Structural Plasticity of Motor Cortices Assessed by Voxel-based Morphometry and Immunohistochemical Analysis Following Internal Capsular Infarcts in Macaque Monkeys

Overview

Journal Cereb Cortex Commun

Publisher Oxford University Press

Date 2022 Dec 2

PMID 36457456

Authors

Kohei Matsuda

Kazuaki Nagasaka

Junpei Kato

Ichiro Takashima

Noriyuki Higo

Affiliations

Soon will be listed here.

Abstract

Compensatory plastic changes in the remaining intact brain regions are supposedly involved in functional recovery following stroke. Previously, a compensatory increase in cortical activation occurred in the ventral premotor cortex (PMv), which contributed to the recovery of dexterous hand movement in a macaque model of unilateral internal capsular infarcts. Herein, we investigated the structural plastic changes underlying functional changes together with voxel-based morphometry (VBM) analysis of magnetic resonance imaging data and immunohistochemical analysis using SMI-32 antibody in a macaque model. Unilateral internal capsular infarcts were pharmacologically induced in 5 macaques, and another 5 macaques were used as intact controls for immunohistochemical analysis. Three months post infarcts, we observed significant increases in the gray matter volume (GMV) and the dendritic arborization of layer V pyramidal neurons in the contralesional rostral PMv (F5) as well as the primary motor cortex (M1). The histological analysis revealed shrinkage of neuronal soma and dendrites in the ipsilesional M1 and several premotor cortices, despite not always detecting GMV reduction by VBM analysis. In conclusion, compensatory structural changes occur in the contralesional F5 and M1 during motor recovery following internal capsular infarcts, and the dendritic growth of pyramidal neurons is partially correlated with GMV increase.

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References

Thiel A, Radlinska B, Paquette C, Sidel M, Soucy J, Schirrmacher R . The temporal dynamics of poststroke neuroinflammation: a longitudinal diffusion tensor imaging-guided PET study with 11C-PK11195 in acute subcortical stroke. J Nucl Med. 2010; 51(9):1404-12. DOI: 10.2967/jnumed.110.076612. View

Yew W, Djukic N, Jayaseelan J, Walker F, Roos K, Chataway T . Early treatment with minocycline following stroke in rats improves functional recovery and differentially modifies responses of peri-infarct microglia and astrocytes. J Neuroinflammation. 2019; 16(1):6. PMC: 6325745. DOI: 10.1186/s12974-018-1379-y. View

Clark T, Sullender C, Jacob D, Zuo Y, Dunn A, Jones T . Rehabilitative Training Interacts with Ischemia-Instigated Spine Dynamics to Promote a Lasting Population of New Synapses in Peri-Infarct Motor Cortex. J Neurosci. 2019; 39(43):8471-8483. PMC: 6807284. DOI: 10.1523/JNEUROSCI.1141-19.2019. View

Touvykine B, Mansoori B, Jean-Charles L, Deffeyes J, Quessy S, Dancause N . The Effect of Lesion Size on the Organization of the Ipsilesional and Contralesional Motor Cortex. Neurorehabil Neural Repair. 2015; 30(3):280-92. PMC: 4766967. DOI: 10.1177/1545968315585356. View

Jiang L, Liu J, Wang C, Guo J, Cheng J, Han T . Structural Alterations in Chronic Capsular versus Pontine Stroke. Radiology. 2017; 285(1):214-222. DOI: 10.1148/radiol.2017161055. View

Suzuki H, Sumiyoshi A, Taki Y, Matsumoto Y, Fukumoto Y, Kawashima R . Voxel-based morphometry and histological analysis for evaluating hippocampal damage in a rat model of cardiopulmonary resuscitation. Neuroimage. 2013; 77:215-21. DOI: 10.1016/j.neuroimage.2013.03.042. View

Bajaj S, Housley S, Wu D, Dhamala M, James G, Butler A . Dominance of the Unaffected Hemisphere Motor Network and Its Role in the Behavior of Chronic Stroke Survivors. Front Hum Neurosci. 2017; 10:650. PMC: 5186808. DOI: 10.3389/fnhum.2016.00650. View

Kato J, Murata Y, Takashima I, Higo N . Time- and area-dependent macrophage/microglial responses after focal infarction of the macaque internal capsule. Neurosci Res. 2020; 170:350-359. DOI: 10.1016/j.neures.2020.12.001. View

Cheng B, Dietzmann P, Schulz R, Boenstrup M, Krawinkel L, Fiehler J . Cortical atrophy and transcallosal diaschisis following isolated subcortical stroke. J Cereb Blood Flow Metab. 2019; 40(3):611-621. PMC: 7026841. DOI: 10.1177/0271678X19831583. View

10.

Nelson E, Guyer A . The development of the ventral prefrontal cortex and social flexibility. Dev Cogn Neurosci. 2011; 1(3):233-45. PMC: 3143481. DOI: 10.1016/j.dcn.2011.01.002. View

11.

Murata Y, Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M . Effects of motor training on the recovery of manual dexterity after primary motor cortex lesion in macaque monkeys. J Neurophysiol. 2007; 99(2):773-86. DOI: 10.1152/jn.01001.2007. View

12.

Rohlfing T, Kroenke C, Sullivan E, Dubach M, Bowden D, Grant K . The INIA19 Template and NeuroMaps Atlas for Primate Brain Image Parcellation and Spatial Normalization. Front Neuroinform. 2012; 6:27. PMC: 3515865. DOI: 10.3389/fninf.2012.00027. View

13.

Rehme A, Fink G, von Cramon D, Grefkes C . The role of the contralesional motor cortex for motor recovery in the early days after stroke assessed with longitudinal FMRI. Cereb Cortex. 2010; 21(4):756-68. DOI: 10.1093/cercor/bhq140. View

14.

Bonstrup M, Schulz R, Schon G, Cheng B, Feldheim J, Thomalla G . Parietofrontal network upregulation after motor stroke. Neuroimage Clin. 2018; 18:720-729. PMC: 5987870. DOI: 10.1016/j.nicl.2018.03.006. View

15.

Yamamoto T, Oishi T, Higo N, Murayama S, Sato A, Takashima I . Differential expression of secreted phosphoprotein 1 in the motor cortex among primate species and during postnatal development and functional recovery. PLoS One. 2013; 8(5):e65701. PMC: 3669139. DOI: 10.1371/journal.pone.0065701. View

16.

Brown C, Li P, Boyd J, Delaney K, Murphy T . Extensive turnover of dendritic spines and vascular remodeling in cortical tissues recovering from stroke. J Neurosci. 2007; 27(15):4101-9. PMC: 6672555. DOI: 10.1523/JNEUROSCI.4295-06.2007. View

17.

He S, Dum R, Strick P . Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J Neurosci. 1993; 13(3):952-80. PMC: 6576595. View

18.

Kurata K . Hierarchical Organization Within the Ventral Premotor Cortex of the Macaque Monkey. Neuroscience. 2018; 382:127-143. DOI: 10.1016/j.neuroscience.2018.04.033. View

19.

Kassem M, Lagopoulos J, Stait-Gardner T, Price W, Chohan T, Arnold J . Stress-induced grey matter loss determined by MRI is primarily due to loss of dendrites and their synapses. Mol Neurobiol. 2012; 47(2):645-61. DOI: 10.1007/s12035-012-8365-7. View

20.

Schaechter J, Perdue K . Enhanced cortical activation in the contralesional hemisphere of chronic stroke patients in response to motor skill challenge. Cereb Cortex. 2007; 18(3):638-47. DOI: 10.1093/cercor/bhm096. View