Decreased resting functional connectivity after traumatic brain injury in the rat

Traumatic brain injury (TBI) contributes to about 10% of acquired epilepsy. Even though the mechanisms of post-traumatic epileptogenesis are poorly known, a disruption of neuronal networks predisposing to altered neuronal synchrony remains a viable candidate mechanism. We tested a hypothesis that re...

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Bibliographic Details
Published in:PloS one 2014-04, Vol.9 (4), p.e95280-e95280
Main Authors: Mishra, Asht Mangal, Bai, Xiaoxiao, Sanganahalli, Basavaraju G, Waxman, Stephen G, Shatillo, Olena, Grohn, Olli, Hyder, Fahmeed, Pitkänen, Asla, Blumenfeld, Hal
Format: Article
Language:English
Subjects:
Abnormalities
Animals
Biology and Life Sciences
Brain
Brain Injuries - physiopathology
Brain mapping
Cortex (frontal)
Cortex (parietal)
EEG
Electrodes
Electroencephalography
Epilepsy
Firing pattern
Fluid filters
Functional magnetic resonance imaging
Head injuries
Hippocampus
Histology
Image analysis
Image processing
Injuries
Low pass filters
Magnetic permeability
Magnetic resonance
Magnetic Resonance Imaging
Male
Medicine and Health Sciences
Neural networks
Neuroimaging
Neurosciences
NMR
Nuclear magnetic resonance
Percussion
Rats
Rats, Sprague-Dawley
Research and Analysis Methods
Rodents
Seizures
Seizures - physiopathology
Statistical analysis
Surgery
Thalamus
Traumatic brain injury
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Summary:Traumatic brain injury (TBI) contributes to about 10% of acquired epilepsy. Even though the mechanisms of post-traumatic epileptogenesis are poorly known, a disruption of neuronal networks predisposing to altered neuronal synchrony remains a viable candidate mechanism. We tested a hypothesis that resting state BOLD-fMRI functional connectivity can reveal network abnormalities in brain regions that are connected to the lesioned cortex, and that these changes associate with functional impairment, particularly epileptogenesis. TBI was induced using lateral fluid-percussion injury in seven adult male Sprague-Dawley rats followed by functional imaging at 9.4T 4 months later. As controls we used six sham-operated animals that underwent all surgical operations but were not injured. Electroencephalogram (EEG)-functional magnetic resonance imaging (fMRI) was performed to measure resting functional connectivity. A week after functional imaging, rats were implanted with bipolar skull electrodes. After recovery, rats underwent pentyleneterazol (PTZ) seizure-susceptibility test under EEG. For image analysis, four pairs of regions of interests were analyzed in each hemisphere: ipsilateral and contralateral frontal and parietal cortex, hippocampus, and thalamus. High-pass and low-pass filters were applied to functional imaging data. Group statistics comparing injured and sham-operated rats and correlations over time between each region were calculated. In the end, rats were perfused for histology. None of the rats had epileptiform discharges during functional imaging. PTZ-test, however revealed increased seizure susceptibility in injured rats as compared to controls. Group statistics revealed decreased connectivity between the ipsilateral and contralateral parietal cortex and between the parietal cortex and hippocampus on the side of injury as compared to sham-operated animals. Injured animals also had abnormal negative connectivity between the ipsilateral and contralateral parietal cortex and other regions. Our data provide the first evidence on abnormal functional connectivity after experimental TBI assessed with resting state BOLD-fMRI.
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0095280