The dorsal premotor cortex orchestrates concurrent speech and fingertapping movements

Human speech and hand use both involve highly specialized complex movement patterns. Whereas previous studies in detail characterized the cortical motor systems mediating speech and finger movements, the network that provides coordination of concurrent speech and hand movements so far is unknown. Using functional magnetic resonance imaging (fMRI), the present study investigated differential cortical networks devoted to speech or fingertapping, and regions mediating integration of these complex movement patterns involving different effectors. The conjunction contrasts revealing regions activated both during sole fingertapping and sole repetitive articulation or reading aloud showed contralateral regions at the border of ventral and dorsal motor cortex. In contrast, the analyses revealing regions showing a higher level of fMRI activation for concurrent movements of both effectors compared with sole hand movements or repetitive articulation or reading aloud showed distinct premotor activations, which were situated dorsal and caudal to the areas activated across speech and fingertapping tasks. These results indicate that the premotor cortex (PMC) subserves coordination of concurrent speech with hand movements. This integrative motor region is not identical with the area that shows overlapping activations for speech and fingertapping. Thus, concurrent performance of these complex movement patterns involving different effectors requires, in addition to somatotopic motor cortex activation, orchestration subserved by a distinct PMC area.

[1]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[2]  Heidi Johansen-Berg,et al.  Attention to movement modulates activity in sensori-motor areas, including primary motor cortex , 2001, Experimental Brain Research.

[3]  Alex Martin,et al.  Semantic memory and the brain: structure and processes , 2001, Current Opinion in Neurobiology.

[4]  N. Dronkers A new brain region for coordinating speech articulation , 1996, Nature.

[5]  C Büchel,et al.  Brain regions involved in articulation , 1999, The Lancet.

[6]  J. Tanji,et al.  Functional specialization in dorsal and ventral premotor areas. , 2004, Progress in brain research.

[7]  Kevin Murphy,et al.  Speech production: Wernicke, Broca and beyond. , 2002, Brain : a journal of neurology.

[8]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[9]  G. Geffen,et al.  Lateralization of speech production using verbal/manual dual tasks: meta-analysis of sex differences and practice effects , 2002, Neuropsychologia.

[10]  R. Johansson,et al.  How a Lateralized Brain Supports Symmetrical Bimanual Tasks , 2006, PLoS biology.

[11]  R. Töpper,et al.  Motor cortex hand area and speech: implications for the development of language , 2003, Neuropsychologia.

[12]  P. Stoeter,et al.  Left-hemispheric dominance for articulation: a prospective study on acute ischaemic dysarthria at different localizations. , 2006, Brain : a journal of neurology.

[13]  M. Rushworth,et al.  The left parietal and premotor cortices: motor attention and selection , 2003, NeuroImage.

[14]  D. V. Cramon,et al.  Functional–anatomical concepts of human premotor cortex: evidence from fMRI and PET studies , 2003, NeuroImage.

[15]  S. Small,et al.  Functional Lateralization of the Human Premotor Cortex during Sequential Movements , 2002, Brain and Cognition.

[16]  D. Boussaoud Attention versus Intention in the Primate Premotor Cortex , 2001, NeuroImage.

[17]  Takenori Uozumi,et al.  Motor hand representation in cortical area 44 , 2004, Neurology.

[18]  Susan Goldin-Meadow,et al.  Gesture Paves the Way for Language Development , 2005, Psychological science.

[19]  M. Erb,et al.  fMRI Evaluation of Somatotopic Representation in Human Primary Motor Cortex , 2000, NeuroImage.

[20]  M. Erb,et al.  fMRI reveals two distinct cerebral networks subserving speech motor control , 2005, Neurology.

[21]  U. Jürgens Neural pathways underlying vocal control , 2002, Neuroscience & Biobehavioral Reviews.

[22]  J. Rothwell,et al.  Speech‐induced changes in corticospinal excitability , 1996, Annals of neurology.

[23]  L. Cohen,et al.  Transitions between dynamical states of differing stability in the human brain , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Paul B. Johnson,et al.  Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. , 1997, Annual review of neuroscience.

[25]  T. Ebner,et al.  Processing of multiple kinematic signals in the cerebellum and motor cortices , 2000, Brain Research Reviews.

[26]  Torrey M. J. Loucks,et al.  Human brain activation during phonation and exhalation: Common volitional control for two upper airway functions , 2007, NeuroImage.

[27]  Frank H. Guenther,et al.  An fMRI investigation of syllable sequence production , 2006, NeuroImage.

[28]  S. Goldin-Meadow,et al.  Why people gesture when they speak , 1998, Nature.

[29]  Christopher Dromey,et al.  Effects of concurrent motor, linguistic, or cognitive tasks on speech motor performance. , 2003, Journal of speech, language, and hearing research : JSLHR.

[30]  S G Kim,et al.  Functional activation in motor cortex reflects the direction and the degree of handedness. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[31]  R J Wise,et al.  Cerebral areas associated with motor control of speech in humans. , 1997, Journal of applied physiology.

[32]  Armin Thron,et al.  Effects of long‐term practice and task complexity in musicians and nonmusicians performing simple and complex motor tasks: Implications for cortical motor organization , 2005, Human brain mapping.

[33]  D Yves von Cramon,et al.  “What” Becoming “Where”: Functional Magnetic Resonance Imaging Evidence for Pragmatic Relevance Driving Premotor Cortex , 2004, The Journal of Neuroscience.

[34]  Richard S. J. Frackowiak,et al.  Multiple nonprimary motor areas in the human cortex. , 1997, Journal of neurophysiology.

[35]  A. P. Georgopoulos,et al.  Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. , 1993, Science.

[36]  Daniel M. Corcos,et al.  Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: A meta-analysis , 2006, NeuroImage.