (Somatosensory cortex (SI and SII), motor (MI) and posterior insula), or emotional (DLPFC, Frontal, Anterior Insula, Cingulate) processing of pain. Both structural and functional (to brush-induced allodynia) scans were obtained and averaged from two different imaging sessions separated by 2-6 months in all patients. Age and gender-matched healthy controls were also scanned twice for cortical thickness measurement. Changes in cortical thickness of TNP patients were frequently colocalized and correlated with functional allodynic activations, and included both cortical thickening and thinning in sensorimotor regions, and predominantly thinning in emotional regions.

Conclusions: Overall, such patterns of cortical thickness suggest a dynamic functionally-driven plasticity of the brain. These structural changes, which correlated with the pain duration, age-at-onset, pain intensity and cortical activity, may be specific targets for evaluating therapeutic interventions.

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Somatosensory (SI & SII) and Motor (MI) Cortices.Panels A and B - SI and MI in this study were defined as the central sulcus including its posterior wall, and the precentral gyrus, respectively. SII was defined was the subcentral section lateroventral to the postcentral gyrus. In the hemispheres contralateral and ipsilateral to the TNP, regions of the sensorimotor cortex were segmented in ten equal vertical sections labeled from bottom to top in an ascendant manner, being section 1 located in the lowest portion, and section ten in the highest.; Panel C - Average BOLD deactivations (dark-light blue) and activations (red-yellow) in the sensorimotor cortex during allodynic brush of the affected V2 of the six TNP patients. The functional clusters were located in the most caudal region of SI and MI where the face and the neighboring regions are somatotopically represented; Panel D – Differences in cortical thickness between TNP and HC along sections of the sensorimotor cortex (pink = TNP<HC; green = TNP>HC). There is bilateral thinning in the most caudal region of the somatosensory cortex, where the face is represented, which was colocalized with functional clusters during allodynic pain.
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pone-0003396-g002: Somatosensory (SI & SII) and Motor (MI) Cortices.Panels A and B - SI and MI in this study were defined as the central sulcus including its posterior wall, and the precentral gyrus, respectively. SII was defined was the subcentral section lateroventral to the postcentral gyrus. In the hemispheres contralateral and ipsilateral to the TNP, regions of the sensorimotor cortex were segmented in ten equal vertical sections labeled from bottom to top in an ascendant manner, being section 1 located in the lowest portion, and section ten in the highest.; Panel C - Average BOLD deactivations (dark-light blue) and activations (red-yellow) in the sensorimotor cortex during allodynic brush of the affected V2 of the six TNP patients. The functional clusters were located in the most caudal region of SI and MI where the face and the neighboring regions are somatotopically represented; Panel D – Differences in cortical thickness between TNP and HC along sections of the sensorimotor cortex (pink = TNP<HC; green = TNP>HC). There is bilateral thinning in the most caudal region of the somatosensory cortex, where the face is represented, which was colocalized with functional clusters during allodynic pain.

Mentions: The Somatosensory Cortex in this study was defined as the combination of the primary somatosensory cortex (SI), which includes the central sulcus in its lower bordering posterior wall (putative BA 3b) with postcentral gyrus (putative BA 1), as well as the secondary somatosensory cortex (SII) localized in the subcentral section lateroventral to the postcentral gyrus on the operculum Rolandi (putative BA 43) [14]. In the average brain, both central sulci and postcentral gyri were segmented in ten equal vertical sections labeled from bottom to top in an ascendant manner, being section 1 (CS1) located in the lowest portion, and section ten in the highest (CSI0) (Figure 2A) (see methods and supplementary data S1 for more details).


Colocalized structural and functional changes in the cortex of patients with trigeminal neuropathic pain.

DaSilva AF, Becerra L, Pendse G, Chizh B, Tully S, Borsook D - PLoS ONE (2008)

