Within-limb somatotopic organization in human SI and parietal operculum for the leg: An fMRI study

Somatotopic organizations in human somatosensory cortex (SI and SII) for scattered portions of the leg have not been systematically observed with functional magnetic resonance imaging (fMRI). In this research we compared functional representations in the contralateral SI and bilateral parietal operculum (that contained subregions OP1, 3-4 of SII and OP2) of four acupoints in right leg in proximal-distal and medial-lateral arrangement. The results were: (1) somatotopy of SI demonstrated a lateral-to-medial and inferior-to-superior pattern when acupoints were shifting from proximal to distal or from medial to lateral; (2) the contralateral OP1 also showed a clear somatotopic organization for the four separated leg portions, and the ipsilateral OP1 showed a similar pattern to the contralateral OP1, thus arrangements of responses in the two areas were mirror-symmetric against y-axis; (3) the contralateral OP2 showed a somatotopic organization when acupoints shifting from proximal to distal, while the contralateral OP3 presented a trend of somatotopy opposite to that of the contralateral OP1. These results first show definite within-leg somatotopy of human SI for scattered leg portions in medial-lateral arrangement using fMRI. Within-limb somatotopic organization of OP1 for leg portions arranging from proximal to distal as well as from medial to lateral, and somatotopy of OP2 for leg portions arranging from proximal to distal, are also shown for the first time. Our results also reinforce the proposal of a somatotopic map existing in human OP3, and indicating a fourth somatotopic map in OP2 in human parietal operculum, which suggests that OP 2 is not just a vestibular area. In addition, separable activations in somatosensory cortex induced by adjacent acupoints should play a fundamental role in acupoint-specific effects in the brain.

[1]  A. Schleicher,et al.  The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions. , 2006, Cerebral cortex.

[2]  Claudio Babiloni,et al.  Functional topography of the secondary somatosensory cortex for nonpainful and painful stimulation of median and tibial nerve: an fMRI study , 2004, NeuroImage.

[3]  Claudio Babiloni,et al.  Human secondary somatosensory cortex is involved in the processing of somatosensory rare stimuli: An fMRI study , 2008, NeuroImage.

[4]  J. Kaas,et al.  What, if anything, is SI? Organization of first somatosensory area of cortex. , 1983, Physiological reviews.

[5]  Paolo Maria Rossini,et al.  Topographic Organization of the Human Primary and Secondary Somatosensory Cortices: Comparison of fMRI and MEG Findings , 2002, NeuroImage.

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

[7]  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.

[8]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[9]  A. Turman,et al.  PARALLEL ORGANIZATION OF SOMATOSENSORY CORTICAL AREAS I AND II FOR TACTILE PROCESSING , 1996, Clinical and experimental pharmacology & physiology.

[10]  Bernd J. Krause,et al.  Variability of BOLD response evoked by foot vibrotactile stimulation: Influence of vibration amplitude and stimulus waveform , 2008, NeuroImage.

[11]  K. Amunts,et al.  The human parietal operculum. II. Stereotaxic maps and correlation with functional imaging results. , 2006, Cerebral cortex.

[12]  Anders Björkman,et al.  Optimizing the mapping of finger areas in primary somatosensory cortex using functional MRI. , 2008, Magnetic resonance imaging.

[13]  A. Villringer,et al.  Preserved responsiveness of secondary somatosensory cortex in patients with thalamic stroke. , 2006, Cerebral cortex.

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

[15]  F Mauguière,et al.  Somatosensory and pain responses to stimulation of the second somatosensory area (SII) in humans. A comparison with SI and insular responses. , 2006, Cerebral cortex.

[16]  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.

[17]  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.

[18]  David C Lyon,et al.  Cortical and thalamic connections of the parietal ventral somatosensory area in marmoset monkeys (Callithrix jacchus) , 2002, The Journal of comparative neurology.

[19]  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.

[20]  W.J.R. Dunseath,et al.  fMRI of the Responses to Vibratory Stimulation of Digit Tips , 2000, NeuroImage.

[21]  K Zilles,et al.  Functional lateralization of face, hand, and trunk representation in anatomically defined human somatosensory areas. , 2008, Cerebral cortex.

[22]  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.

