fMRI reveals two distinct cerebral networks subserving speech motor control

Background: There are few data on the cerebral organization of motor aspects of speech production and the pathomechanisms of dysarthric deficits subsequent to brain lesions and diseases. The authors used fMRI to further examine the neural basis of speech motor control. Methods and Results: In eight healthy volunteers, fMRI was performed during syllable repetitions synchronized to click trains (2 to 6 Hz; vs a passive listening task). Bilateral hemodynamic responses emerged at the level of the mesiofrontal and sensorimotor cortex, putamen/pallidum, thalamus, and cerebellum (two distinct activation spots at either side). In contrast, dorsolateral premotor cortex and anterior insula showed left-sided activation. Calculation of rate/response functions revealed a negative linear relationship between repetition frequency and blood oxygen level–dependent (BOLD) signal change within the striatum, whereas both cerebellar hemispheres exhibited a step-wise increase of activation at ∼3 Hz. Analysis of the temporal dynamics of the BOLD effect found the various cortical and subcortical brain regions engaged in speech motor control to be organized into two separate networks (medial and dorsolateral premotor cortex, anterior insula, and superior cerebellum vs sensorimotor cortex, basal ganglia, and inferior cerebellum). Conclusion: These data provide evidence for two levels of speech motor control bound, most presumably, to motor preparation and execution processes. They also help to explain clinical observations such as an unimpaired or even accelerated speaking rate in Parkinson disease and slowed speech tempo, which does not fall below a rate of 3 Hz, in cerebellar disorders.

[1]  D Le Bihan,et al.  Postoperative speech disorder after medial frontal surgery , 2003, Neurology.

[2]  J. Ashburner,et al.  Multimodal Image Coregistration and Partitioning—A Unified Framework , 1997, NeuroImage.

[3]  M. Erb,et al.  Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization , 2001, Human brain mapping.

[4]  Michael Erb,et al.  From will to action: sequential cerebellar contributions to voluntary movement , 2003, NeuroImage.

[5]  R W Cox,et al.  Event‐related fMRI of tasks involving brief motion , 1999, Human brain mapping.

[6]  H Shibasaki,et al.  The functions of the supplementary motor area. Summary of a workshop. , 1996, Advances in neurology.

[7]  W. Ziegler,et al.  Cerebellar voice tremor: an acoustic analysis. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[8]  Gary W Thickbroom,et al.  Dual representation of the hand in the cerebellum: activation with voluntary and passive finger movement , 2003, NeuroImage.

[9]  S. Cobb Speech and Brain-Mechanisms. , 1960 .

[10]  M. Hallett,et al.  Frequency-Dependent Changes of Regional Cerebral Blood Flow during Finger Movements , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[11]  Barry Horwitz,et al.  The elusive concept of brain connectivity , 2003, NeuroImage.

[12]  Donald T. Stuss,et al.  Frontal lobes and language , 1989, Brain and Language.

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

[14]  B. Horwitz,et al.  Correlations between Reaction Time and Cerebral Blood Flow during Motor Preparation , 2000, NeuroImage.

[15]  G. Schlaug,et al.  Cerebral activation covaries with movement rate , 1996, Neuroreport.

[16]  H. Freund,et al.  Motor impairment in Wilson's disease, II: slowness of speech , 1993, Acta neurologica Scandinavica.

[17]  Andrea Mechelli,et al.  A report of the functional connectivity workshop, Dusseldorf 2002 , 2003, NeuroImage.

[18]  R I Kitney,et al.  Investigation of acoustic noise on 15 MRI scanners from 0.2 T to 3 T , 2001, Journal of magnetic resonance imaging : JMRI.

[19]  Karl J. Friston,et al.  Functional Connectivity: The Principal-Component Analysis of Large (PET) Data Sets , 1993, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[20]  Wolfgang Grodd,et al.  Parametric analysis of rate-dependent hemodynamic response functions of cortical and subcortical brain structures during auditorily cued finger tapping: a fMRI study , 2003, NeuroImage.

[21]  Hermann Ackermann,et al.  Acoustic Analysis of Durational Speech Parameters in Neurological Dysarthrias , 1997 .

[22]  John R. Hodges,et al.  Localization and Neuroimaging in Neuropsychology , 1995 .

[23]  Stephen C Strother,et al.  Predicting performance from functional imaging data: methods matter , 2003, NeuroImage.

[24]  M. Botez,et al.  Role of subcortical structures, and particularly of the thalamus, in the mechanisms of speech and language. A review. , 1971, International journal of neurology.

[25]  M. J. Norušis,et al.  SPSS for Windows : professional statistics, release 5 , 1992 .

[26]  R. Passingham,et al.  The effect of movement frequency on cerebral activation: a positron emission tomography study , 1997, Journal of the Neurological Sciences.

[27]  L. Deecke,et al.  The Preparation and Execution of Self-Initiated and Externally-Triggered Movement: A Study of Event-Related fMRI , 2002, NeuroImage.

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

[29]  W Grodd,et al.  Impaired procedural learning after damage to the left supplementary motor area (SMA). , 1996, Journal of neurology, neurosurgery, and psychiatry.

[30]  J. Hufnagle The Speech Sciences , 1998 .

[31]  E. Eldred,et al.  CEREBRO-CEREBELLAR RELATIONSHIPS IN THE MONKEY , 1952 .

[32]  H. Ackermann,et al.  The contribution of the cerebellum to speech processing , 2000, Journal of Neurolinguistics.

[33]  Karl J. Friston,et al.  Characterizing Stimulus–Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments , 1998, NeuroImage.

[34]  Y. Lebrun From the Brain to the Mouth , 1997 .

[35]  H. Freund,et al.  Does tremor pace repetitive voluntary motor behavior in parkinson's disease? , 1991, Annals of neurology.

[36]  E. Eldred,et al.  Cerebrocerebellar relationships in the monkey. , 1952, Journal of neurophysiology.

[37]  R W Cox,et al.  Magnetic field changes in the human brain due to swallowing or speaking , 1998, Magnetic resonance in medicine.

[38]  H. Ackermann,et al.  Acquired dysfluencies following infarction of the left mesiofrontal cortex , 1996 .

[39]  M. Posner,et al.  Attention, self-regulation and consciousness. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  Andrew Kertesz,et al.  Localization and neuroimaging in neuropsychology , 1994 .

[41]  W. Grodd,et al.  Differential Contributions of Motor Cortex, Basal Ganglia, and Cerebellum to Speech Motor Control: Effects of Syllable Repetition Rate Evaluated by fMRI , 2001, NeuroImage.

[42]  Wolfram Ziegler,et al.  Psycholinguistic and Motor Theories of Apraxia of Speech , 2002, Seminars in speech and language.

[43]  H. Lüders Supplementary sensorimotor area , 1996 .

[44]  Raymond D. Kent,et al.  Maximum performance tests of speech production. , 1987, The Journal of speech and hearing disorders.