Role of the corpus callosum in the somatosensory activation of the ipsilateral cerebral cortex: an fMRI study of callosotomized patients

To verify whether the activation of the posterior parietal and parietal opercular cortices to tactile stimulation of the ipsilateral hand is mediated by the corpus callosum, a functional magnetic resonance imaging (fMRI, 1.0 tesla) study was performed in 12 control and 12 callosotomized subjects (three with total and nine with partial resection). Eleven patients were also submitted to the tactile naming test. In all subjects, unilateral tactile stimulation provoked a signal increase temporally correlated with the stimulus in three cortical regions of the contralateral hemisphere. One corresponded to the first somatosensory area, the second was in the posterior parietal cortex, and the third in the parietal opercular cortex. In controls, activation was also observed in the ipsilateral posterior parietal and parietal opercular cortices, in regions anatomically corresponding to those activated contralaterally. In callosotomized subjects, activation in the ipsilateral hemisphere was observed only in two patients with splenium and posterior body intact. These two patients and another four with the entire splenium and variable portions of the posterior body unsectioned named objects explored with the right and left hand without errors. This ability was impaired in the other patients. The present physiological and anatomical data indicate that in humans activation of the posterior parietal and parietal opercular cortices in the hemisphere ipsilateral to the stimulated hand is mediated by the corpus callosum, and that the commissural fibres involved probably cross the midline in the posterior third of its body.

[1]  Harold Burton,et al.  Second Somatosensory Cortex and Related Areas , 1986 .

[2]  E C Wong,et al.  Effect of motion outside the field of view on functional MR. , 1996, AJNR. American journal of neuroradiology.

[3]  C C Wood,et al.  Human cortical potentials evoked by stimulation of the median nerve. II. Cytoarchitectonic areas generating long-latency activity. , 1989, Journal of neurophysiology.

[4]  R. Sperry,et al.  Interhemispheric Communication After Section of the Forebrain Commissures , 1985, Cortex.

[5]  S. Röricht,et al.  Topography of fibers in the human corpus callosum mediating interhemispheric inhibition between the motor cortices , 1998, Annals of neurology.

[6]  K. Uğurbil,et al.  Functional magnetic resonance imaging of the human brain , 1997, Journal of Neuroscience Methods.

[7]  Extent and limits of cerebral adjustment to early section or congenital absence of the corpus callosum , 1988, Behavioural Brain Research.

[8]  G. Ettlinger,et al.  Tactile Discrimination Learning in the Monkey: The Effects of Unilateral or Bilateral Removals of the Second Somatosensory Cortex (Area SII) , 1980, Cortex.

[9]  J. Kaas,et al.  The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of new and old world monkeys , 1983, The Journal of comparative neurology.

[10]  M. Fabri,et al.  Callosal projections from area SII to SI in monkeys: Anatomical organization and comparison with association projections , 1986, The Journal of comparative neurology.

[11]  E. Ross,et al.  Topography of the Human Corpus Callosum , 1985, Journal of neuropathology and experimental neurology.

[12]  Elisabeth A. Murray,et al.  Relative contributions of SII and area 5 to tactile discrimination in monkeys , 1984, Behavioural Brain Research.

[13]  H Burton,et al.  Somatotopographic organization in the second somatosensory area of M. fascicularis , 1980, The Journal of comparative neurology.

[14]  R Caminiti,et al.  The callosal system of the superior parietal lobule in the monkey , 1985, The Journal of comparative neurology.

[15]  Hiroshi Shibasaki,et al.  Human second somatosensory area: subdural and magnetoencephalographic recording of somatosensory evoked responses , 1997, Journal of neurology, neurosurgery, and psychiatry.

[16]  R Caminiti,et al.  Corticocortical efferent systems in the monkey: A quantitative spatial analysis of the tangential distribution of cells of origin , 1985, The Journal of comparative neurology.

[17]  Commissurotomy studies in animals , 1990 .

[18]  P. Barbaresi,et al.  Callosal mechanism for the interhemispheric transfer of hand somatosensory information in the monkey , 1984, Behavioural Brain Research.

[19]  R. Sperry,et al.  Absence of deconnexion syndrome in two patients with partial section of the neocommissures. , 1971, Brain : a journal of neurology.

[20]  R. Caselli,et al.  Ventrolateral and dorsomedial somatosensory association cortex damage produces distinct somesthetic syndromes in humans , 1993, Neurology.

[21]  Nikolaus M. Szeverenyi,et al.  Fingertip Representation in the Human Somatosensory Cortex: An fMRI Study , 1998, NeuroImage.

[22]  Riitta Salmelin,et al.  Tactile information from the human hand reaches the ipsilateral primary somatosensory cortex , 1995, Neuroscience Letters.

