Handedness Shift as a Consequence of Motor Cortex Reorganization After Early Functional Impairment in Left Temporal Lobe Epilepsy—An fMRI Case Report

Chlebus, Pavel; Brázdil, Milan; Hluštı́k, Petr; Mikl, Michal; Pažourková, Marta; Krůpa, Petr

doi:10.1080/13554790490507669

Cited by 17 publications

(8 citation statements)

References 13 publications

(8 reference statements)

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“…The majority of our patients had lesional (MTS, FCD), or non-lesional epilepsy and data about ipsilateral motor responses in these patient groups are rare, but could be potentially interesting for resective epilepsy surgery around motor areas. We only found one report of an ipsilateral response in MTS ( Chlebus et al, 2004 ) and one case report with FCD ( Maegaki et al, 1995 ). Recently, Mäkelä et al described two patients from a group of 19 patients with intractable epilepsy, with unexpected motor cortex localization, of whom one had a history of a large perinatal vascular infarction in the left hemisphere and ipsilateral hand motor cortex representation in the right hemisphere ( Mäkelä et al, 2013 ).…”

Section: Discussionmentioning

confidence: 99%

Magnetoencephalographic study of hand and foot sensorimotor organization in 325 consecutive patients evaluated for tumor or epilepsy surgery

Willemse

Hillebrand

Ronner

et al. 2016

NeuroImage: Clinical

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ObjectivesThe presence of intracranial lesions or epilepsy may lead to functional reorganization and hemispheric lateralization. We applied a clinical magnetoencephalography (MEG) protocol for the localization of the contralateral and ipsilateral S1 and M1 of the foot and hand in patients with non-lesional epilepsy, stroke, developmental brain injury, traumatic brain injury and brain tumors. We investigated whether differences in activation patterns could be related to underlying pathology.MethodsUsing dipole fitting, we localized the sources underlying sensory and motor evoked magnetic fields (SEFs and MEFs) of both hands and feet following unilateral stimulation of the median nerve (MN) and posterior tibial nerve (PTN) in 325 consecutive patients. The primary motor cortex was localized using beamforming following a self-paced repetitive motor task for each hand and foot.ResultsThe success rate for motor and sensory localization for the feet was significantly lower than for the hands (motor_hand 94.6% versus motor_feet 81.8%, p < 0.001; sensory_hand 95.3% versus sensory_feet 76.0%, p < 0.001). MN and PTN stimulation activated 86.6% in the contralateral S1, with ipsilateral activation < 0.5%. Motor cortex activation localized contralaterally in 76.1% (5.2% ipsilateral, 7.6% bilateral and 11.1% failures) of all motor MEG recordings. The ipsilateral motor responses were found in 43 (14%) out of 308 patients with motor recordings (range: 8.3–50%, depending on the underlying pathology), and had a higher occurrence in the foot than in the hand (motor_foot 44.8% versus motor_hand 29.6%, p = 0.031). Ipsilateral motor responses tended to be more frequent in patients with a history of stroke, traumatic brain injury (TBI) or developmental brain lesions (p = 0.063).ConclusionsMEG localization of sensorimotor cortex activation was more successful for the hand compared to the foot. In patients with neural lesions, there were signs of brain reorganization as measured by more frequent ipsilateral motor cortical activation of the foot in addition to the traditional sensory and motor activation patterns in the contralateral hemisphere. The presence of ipsilateral neural reorganization, especially around the foot motor area, suggests that careful mapping of the hand and foot in both contralateral and ipsilateral hemispheres prior to surgery might minimize postoperative deficits.

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Section: Discussionmentioning

confidence: 99%

Magnetoencephalographic study of hand and foot sensorimotor organization in 325 consecutive patients evaluated for tumor or epilepsy surgery

Willemse

Hillebrand

Ronner

et al. 2016

NeuroImage: Clinical

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“…Remapping revealed a reorganization of arm, face, and eye movement representations that took place after the first mapping session. Moreover, functional MRI has been used to demonstrate motor neocortex reorganization and a subsequent shift of handedness as well as involuntary "mirror" movements of fingers in the nondominant hand in a patient with temporal lobe epilepsy (7). Thus it appears that repeated seizure activity in humans and nonhumans can alter the functional organization of motor neocortex, with alterations in motor behavior.…”

