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Resting-sate functional reorganization of the rat limbic system following neuropathic injury.

Baliki MN, Chang PC, Baria AT, Centeno MV, Apkarian AV - Sci Rep (2014)

Bottom Line: Similar to the human, the rat brain topological properties exhibited small world features and did not differ between SNI and sham.Twenty-eight days after SNI, functional connection changes were localized mainly to within the limbic system, as well as between the limbic and nociceptive systems.Furthermore, these changes were lateralized and in proportion to the tactile allodynia exhibited by SNI animals.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Northwestern University Feinberg School of Medicine, Chicago, Illinois 60611, USA.

ABSTRACT
Human brain imaging studies from various clinical cohorts show that chronic pain is associated with large-scale brain functional and morphological reorganization. However, how the rat whole-brain network is topologically reorganized to support persistent pain-like behavior following neuropathic injury remains unknown. Here we compare resting state fMRI functional connectivity-based whole-brain network properties between rats receiving spared nerve injury (SNI) vs. sham injury, at 5 days (n = 11 SNI; n = 12 sham) and 28 days (n = 11 SNI; n = 12 sham) post-injury. Similar to the human, the rat brain topological properties exhibited small world features and did not differ between SNI and sham. Local neural networks in SNI animals showed minimal disruption at day 5, and more extensive reorganization at day 28 post-injury. Twenty-eight days after SNI, functional connection changes were localized mainly to within the limbic system, as well as between the limbic and nociceptive systems. No connectivity changes were observed within the nociceptive network. Furthermore, these changes were lateralized and in proportion to the tactile allodynia exhibited by SNI animals. The findings establish that SNI is primarily associated with altered information transfer of limbic regions and provides a novel translational framework for understanding brain functional reorganization in response to a persistent neuropathic injury.

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Functional Connectivity exhibits laterality differences 28 days after SNI.Connectivity strength changes in intra- and inter- hemispheric connectivity in comparison to sham. Connectivity strength was computed as the ratio of the total number of significant connections (at link density = 0.1) relative to the total number of all possible connections. SNI showed increased functional connectivity within the right (contralateral to injury) hemisphere and decreased inter-hemispheric functional connectivity. Error bars represent S.D. (L = left; R = right; *p<0.05, two-sided unpaired t-test).
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f4: Functional Connectivity exhibits laterality differences 28 days after SNI.Connectivity strength changes in intra- and inter- hemispheric connectivity in comparison to sham. Connectivity strength was computed as the ratio of the total number of significant connections (at link density = 0.1) relative to the total number of all possible connections. SNI showed increased functional connectivity within the right (contralateral to injury) hemisphere and decreased inter-hemispheric functional connectivity. Error bars represent S.D. (L = left; R = right; *p<0.05, two-sided unpaired t-test).

Mentions: Global changes in inter- and intra- hemispheric connectivity was examined and compared between SNI and sham animals 28 days following injury. The connectivity strength was computed as the ratio of the total number of significant connections relative to the total number of all possible connections. Significant differences between SNI and sham were assessed using a two-tailed unpaired t-test. SNI showed increased functional connectivity within the right (contralateral to injury) hemisphere (mean ± S.D. for SNI = 0.124 ± 0.008; sham = 0.113 ± 0.012; t-value = 2.31, p < 0.05) and decreased inter-hemispheric functional connectivity (SNI = 0.060 ± 0.006; sham = 0.068 ± 0.010; t-value = 2.09, p < 0.05). There were no differences in the left intra-hemispheric connectivity between SNI and sham at day 28 (SNI = 0.116 ± 0.009; sham = 0.112 ± 0.013; t-value = 0.964, p = 0.35) (Fig. 4).


Resting-sate functional reorganization of the rat limbic system following neuropathic injury.

Baliki MN, Chang PC, Baria AT, Centeno MV, Apkarian AV - Sci Rep (2014)

Functional Connectivity exhibits laterality differences 28 days after SNI.Connectivity strength changes in intra- and inter- hemispheric connectivity in comparison to sham. Connectivity strength was computed as the ratio of the total number of significant connections (at link density = 0.1) relative to the total number of all possible connections. SNI showed increased functional connectivity within the right (contralateral to injury) hemisphere and decreased inter-hemispheric functional connectivity. Error bars represent S.D. (L = left; R = right; *p<0.05, two-sided unpaired t-test).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4151103&req=5

f4: Functional Connectivity exhibits laterality differences 28 days after SNI.Connectivity strength changes in intra- and inter- hemispheric connectivity in comparison to sham. Connectivity strength was computed as the ratio of the total number of significant connections (at link density = 0.1) relative to the total number of all possible connections. SNI showed increased functional connectivity within the right (contralateral to injury) hemisphere and decreased inter-hemispheric functional connectivity. Error bars represent S.D. (L = left; R = right; *p<0.05, two-sided unpaired t-test).
Mentions: Global changes in inter- and intra- hemispheric connectivity was examined and compared between SNI and sham animals 28 days following injury. The connectivity strength was computed as the ratio of the total number of significant connections relative to the total number of all possible connections. Significant differences between SNI and sham were assessed using a two-tailed unpaired t-test. SNI showed increased functional connectivity within the right (contralateral to injury) hemisphere (mean ± S.D. for SNI = 0.124 ± 0.008; sham = 0.113 ± 0.012; t-value = 2.31, p < 0.05) and decreased inter-hemispheric functional connectivity (SNI = 0.060 ± 0.006; sham = 0.068 ± 0.010; t-value = 2.09, p < 0.05). There were no differences in the left intra-hemispheric connectivity between SNI and sham at day 28 (SNI = 0.116 ± 0.009; sham = 0.112 ± 0.013; t-value = 0.964, p = 0.35) (Fig. 4).

Bottom Line: Similar to the human, the rat brain topological properties exhibited small world features and did not differ between SNI and sham.Twenty-eight days after SNI, functional connection changes were localized mainly to within the limbic system, as well as between the limbic and nociceptive systems.Furthermore, these changes were lateralized and in proportion to the tactile allodynia exhibited by SNI animals.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Northwestern University Feinberg School of Medicine, Chicago, Illinois 60611, USA.

ABSTRACT
Human brain imaging studies from various clinical cohorts show that chronic pain is associated with large-scale brain functional and morphological reorganization. However, how the rat whole-brain network is topologically reorganized to support persistent pain-like behavior following neuropathic injury remains unknown. Here we compare resting state fMRI functional connectivity-based whole-brain network properties between rats receiving spared nerve injury (SNI) vs. sham injury, at 5 days (n = 11 SNI; n = 12 sham) and 28 days (n = 11 SNI; n = 12 sham) post-injury. Similar to the human, the rat brain topological properties exhibited small world features and did not differ between SNI and sham. Local neural networks in SNI animals showed minimal disruption at day 5, and more extensive reorganization at day 28 post-injury. Twenty-eight days after SNI, functional connection changes were localized mainly to within the limbic system, as well as between the limbic and nociceptive systems. No connectivity changes were observed within the nociceptive network. Furthermore, these changes were lateralized and in proportion to the tactile allodynia exhibited by SNI animals. The findings establish that SNI is primarily associated with altered information transfer of limbic regions and provides a novel translational framework for understanding brain functional reorganization in response to a persistent neuropathic injury.

Show MeSH
Related in: MedlinePlus