Discrete functional contributions of cerebral cortical foci in voluntary swallowing: a functional magnetic resonance imaging (fMRI) “Go, No-Go” study

Brain-imaging studies have shown that visually-cued, voluntary swallowing activates a distributed network of cortical regions including the precentral and postcentral gyri, anterior cingulate cortex (ACC), insula, frontoparietal operculum, cuneus and precuneus. To elucidate the functional contributions of these discrete activation foci for swallowing, a “Go, No-Go” functional magnetic resonance imaging (fMRI) paradigm was designed. Brain activation associated with visually-cued swallowing was compared with brain activation evoked by a comparable visual cue instructing the subject not to swallow. Region-of-interest analyses performed on data from eight healthy subjects showed a significantly greater number of activated voxels within the precentral gyrus, postcentral gyrus, and ACC during the “Go” condition compared to the “No-Go” condition. This finding suggests that the precentral gyrus, postcentral gyrus, and ACC contribute primarily to the act of swallowing. In contrast, the numbers of activated voxels within the cuneus and precuneus were not significantly different for the “Go” and “No-Go” conditions, suggesting that these regions mediate processing of the cue to swallow. Together these findings support the view that the discrete cortical foci previously implicated in swallowing mediate functionally distinct components of the swallowing act.

[1]  P J Kahrilas,et al.  Closure mechanisms of laryngeal vestibule during swallow. , 1992, The American journal of physiology.

[2]  G. M. Murray,et al.  Effects on non-human primate mastication of reversible inactivation by cooling of the face primary somatosensory cortex. , 1998, Archives of Oral Biology.

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

[4]  Yuji Masuda,et al.  Effects of reversible bilateral inactivation of face primary motor cortex on mastication and swallowing , 2002, Brain Research.

[5]  B. Sessle,et al.  Effects on mastication of reversible bilateral inactivation of the lateral pericentral cortex in the monkey (Macaca fascicularis). , 2002, Archives of oral biology.

[6]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[7]  Arno Villringer,et al.  Visual Feature and Conjunction Searches of Equal Difficulty Engage Only Partially Overlapping Frontoparietal Networks , 2002, NeuroImage.

[8]  J C Rothwell,et al.  Identification of the cerebral loci processing human swallowing with H2(15)O PET activation. , 1999, Journal of neurophysiology.

[9]  Karl J. Friston,et al.  Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  Yoshikazu Isomura,et al.  Neural Coding of “Attention for Action” and “Response Selection” in Primate Anterior Cingulate Cortex , 2003, The Journal of Neuroscience.

[11]  A Jesmanowicz,et al.  Swallow-related cerebral cortical activity maps are not specific to deglutition. , 2001, American journal of physiology. Gastrointestinal and liver physiology.

[12]  S. Baredes,et al.  Cortical Representation of Swallowing in Normal Adults: Functional Implications , 1999, The Laryngoscope.

[13]  Alan C. Evans,et al.  In vivo morphometry of the intrasulcal gray matter in the human cingulate, paracingulate, and superior‐rostral sulci: Hemispheric asymmetries, gender differences and probability maps , 1996, The Journal of comparative neurology.

[14]  G. M. Murray,et al.  Neuronal activity patterns in primate primary motor cortex related to trained or semiautomatic jaw and tongue movements. , 2002, Journal of neurophysiology.

[15]  M. Hallett,et al.  Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. , 1999, Journal of neurophysiology.

[16]  Ravi S. Menon Postacquisition suppression of large‐vessel BOLD signals in high‐resolution fMRI , 2002, Magnetic resonance in medicine.

[17]  Ravi S. Menon,et al.  A transmit‐only/receive‐only (TORO) RF system for high‐field MRI/MRS applications , 2000, Magnetic resonance in medicine.

[18]  M. Inase,et al.  Two movement-related foci in the primate cingulate cortex observed in signal-triggered and self-paced forelimb movements. , 1991, Journal of neurophysiology.