Section: Discussionmentioning

confidence: 99%

“…Because Penfield's homunculus was based on data obtained from patients with epilepsy, this suggests that recurrent seizure activity may induce changes in the topography of neocortical movement representations. Supportive evidence for this suggestion comes from a few reports that some people with epilepsy have atypically organized motor maps (4)(5)(6)(7).…”

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confidence: 98%

Hippocampal Kindling Leads to Motor Map Expansion

et al. 2006

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Summary:Purpose: To determine whether seizure activity, repeatedly elicited in the hippocampus, could alter the functional organization of neocortical movement representations (motor maps) and whether a relation exists between the number of afterdischarges recorded in the sensorimotor neocortex and the size of the motor maps.Methods: We electrically kindled the right ventral hippocampus of Long-Evans hooded rats, twice daily, for 40 sessions and recorded the afterdischarges in the stimulated hippocampus and right sensorimotor neocortex. Between 3 and 7 days after the last seizure, we used high-resolution intracortical microstimulation to derive the forelimb-movement representations in the left (un-implanted) sensorimotor neocortex.Results: In the hippocampal kindled rats, we observed a dramatic expansion of the area of neocortex that would elicit forelimb movements compared with sham-kindled controls. The number of afterdischarges recorded in the neocortex was significantly and positively correlated with the size of the motor maps.Conclusions: Seizures propagating from the hippocampus have long-distance effects on the functional organization of motor maps.

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“…The mammalian neocortex is organized into topographic maps (Kaas, 1997). People with epilepsy have been shown to have differently organized sensory (Uematsu et al., 1992; Urasaki et al., 1994) and motor (Uematsu et al., 1992; Urasaki et al., 1994; Lado et al., 2002; Branco et al., 2003; Chlebus et al., 2004; Labyt et al., 2007) maps. These changes in the topographic maps may be associated with interictal behavioral deficits in planning and executing voluntary movements that some people with epilepsy display when the seizure focus is in the frontal lobes (Helmstaedter et al., 1996; Matsuoka et al., 2000; Hernandez et al., 2002).…”

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confidence: 99%

Persistent enhancement of functional MRI responsiveness to sensory stimulation following repeated seizures

et al. 2011

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SUMMARYPurpose: Neural reorganization and interictal behavioral anomalies have been documented in people with epilepsy and in animal seizure models. Alterations in behavior could be due to somatosensory dysfunction. This study was designed to determine whether seizures can lead to changes in somatosensory representations and whether those changes are persistent. Methods: Twice-daily seizures were elicited by delivering 1 s of electrical stimulation through carbon fiber electrodes implanted in both the corpus callosum and sensorimotor neocortex of young adult male Long-Evans rats until a total of 20 seizures were elicited. Either 1-3 days or 3-5 weeks following the last seizure, functional magnetic resonance imaging (MRI) was used to image the brain during electrical stimulation of each forepaw independently. Key Findings: Forepaw stimulation in control rats resulted in a focused and contralateral fMRI signal in the somatosensory neocortex. Rats that had repeated seizures had a 151% increase in the number of voxels activated in the contralateral hemisphere 1-3 days after the last seizure and a 166% increase at 3-5 weeks after the last seizure. The number of voxels activated in response to forepaw stimulation was positively correlated with the duration of the longest seizure experienced by each rat. The intensity of the activated voxels was not significantly increased at either time interval from the last seizure. Significance: The increased area of activation in somatosensory cortex, which is persistent at 3-5 weeks, is consistent with previous observations of larger motor maps following seizures. Seizure-induced changes in the functioning of sensory cortex may also contribute to interictal behavioral anomalies.

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Handedness Shift as a Consequence of Motor Cortex Reorganization After Early Functional Impairment in Left Temporal Lobe Epilepsy—An fMRI Case Report

Cited by 17 publications

References 13 publications

Magnetoencephalographic study of hand and foot sensorimotor organization in 325 consecutive patients evaluated for tumor or epilepsy surgery

Magnetoencephalographic study of hand and foot sensorimotor organization in 325 consecutive patients evaluated for tumor or epilepsy surgery

Hippocampal Kindling Leads to Motor Map Expansion

Persistent enhancement of functional MRI responsiveness to sensory stimulation following repeated seizures

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