Somatosensory (SI & SII) and Motor (MI) Cortices.Panels A and B - SI and MI in this study were defined as the central sulcus including its posterior wall, and the precentral gyrus, respectively. SII was defined was the subcentral section lateroventral to the postcentral gyrus. In the hemispheres contralateral and ipsilateral to the TNP, regions of the sensorimotor cortex were segmented in ten equal vertical sections labeled from bottom to top in an ascendant manner, being section 1 located in the lowest portion, and section ten in the highest.; Panel C - Average BOLD deactivations (dark-light blue) and activations (red-yellow) in the sensorimotor cortex during allodynic brush of the affected V2 of the six TNP patients. The functional clusters were located in the most caudal region of SI and MI where the face and the neighboring regions are somatotopically represented; Panel D – Differences in cortical thickness between TNP and HC along sections of the sensorimotor cortex (pink = TNP<HC; green = TNP>HC). There is bilateral thinning in the most caudal region of the somatosensory cortex, where the face is represented, which was colocalized with functional clusters during allodynic pain.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2561059&req=5

pone-0003396-g002: Somatosensory (SI & SII) and Motor (MI) Cortices.Panels A and B - SI and MI in this study were defined as the central sulcus including its posterior wall, and the precentral gyrus, respectively. SII was defined was the subcentral section lateroventral to the postcentral gyrus. In the hemispheres contralateral and ipsilateral to the TNP, regions of the sensorimotor cortex were segmented in ten equal vertical sections labeled from bottom to top in an ascendant manner, being section 1 located in the lowest portion, and section ten in the highest.; Panel C - Average BOLD deactivations (dark-light blue) and activations (red-yellow) in the sensorimotor cortex during allodynic brush of the affected V2 of the six TNP patients. The functional clusters were located in the most caudal region of SI and MI where the face and the neighboring regions are somatotopically represented; Panel D – Differences in cortical thickness between TNP and HC along sections of the sensorimotor cortex (pink = TNP<HC; green = TNP>HC). There is bilateral thinning in the most caudal region of the somatosensory cortex, where the face is represented, which was colocalized with functional clusters during allodynic pain.
Mentions: The Somatosensory Cortex in this study was defined as the combination of the primary somatosensory cortex (SI), which includes the central sulcus in its lower bordering posterior wall (putative BA 3b) with postcentral gyrus (putative BA 1), as well as the secondary somatosensory cortex (SII) localized in the subcentral section lateroventral to the postcentral gyrus on the operculum Rolandi (putative BA 43) [14]. In the average brain, both central sulci and postcentral gyri were segmented in ten equal vertical sections labeled from bottom to top in an ascendant manner, being section 1 (CS1) located in the lowest portion, and section ten in the highest (CSI0) (Figure 2A) (see methods and supplementary data S1 for more details).

Bottom Line: Changes in cortical thickness of TNP patients were frequently colocalized and correlated with functional allodynic activations, and included both cortical thickening and thinning in sensorimotor regions, and predominantly thinning in emotional regions.Overall, such patterns of cortical thickness suggest a dynamic functionally-driven plasticity of the brain.These structural changes, which correlated with the pain duration, age-at-onset, pain intensity and cortical activity, may be specific targets for evaluating therapeutic interventions.

View Article: PubMed Central - PubMed

Affiliation: PAIN Group, Brain Imaging Center, Mclean Hospital, Harvard Medical School, Boston, MA, USA. adasilva@umich.edu

ABSTRACT

Background: Recent data suggests that in chronic pain there are changes in gray matter consistent with decreased brain volume, indicating that the disease process may produce morphological changes in the brains of those affected. However, no study has evaluated cortical thickness in relation to specific functional changes in evoked pain. In this study we sought to investigate structural (gray matter thickness) and functional (blood oxygenation dependent level - BOLD) changes in cortical regions of precisely matched patients with chronic trigeminal neuropathic pain (TNP) affecting the right maxillary (V2) division of the trigeminal nerve. The model has a number of advantages including the evaluation of specific changes that can be mapped to known somatotopic anatomy.

Methodology/principal findings: Cortical regions were chosen based on sensory (Somatosensory cortex (SI and SII), motor (MI) and posterior insula), or emotional (DLPFC, Frontal, Anterior Insula, Cingulate) processing of pain. Both structural and functional (to brush-induced allodynia) scans were obtained and averaged from two different imaging sessions separated by 2-6 months in all patients. Age and gender-matched healthy controls were also scanned twice for cortical thickness measurement. Changes in cortical thickness of TNP patients were frequently colocalized and correlated with functional allodynic activations, and included both cortical thickening and thinning in sensorimotor regions, and predominantly thinning in emotional regions.

Conclusions: Overall, such patterns of cortical thickness suggest a dynamic functionally-driven plasticity of the brain. These structural changes, which correlated with the pain duration, age-at-onset, pain intensity and cortical activity, may be specific targets for evaluating therapeutic interventions.

Show MeSH
Related in: MedlinePlus