[23]  R. Hari,et al.  Separate finger representations at the human second somatosensory cortex , 1990, Neuroscience.

[24]  William Byne,et al.  Can the corpus callosum predict gender, age, handedness, or cognitive differences? , 1986, Trends in Neurosciences.

[25]  E. Cabanis,et al.  The Human Brain: Surface, Three-Dimensional Sectional Anatomy and Mri , 1991 .

[26]  N. Picard,et al.  Bilateral receptive fields in cortical area SII: contribution of the corpus callosum and other interhemispheric commissures. , 1990, Somatosensory & motor research.

[27]  M Hämäläinen,et al.  Neuromagnetic responses from the second somatosensory cortex in man , 1983, Acta neurologica Scandinavica.

[28]  G. Spidalieri,et al.  Relevance of the callosal transfer in defining the peripheral reactivity of somesthetic cortical neurones. , 1973, Archives italiennes de biologie.

[29]  David C. Alsop,et al.  Mapping of secondary somatosensory cortex activation induced by vibrational stimulation: an fMRI study , 1999, Brain Research.

[30]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[31]  J. Kaas,et al.  Corticocortical connections of area 2 of somatosensory cortex in macaque monkeys: A correlative anatomical and electrophysiological study , 1986, The Journal of comparative neurology.

[32]  Mara Fabri,et al.  Cortical areas within the lateral sulcus connected to cutaneous representations in areas 3b and 1: A revised interpretation of the second somatosensory area in macaque monkeys , 1995, The Journal of comparative neurology.

[33]  R P Lesser,et al.  The second sensory area in humans: Evoked potential and electrical stimulation studies , 1985, Annals of neurology.

[34]  R W Sperry,et al.  Hemisphere deconnection and unity in conscious awareness. , 1968, The American psychologist.

[35]  Mortimer Mishkin,et al.  Analogous neural models for tactual and visual learning , 1979, Neuropsychologia.

[36]  H. Burton,et al.  Somatic submodality distribution within the second somatosensory (SII), 7b, retroinsular, postauditory, and granular insular cortical areas of M. fascicularis , 1980, The Journal of comparative neurology.

[37]  D. Simons,et al.  Thalamic and corticocortical connections of the second somatic sensory area of the mouse , 1987, The Journal of comparative neurology.

[38]  H Burton,et al.  Functional MRI in human somatosensory cortex activated by touching textured surfaces , 1996, Journal of magnetic resonance imaging : JMRI.

[39]  E. Zaidel Stereognosis in the chronic split brain: hemispheric differences, ipsilateral control and sensory integration across the midline , 1998, Neuropsychologia.

[40]  R. Hari,et al.  Cerebral magnetic fields evoked by peroneal nerve stimulation. , 1986, Somatosensory research.

[41]  R. Treede,et al.  Median and tibial nerve somatosensory evoked potentials: middle-latency components from the vicinity of the secondary somatosensory cortex in humans. , 1997, Electroencephalography and clinical neurophysiology.

[42]  D. Robinson Electrophysiological analysis of interhemispheric relations in the second somatosensory cortex of the cat , 1973, Experimental Brain Research.

[43]  Bruce T. Volpe Cortical mechanisms involved in praxis: observations following partial and complete section of the corpus callosum in man , 1995 .

[44]  T Manzoni The callosal connections of the hierarchically organized somatosensory areas of primates. , 1997, Journal of neurosurgical sciences.

[45]  U Salvolini,et al.  Localization of the first and second somatosensory areas in the human cerebral cortex with functional MR imaging. , 1999, AJNR. American journal of neuroradiology.

[46]  L Krubitzer,et al.  A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  A. Rubens,et al.  Interhemispheric transfer in patients with incomplete section of the corpus callosum. Anatomic verification with magnetic resonance imaging. , 1989, Archives of neurology.

[48]  R Salmelin,et al.  Comparison of somatosensory evoked fields to airpuff and electric stimuli. , 1994, Electroencephalography and clinical neurophysiology.

[49]  G. Werner,et al.  Symmetry and connectivity in the map of the body surface in somatosensory area II of primates. , 1969, Journal of neurophysiology.

[50]  Veikko Jousmäki,et al.  Sensorimotor integration in human primary and secondary somatosensory cortices , 1998, Brain Research.

[51]  N. Geschwind Disconnexion syndromes in animals and man. II. , 1965, Brain : a journal of neurology.

[52]  J Xiong,et al.  Assessment and optimization of functional MRI analyses , 1996, Human brain mapping.

[53]  C. Robinson,et al.  Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insula of M. fascicularis , 1980, The Journal of comparative neurology.

[54]  M. Moscovitch,et al.  Intermanual information transfer in patients with lesions in the trunk of the corpus callosum , 1984, Neuropsychologia.