[19]  Mark S. Cohen,et al.  Parametric Analysis of fMRI Data Using Linear Systems Methods , 1997, NeuroImage.

[20]  X. Hu,et al.  Reduction of signal fluctuation in functional MRI using navigator echoes , 1994, Magnetic resonance in medicine.

[21]  K. Kiehl,et al.  Event‐related fMRI study of response inhibition , 2001, Human brain mapping.

[22]  R. Passingham,et al.  Functional anatomy of the mental representation of upper extremity movements in healthy subjects. , 1995, Journal of neurophysiology.

[23]  N. Diamant,et al.  Coordination of respiration and swallowing: effect of bolus volume in normal adults. , 1992, The American journal of physiology.

[24]  L. Optican,et al.  Cortical regions involved in visual texture perception: a fMRI study. , 1998, Brain research. Cognitive brain research.

[25]  Ravi S. Menon,et al.  Cerebral areas processing swallowing and tongue movement are overlapping but distinct: a functional magnetic resonance imaging study. , 2004, Journal of neurophysiology.

[26]  D. Brooks,et al.  Motor sequence learning: a study with positron emission tomography , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[28]  R Shaker,et al.  Cerebral cortical representation of reflexive and volitional swallowing in humans. , 2001, American journal of physiology. Gastrointestinal and liver physiology.

[29]  T. Paus Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[30]  W. Press,et al.  Numerical Recipes in C++: The Art of Scientific Computing (2nd edn)1 Numerical Recipes Example Book (C++) (2nd edn)2 Numerical Recipes Multi-Language Code CD ROM with LINUX or UNIX Single-Screen License Revised Version3 , 2003 .

[31]  Gregory V. Simpson,et al.  Evidence for Anterior Cingulate Cortex Involvement in Monitoring Preparatory Attentional Set , 2002, NeuroImage.

[32]  A. Crawley,et al.  Cortical activation during human volitional swallowing: an event-related fMRI study. , 1999, American journal of physiology. Gastrointestinal and liver physiology.

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

[34]  G. M. Murray,et al.  Functional properties of neurons in the primate tongue primary motor cortex during swallowing. , 1997, Journal of neurophysiology.

[35]  Hiroshi Fukuda,et al.  The human prefrontal and parietal association cortices are involved in NO-GO performances—an event-related fMRI study , 2000, NeuroImage.

[36]  Y. Lamarre,et al.  Activity of neurons in the lower precentral cortex during voluntary and rhythmical jaw movements in the monkey , 1974, Experimental Brain Research.

[37]  G. M. Murray,et al.  Features of cortically evoked swallowing in the awake primate (Macaca fascicularis). , 1999, Journal of neurophysiology.

[38]  J. Pardo,et al.  The functional neuroanatomy of voluntary swallowing , 1999, Annals of neurology.

[39]  K. Mosier,et al.  Parallel cortical networks for volitional control of swallowing in humans , 2001, Experimental Brain Research.

[40]  M. Hallett,et al.  The functional neuroanatomy of simple and complex sequential finger movements: a PET study. , 1998, Brain : a journal of neurology.

[41]  Ravi S. Menon,et al.  Cerebral cortical representation of automatic and volitional swallowing in humans. , 2001, Journal of neurophysiology.

[42]  J. Downar,et al.  A multimodal cortical network for the detection of changes in the sensory environment , 2000, Nature Neuroscience.

[43]  G. M. Murray,et al.  Topographical distribution and functional properties of cortically induced rhythmical jaw movements in the monkey (Macaca fascicularis). , 1989, Journal of neurophysiology.

[44]  J. Rosenbek,et al.  Swallowing after unilateral stroke of the cerebral cortex. , 1993, Archives of physical medicine and rehabilitation.

[45]  Y. Miyashita,et al.  No‐go dominant brain activity in human inferior prefrontal cortex revealed by functional magnetic resonance imaging , 1998, The European journal of neuroscience.