Congenital hemiparesis: Different functional reorganization of somatosensory and motor pathways

Azienda Ospedaliera Santa Maria Nuova di Reggio Emilia, Reggio nell'Emilia, Emilia-Romagna, Italy
Clinical Neurophysiology (Impact Factor: 3.1). 09/2002; 113(8):1273-8. DOI: 10.1016/S1388-2457(02)00150-5
Source: PubMed


To investigate the reorganization of somatosensory and motor cortex in congenital brain injury.
We recorded motor evoked potentials (MEPs) following transcranial magnetic stimulation (TMS) and somatosensory evoked potentials (SEPs) in a 41 year old man with severe congenital right hemiparesis but only mild proprioceptive impairment. Brain magnetic resonance imaging showed a large porencephalic cavitation in the left hemisphere mainly involving the frontal and parietal lobes.
TMS showed fast-conducting projections from the undamaged primary motor cortex to both hands, whereas MEPs were not elicited from the damaged hemisphere. Left median nerve stimulation evoked normal short-latency SEPs in the contralateral undamaged somatosensory cortex. Right median nerve stimulation did not evoke any SEP in the contralateral damaged hemisphere, but a middle-latency SEP (positive-negative-positive, 39-44-48 ms) in the ipsilateral undamaged hemisphere, with a fronto-central scalp distribution.
Our data show that somatosensory function of the affected arm is preserved, most likely through slow-conducting non-lemniscal connections between the affected arm and ipsilateral non-primary somatosensory cortex. In contrast, motor function was poor despite fast-conducting ipsilateral cortico-motoneuronal output from the primary motor cortex of the undamaged hemisphere to the affected arm. This suggests that different forms of reorganization operate in congenital brain injury and that fast-conducting connections between primary cortex areas and ipsilateral spinal cord are not sufficient for preservation or recovery of function.

