Reorganization of the Hand Somatosensory Cortex Following Perinatal Unilateral Brain Injury

Functional magnetic resonance imaging was used to map the hand somatosensory cortices of nine hemiparetic young adult patients with perinatal unilateral brain injury in the sensorimotor area and five normal subjects. Stimulation of the paretic hand by periodic manual squeezing produced activation in the contralateral hemisphere of three patients and in the ipsilateral hemisphere of three other patients. Paretic hand stimulation produced no activation in either hemisphere of the remaining three patients. Therefore, one-third of the patients demonstrated functional “plasticity” of the brain in the form of inter-hemispheric relocation of the hand somatosensory function. The volume and pattern of activation for both hands was altered for those patients that showed evidence of cortical reorganization to the opposite hemisphere. This differs from the hand motor system, which exhibited inter-hemispheric reorganization in a higher proportion of a related group of hemiparetic subjects.

Key words

Brain plasticity - Perinatal brain injury - Somatosensory cortex - Functional magnetic resonance imaging - FMRI, BOLD - Functional reorganization

References

• 1 Albe-Fessard D. Organization of somatic central projections. Neff WD Contributions to Sensory Physiology. Vol. 2. New York; Academic Press 1967: 101-168
• 2 Bandettini P A, Jesmanowicz A, Wong E C, Hyde J S. Processing strategies for timecourse data sets in functional MRI of the human brain.  Mag Res Med. 1993;  30 161-173
• 3 Belliveau J W, Kennedy D N, McKinstry R C, Buchbinder B R, Weisskoff R M, Cohen M S. et al . Functional mapping of the human visual cortex by magnetic resonance imaging.  Science. 1991;  254 716-719
• 4 Burton H. Second somatosensory cortex and related areas. Jones EG, Peters A Cerebral Cortex: Sensory-motor Areas and Aspects of Cortical Connectivity. New York; Plenum 1986: 31-98
• 5 Cao Y, D'Olhaberriague L, Vikingstad E M, Levine S R, Welch K MA. Pilot study of functional MRI to assess cerebral activation of motor function after poststroke hemiparesis.  Stroke. 1998;  29 112-122
• 6 Cao Y, Vikingstad E M, Huttenlocher P R, Towle V L, Levin D N. Functional magnetic resonance studies of the reorganization of the human hand sensorimotor area after unilateral brain injury in the perinatal period.  Proc Nat Acad Sci USA. 1994;  91 9612-9616
• 7 D'Amato C J, Hicks S P. Normal development and post-traumatic plasticity of corticospinal neurons in rats.  Exp Neurol. 1978;  60 557-569
• 8 Finger S, LeVere T E, Almli C R, Stein D G. Brain Injury and Recovery. New York; Plenum Press 1988
• 9 Flor H, Elbert T, Knecht S, Wienbruch C, Pantev C, Birbaumer N. et al . Phantomlimb pain as a perceptual correlate of cortical reorganization following arm amputation.  Nature. 1995;  378 482-484
• 10 Huttenlocher P R, Raichelson R M. Effects of neonatal hemispherectomy on location and number of corticospinal neurons in the rat.  Dev Brn Res. 1989;  47 59-69
• 11 Innocenti G M. Exuberant development of connections, and its possible permissive role in cortical evolution.  Trends Neurosci. 1995;  18 397-402
• 12 Julez B, Kovacs I. Maturational windows and adult cortical plasticity. Addison-Wesley 1995
• 13 Kaas J H. Somatosensory system. Paxinos G The Human Nervous System. San Diego; Academic Press 1990: 813-844
• 14 Lenn N J, Freinkel A J. Facial sparing as a feature of prenatal-onset hemiparesis.  Ped Neurol. 1989;  5 291-295
• 15 LeVere N D, Gray-Silva S, LeVere T E. Infant brain injury. Finger S, LeVere TE, Almli CR, Stein DG Brain Injury and Recovery. New York; Plenum Press 1988: 133-150
• 16 Levin D N, Hu X, Tan K K, Galhotra S, Pelizzari C A, Chen G TY. et al . The brain: Integrated three-dimensional display of MR and PET images.  Radiol. 1989;  172 783-789
• 17 Levine R I, Jacobson M. Discontinuous mapping of retina onto tectum innervated by both eyes.  Brn Res. 1975;  98 172-176
• 18 Lewine J D, Astur R S, Davis L E, Knight J E, Maclin E L, Orrison W W. Cortical organization in adulthood is modified by neonatal infarct: A case study.  Radiol. 1994;  190 93-96
• 19 Lüders H, Lesser R P, Dinner D S, Hahn J F, Salanga V, Morris H H. The second sensory area in humans: Evoked potential and electrical stimulation studies.  Ann Neurol. 1985;  17 177-184
• 20 Lund R D, Lund J S. Reorganization of the retinotectal pathway in rats after neonatal retinal lesions.  Exp Neurol. 1973;  40 377-390
• 21 Merzenich M M, Nelson R J, Stryker M P, Cynader M S, Schoppmann A, Zook J M. Somatosensory cortical map changes following digit amputation in adult monkeys.  J Comp Neurol. 1984;  224 591-605
• 22 Ogawa S, Tank D W, Menon R, Ellermann J M, Kim S G, Merkel H. et al . Intrinsic signal changes accompanying sensory stimulation: Functional brain mapping with magnetic resonance imaging.  Proc Nat Acad Sci USA. 1992;  89 5951-5955
• 23 Pons T P, Garraghty P E, Ommaya A K, Kaas J H, Taub E, Mishkin M. Massive cortical reorganization after sensory deafferentation in adult macaques.  Science. 1991;  252 1857-1860
• 24 Ramachandran V S. Filling in gaps in perception: II. Scotomas and phantom limbs.  Curr Direct Psychol Sci. 1993;  2 36-65
• 25 Ramachandran V S, Stewart M, Rogers-Ramachandran D C. Perceptual correlates of massive cortical reorganization.  NeuroReport. 1992;  3 583-586
• 26 Sharma S C. Reformation of retinotectal projections after various tectal ablations in adult goldfish.  Exp Neurol. 1972;  34 171-182
• 27 Stanfield B B, O'Leary D DM. The transient corticospinal projection from occipital cortex during the postnatal development of the rat.  J Comp Neurol. 1985;  238 236-248
• 28 Ueki K. Hemispherectomy in the human with special reference to the preservation of motor and sensory function.  Adv Neurol Sci. 1988;  24 644-660
• 29 Van der Loos H, Dörfl J. Does the skin tell the somatosensory cortex how to construct a map of the periphery?.  Neurosci Lett. 1978;  7 23-30
• 30 Villablanca J R, Gómez-Pinilla F. Novel crossed corticothalamic projections after neonatal cerebral hemispherectomy. A quantitative autoradiography study in cats.  Brn Res. 1987;  410 219-231
• 31 Villablanca J R, Gómez-Pinilla F, Sonnier B J, Hovda D A. Bilateral pericruciate cortical innervation of the red nucleus in cats with adult or neonatal cerebral hemispherectomy.  Brn Res. 1988;  453 17-31
• 32 Weiller C, Chollet F, Friston K J, Wise R JS, Frackowiak R SJ. Functional reorganization of the brain in recovery from striatocapsular infarction in man.  Ann Neurol. 1992;  31 463-472
• 33 Woods R P, Cherry S R, Mazziotta J C. Rapid automated algorithm for aligning and reslicing PET mages.  J Comp Assist Tomogr. 1992;  16 620-633