Reorganization of Thalamic Inputs to Lesioned Cortex Following Experimental Traumatic Brain Injury
Traumatic brain injury (TBI) disrupts thalamic and cortical integrity. The effect of post-injury reorganization and plasticity in thalamocortical pathways on the functional outcome remains unclear. We evaluated whether TBI causes structural changes in the thalamocortical axonal projection terminals...
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| Format: | Article |
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MDPI AG
2021-06-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/22/12/6329 |
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| author | Xavier Ekolle Ndode-Ekane Maria del Mar Puigferrat Pérez Rossella Di Sapia Niina Lapinlampi Asla Pitkänen |
| author_facet | Xavier Ekolle Ndode-Ekane Maria del Mar Puigferrat Pérez Rossella Di Sapia Niina Lapinlampi Asla Pitkänen |
| author_sort | Xavier Ekolle Ndode-Ekane |
| collection | DOAJ |
| description | Traumatic brain injury (TBI) disrupts thalamic and cortical integrity. The effect of post-injury reorganization and plasticity in thalamocortical pathways on the functional outcome remains unclear. We evaluated whether TBI causes structural changes in the thalamocortical axonal projection terminals in the primary somatosensory cortex (S1) that lead to hyperexcitability. TBI was induced in adult male Sprague Dawley rats with lateral fluid-percussion injury. A virus carrying the fluorescent-tagged opsin channel rhodopsin 2 transgene was injected into the ventroposterior thalamus. We then traced the thalamocortical pathways and analyzed the reorganization of their axonal terminals in S1. Next, we optogenetically stimulated the thalamocortical relays from the ventral posterior lateral and medial nuclei to assess the post-TBI functionality of the pathway. Immunohistochemical analysis revealed that TBI did not alter the spatial distribution or lamina-specific targeting of projection terminals in S1. TBI reduced the axon terminal density in the motor cortex by 44% and in S1 by 30%. A nematic tensor-based analysis revealed that in control rats, the axon terminals in layer V were orientated perpendicular to the pial surface (60.3°). In TBI rats their orientation was more parallel to the pial surface (5.43°, difference between the groups <i>p <</i> 0.05). Moreover, the level of anisotropy of the axon terminals was high in controls (0.063) compared with TBI rats (0.045, <i>p <</i> 0.05). Optical stimulation of the sensory thalamus increased alpha activity in electroencephalography by 312% in controls (<i>p ></i> 0.05) and 237% (<i>p ></i> 0.05) in TBI rats compared with the baseline. However, only TBI rats showed increased beta activity (33%) with harmonics at 5 Hz. Our findings indicate that TBI induces reorganization of thalamocortical axonal terminals in the perilesional cortex, which alters responses to thalamic stimulation. |
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| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T10:26:53Z |
| publishDate | 2021-06-01 |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-f4f1aa37543d47038eb14efd900b73472023-11-21T23:57:45ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-06-012212632910.3390/ijms22126329Reorganization of Thalamic Inputs to Lesioned Cortex Following Experimental Traumatic Brain InjuryXavier Ekolle Ndode-Ekane0Maria del Mar Puigferrat Pérez1Rossella Di Sapia2Niina Lapinlampi3Asla Pitkänen4A. I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, FI-70211 Kuopio, FinlandA. I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, FI-70211 Kuopio, FinlandA. I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, FI-70211 Kuopio, FinlandA. I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, FI-70211 Kuopio, FinlandA. I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, FI-70211 Kuopio, FinlandTraumatic brain injury (TBI) disrupts thalamic and cortical integrity. The effect of post-injury reorganization and plasticity in thalamocortical pathways on the functional outcome remains unclear. We evaluated whether TBI causes structural changes in the thalamocortical axonal projection terminals in the primary somatosensory cortex (S1) that lead to hyperexcitability. TBI was induced in adult male Sprague Dawley rats with lateral fluid-percussion injury. A virus carrying the fluorescent-tagged opsin channel rhodopsin 2 transgene was injected into the ventroposterior thalamus. We then traced the thalamocortical pathways and analyzed the reorganization of their axonal terminals in S1. Next, we optogenetically stimulated the thalamocortical relays from the ventral posterior lateral and medial nuclei to assess the post-TBI functionality of the pathway. Immunohistochemical analysis revealed that TBI did not alter the spatial distribution or lamina-specific targeting of projection terminals in S1. TBI reduced the axon terminal density in the motor cortex by 44% and in S1 by 30%. A nematic tensor-based analysis revealed that in control rats, the axon terminals in layer V were orientated perpendicular to the pial surface (60.3°). In TBI rats their orientation was more parallel to the pial surface (5.43°, difference between the groups <i>p <</i> 0.05). Moreover, the level of anisotropy of the axon terminals was high in controls (0.063) compared with TBI rats (0.045, <i>p <</i> 0.05). Optical stimulation of the sensory thalamus increased alpha activity in electroencephalography by 312% in controls (<i>p ></i> 0.05) and 237% (<i>p ></i> 0.05) in TBI rats compared with the baseline. However, only TBI rats showed increased beta activity (33%) with harmonics at 5 Hz. Our findings indicate that TBI induces reorganization of thalamocortical axonal terminals in the perilesional cortex, which alters responses to thalamic stimulation.https://www.mdpi.com/1422-0067/22/12/6329axonal injuryhyperexcitationlateral fluid-percussion injuryperilesional cortexthalamo-cortical projectiontraumatic brain injury |
| spellingShingle | Xavier Ekolle Ndode-Ekane Maria del Mar Puigferrat Pérez Rossella Di Sapia Niina Lapinlampi Asla Pitkänen Reorganization of Thalamic Inputs to Lesioned Cortex Following Experimental Traumatic Brain Injury International Journal of Molecular Sciences axonal injury hyperexcitation lateral fluid-percussion injury perilesional cortex thalamo-cortical projection traumatic brain injury |
| title | Reorganization of Thalamic Inputs to Lesioned Cortex Following Experimental Traumatic Brain Injury |
| title_full | Reorganization of Thalamic Inputs to Lesioned Cortex Following Experimental Traumatic Brain Injury |
| title_fullStr | Reorganization of Thalamic Inputs to Lesioned Cortex Following Experimental Traumatic Brain Injury |
| title_full_unstemmed | Reorganization of Thalamic Inputs to Lesioned Cortex Following Experimental Traumatic Brain Injury |
| title_short | Reorganization of Thalamic Inputs to Lesioned Cortex Following Experimental Traumatic Brain Injury |
| title_sort | reorganization of thalamic inputs to lesioned cortex following experimental traumatic brain injury |
| topic | axonal injury hyperexcitation lateral fluid-percussion injury perilesional cortex thalamo-cortical projection traumatic brain injury |
| url | https://www.mdpi.com/1422-0067/22/12/6329 |
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