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    • "Thus, reduced and stereotypical pattern of spontaneous movements in patients with hemiplegic CP would result in abnormal sensory feedback and altered cortical reorganization, thus leading to asymmetric somatosensory processing deficits [25,26]. A case study by Ragazzoni and colleagues (2002) [27] has further showed that somatosensory function of the affected (right) arm was preserved, whereas motor function was poor despite fast-conducting ipsilateral cortico-motoneuronal output from primary motor cortex of the intact hemisphere to the affected arm. This finding seems to suggest that different forms of motor and somatosensory reorganization are involved in congenital brain injury, and that fast-conducting connections between primary cortex areas and ipsilateral spinal cord are not sufficient for preservation or recovery of function. "
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    ABSTRACT: Although cerebral palsy (CP) is usually defined as a group of permanent motor disorders due to non-progressive disturbances in the developing fetal or infant brain, recent research has shown that CP individuals are also characterized by altered somatosensory perception, increased pain and abnormal activation of cortical somatosensory areas. The present study was aimed to examine hemispheric differences on somatosensory brain processing in individuals with bilateral CP and lateralized motor impairments compared with healthy controls. Nine CP individuals with left-dominant motor impairments (LMI) (age range 5-28 yrs), nine CP individuals with right-dominant motor impairments (RMI) (age range 7-29 yrs), and 12 healthy controls (age range 5-30 yrs) participated in the study. Proprioception, touch and pain thresholds, as well as somatosensory evoked potentials (SEP) elicited by tactile stimulation of right and left lips and thumbs were compared. Pain sensitivity was higher, and lip stimulation elicited greater beta power and more symmetrical SEP amplitudes in individuals with CP than in healthy controls. In addition, although there was no significant differences between individuals with RMI and LMI on pain or touch sensitivity, lip and thumb stimulation elicited smaller beta power and more symmetrical SEP amplitudes in individuals with LMI than with RMI. Our data revealed that brain processing of somatosensory stimulation was abnormal in CP individuals. Moreover, this processing was different depending if they presented right- or left-dominant motor impairments, suggesting that different mechanisms of sensorimotor reorganization should be involved in CP depending on dominant side of motor impairment.
    Full-text · Article · Jan 2014 · BMC Neuroscience
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    • "When electrical median nerve stimulation of the paretic hand was used to elicit somatosensory-evoked potentials (SEPs) in congenitally hemiparetic patients with extended lesions (Ragazzoni et al. 2002) or posthemispherectomy (Bernasconi et al. 2000; Holloway et al. 2000), all ipsilateral cortical responses showed prolonged latencies (39--65 ms) and abnormal topographies. This was interpreted as evidence for ipsilateral reorganization via nonlemniscal sensory fibers (Ragazzoni et al. 2002). Maegaki et al. (1995) reported on a child with a large unilateral malformation, in whom median nerve stimulation of the paretic hand evoked an atypically configured early cortical SEP in the contralateral (malformed) hemisphere and an additional early negative component (N20) in the contralesional hemisphere. "
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    ABSTRACT: The developing brain possesses a high potential for neuroplasticity. Yet, this remarkable potential of (re-)organization is not a general principle. It seems to vary among different functional systems. Here, we show that distinct brain structures involved in somatosensory processing are already prenatally determined so that a pre- or perinatally acquired (congenital) brain damage of such structures results in a persistent somatosensory deficit. Eleven patients with hemiparesis due to congenital cortico-subcortical unilateral stroke who showed versus not showed a somatosensory deficit were contrasted with magnetic resonance imaging lesion–behavior mapping. The brain areas which were typically damaged in patients with a somatosensory deficit but typically spared in patients without a somatosensory deficit were located in the primary and secondary somatosensory cortex (S1, S2) as well as the inferior parietal cortex directly neighboring S1 and S2. The results argue for an early functional determination of primary and secondary somatosensory cortex, without substantial capacities for (re-)organization. They demonstrate that cortical damage of these areas cannot be compensated by shifting the functional representation to undamaged parts of the cortex.
    Preview · Article · Jul 2011 · Cerebral Cortex
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    • "In recent years, several groups have shown a special mechanism of compensation in the motor domain: following unilateral early brain lesions, the neuronal representation of the primary motor region (M1) is reorganized to the ipsilateral hemisphere [i.e., both motor representations are located in the contralesional hemisphere; Carr et al., 1993, Guzzetta et al., 2007a; Jang et al., 2001; Ragazzoni et al., 2002]. This pattern of motor reorganization is influenced by lesion size [only larger lesions will induce this ''shift''; Staudt et al., 2000, 2002]; it is nicely explained by neuroembryological studies showing that the adult pattern of contralateral motor representation is preceded by early bilateral motor projections which are only ''withdrawn'' later, depending on activity [Carr et al., 1993; Eyre et al., 2001]. "
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    ABSTRACT: This study investigates the (re-)organization of somatosensory functions following early brain lesions. Using functional magnetic resonance imaging (fMRI), passive hand movement was studied. Transcranial magnetic stimulation (TMS) and magnetoencephalography (MEG) were used as complementary methods. fMRI data was analyzed on the first level with regard to topographical variability; second-level group effects as well as the overall integrity of the somatosensory circuitry were also assessed. Subjects with unilateral brain lesions occurring in the third trimester of pregnancy or perinatally with different types of motor reorganization were included: patients with regular, contralateral motor organization following middle cerebral artery strokes (CONTRA(MCA), n = 6) and patients with reorganized, ipsilateral motor functions due to periventricular lesions (IPSI(PL), n = 8). Motor impairment was similar, but sensory impairment was more pronounced in the CONTRA(MCA) group. Using fMRI and MEG, both groups showed a normal pattern with a contralateral somatosensory representation, despite the transhemispherically reorganized primary motor cortex in the IPSI(PL) group, as verified by TMS. Activation topography for the paretic hands was more variable than for the nonparetic hand in both groups. The cortico-cerebellar circuitry was well-preserved in almost all subjects. We conclude that in both models of motor reorganization, no interhemispheric reorganization of somatosensory functions occurred. Also, no relevant intrahemispheric reorganization was observed apart from a higher topographical variability of fMRI activations. This preserved pattern of somatosensory organization argues in favor of a differential lesion effect on motor and somatosensory functions and demonstrates a limited compensatory potential for the latter.
    Full-text · Article · Mar 2009 · Human Brain Mapping
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