[55]  Alan C. Evans,et al.  Distributed processing of pain and vibration by the human brain , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  David P. Friedman,et al.  Representation pattern in the second somatic sensory area of the monkey cerebral cortex , 1980, The Journal of comparative neurology.

[57]  R. Hari,et al.  Functional Organization of the Human First and Second Somatosensory Cortices: a Neuromagnetic Study , 1993, The European journal of neuroscience.

[58]  R. Rauch,et al.  Analysis of cross-sectional area measurements of the corpus callosum adjusted for brain size in male and female subjects from childhood to adulthood , 1994, Behavioural Brain Research.

[59]  N. Geschwind Disconnexion syndromes in animals and man. I. , 1965, Brain : a journal of neurology.

[60]  S. Gandevia The sensation of heaviness after surgical disconnection of the cerebral hemispheres in man. , 1978, Brain : a journal of neurology.

[61]  L A Krubitzer,et al.  The organization and connections of somatosensory cortex in marmosets , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[62]  R König,et al.  Surgical and neurological complications in a series of 708 epilepsy surgery procedures. , 1998, Neurosurgery.

[63]  A. Caramazza,et al.  Haptic processing by the left hemisphere in a split-brain patient , 1997, Neuropsychologia.

[64]  H Hämäläinen,et al.  Human somatosensory evoked potentials to mechanical pulses and vibration: contributions of SI and SII somatosensory cortices to P50 and P100 components. , 1990, Electroencephalography and clinical neurophysiology.

[65]  S. Dimond,et al.  Functions of the centre section (trunk) of the corpus callosum in man. , 1977, Brain : a journal of neurology.

[66]  M S Gazzaniga,et al.  Observations on visual processes after posterior callosal section , 1973, Neurology.

[67]  H S Levin,et al.  Effects of transcallosal surgery on interhemispheric transfer of information. , 1993, Surgical neurology.

[68]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[69]  David P. Friedman,et al.  Physiological evidence for serial processing in somatosensory cortex. , 1987, Science.

[70]  A. Iriki,et al.  Bilateral hand representation in the postcentral somatosensory cortex , 1994, Nature.

[71]  H. Ku¨nzle,et al.  Cortico-cortical efferents of primary motor and somatosensory regions of the cerebral cortex in Macaca fascicularis , 1978, Neuroscience.

[72]  Franco Lepore,et al.  Bilateral interaction in the second somatosensory area (SII) of the cat and contribution of the corpus callosum , 1990, Brain Research.

[73]  Jens Frahm,et al.  High‐resolution functional magnetic resonance imaging of cortical activation during tactile exploration , 1995 .

[74]  G. Ettlinger,et al.  Unilateral removal of the second somatosensory projection cortex in the monkey: evidence for cerebral predominance? , 1982, Brain : a journal of neurology.

[75]  A. Angelucci,et al.  Segregation and overlap of callosal and association neurons in frontal and parietal cortices of primates: a spectral and coherency analysis , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[76]  A R Damasio,et al.  Posterior callosal section in a non-epileptic patient. , 1980, Journal of neurology, neurosurgery, and psychiatry.

[77]  Masahiro Sakamoto,et al.  Functional surface integration, submodality convergence, and tactile feature detection in area 2 of the monkey somatosensory cortex , 1985 .

[78]  P. Roland,et al.  Somatosensory Activations of the Parietal Operculum of Man. A PET Study , 1995, The European journal of neuroscience.

[79]  C. L. Kwan,et al.  Functional MRI study of thalamic and cortical activations evoked by cutaneous heat, cold, and tactile stimuli. , 1998, Journal of neurophysiology.

[80]  G. Ettlinger,et al.  Tactile discrimination performance in the monkey: the effect of commissure section on transfer of training between the hands. , 1973, Cortex; a journal devoted to the study of the nervous system and behavior.

[81]  E. Làdavas,et al.  Emotional Evaluation With and Without Conscious Stimulus Identification: Evidence from a Split-brain Patient , 1993 .

[82]  E. Disbrow,et al.  Somatosensory cortex: A comparison of the response to noxious thermal, mechanical, and electrical stimuli using functional magnetic resonance imaging , 1998, Human brain mapping.

[83]  H Burton,et al.  Multiple foci in parietal and frontal cortex activated by rubbing embossed grating patterns across fingerpads: a positron emission tomography study in humans. , 1997, Cerebral cortex.

[84]  G. Geffen,et al.  The effect of lesions of the corpus callosum on finger localization , 1985, Neuropsychologia.

[85]  W. Penfield,et al.  The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1968 .

[86]  M. Raichle,et al.  Tactile-vibration-activated foci in insular and parietal-opercular cortex studied with positron emission tomography: mapping the second somatosensory area in humans. , 1993, Somatosensory & motor research.