[23]  Gereon R Fink,et al.  The somatotopic organization of cytoarchitectonic areas on the human parietal operculum. , 2007, Cerebral cortex.

[24]  Simon B. Eickhoff,et al.  Assignment of functional activations to probabilistic cytoarchitectonic areas revisited , 2007, NeuroImage.

[25]  Srikantan S Nagarajan,et al.  Sensorimotor integration in S2, PV, and parietal rostroventral areas of the human sylvian fissure. , 2007, Journal of neurophysiology.

[26]  H. Burton,et al.  Second somatic sensory area in the cerebral cortex of cats: Somatotopic organization and cytoarchitecture , 1982, The Journal of comparative neurology.

[27]  Leah Krubitzer,et al.  Cortical connections of the second somatosensory area and the parietal ventral area in macaque monkeys , 2003, The Journal of comparative neurology.

[28]  Francis McGlone,et al.  Functional neuroimaging studies of human somatosensory cortex , 2002, Behavioural Brain Research.

[29]  L. Krubitzer,et al.  Evidence for interhemispheric processing of inputs from the hands in human S2 and PV. , 2001, Journal of neurophysiology.

[30]  Dora E Angelaki,et al.  Macaque Parieto-Insular Vestibular Cortex: Responses to Self-Motion and Optic Flow , 2010, Journal of Neuroscience.

[31]  A Villringer,et al.  Somatotopic organization of human secondary somatosensory cortex. , 2001, Cerebral cortex.

[32]  David M Rector,et al.  Hemispheric mapping of secondary somatosensory cortex in the rat. , 2007, Journal of neurophysiology.

[33]  Volkmar Glauche,et al.  Somatotopic organization of human somatosensory cortices for pain: a single trial fMRI study , 2004, NeuroImage.

[34]  Riitta Hari,et al.  Improved differentiation of tactile activations in human secondary somatosensory cortex and thalamus using cardiac-triggered fMRI , 2006, Experimental Brain Research.

[35]  Jun-Ming Zhang,et al.  Human acupuncture points mapped in rats are associated with excitable muscle/skin–nerve complexes with enriched nerve endings , 2004, Brain Research.

[36]  N. Costes,et al.  Haemodynamic brain responses to acute pain in humans: sensory and attentional networks. , 1999, Brain : a journal of neurology.

[37]  Jan Ruben,et al.  Evidence for a rostral-to-caudal somatotopic organization in human primary somatosensory cortex with mirror-reversal in areas 3b and 1. , 2003, Cerebral cortex.

[38]  Tony Ro,et al.  Human MST But Not MT Responds to Tactile Stimulation , 2007, The Journal of Neuroscience.

[39]  H. Jasper,et al.  Epilepsy and the functional anatomy of the human brain , 1985 .

[40]  Simon B. Eickhoff,et al.  Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps , 2006, NeuroImage.

[41]  Karl J. Friston,et al.  Classical and Bayesian Inference in Neuroimaging: Theory , 2002, NeuroImage.

[42]  K. Amunts,et al.  Identifying human parieto‐insular vestibular cortex using fMRI and cytoarchitectonic mapping , 2006, Human brain mapping.

[43]  D J Felleman,et al.  Somatotopic organization of the lateral sulcus of owl monkeys: Area 3b, s‐II, and a ventral somatosensory area , 1989, The Journal of comparative neurology.

[44]  Harold Burton,et al.  Multiple parietal operculum subdivisions in humans: Tactile activation maps , 2008, Somatosensory & motor research.

[45]  Masahiro Umeda,et al.  Somatotopic representation of acupoints in human primary somatosensory cortex: an FMRI study. , 2005, Magnetic resonance in medical sciences : MRMS : an official journal of Japan Society of Magnetic Resonance in Medicine.

[46]  A. Schleicher,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 1. Microstructural Organization and Interindividual Variability , 1999, NeuroImage.

[47]  Jon H Kaas,et al.  The organization of sensory cortex , 2001, Current Opinion in Neurobiology.

[48]  H Burton,et al.  Attending to and Remembering Tactile Stimuli: A Review of Brain Imaging Data and Single-Neuron Responses , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[49]  L. Krubitzer,et al.  Somatotopic organization of cortical fields in the lateral sulcus of Homo sapiens: Evidence for SII and PV , 2000, The Journal of comparative neurology.