Multimodal assessment of cortical activation during apple peeling by NIRS and fMRI

An intriguing application of neuroimaging is directly measuring actual human brain activities during daily living. To this end, we investigated cortical activation patterns during apple peeling. We first conducted a pilot study to assess the activation pattern of the whole lateral cortical surface during apple peeling by multichannel near-infrared spectroscopy (NIRS) and detected substantial activation in the prefrontal region in addition to expected activations extending over the motor, premotor and supplementary motor areas. We next examined cortical activation during mock apple peeling by simultaneous measurement using multichannel NIRS and functional magnetic resonance imaging (fMRI) in four subjects. We detected activations extending over the motor, premotor and supplementary motor areas, but not in the prefrontal cortex. Thus, we finally focused on the prefrontal cortex and examined its activation during apple peeling in 12 subjects using a multichannel NIRS. We subsequently found that regional concentrations of oxygenated hemoglobin significantly increased in the measured region, which encompassed portions of the dorsolateral, ventrolateral and frontopolar areas of the prefrontal cortex. The current study demonstrated that apple peeling as practiced in daily life recruited the prefrontal cortex but that such activation might not be detected for less laborious mock apple peeling that can be performed in an fMRI environment. We suggest the importance of cortical study of an everyday task as it is but not as a simplified form; we also suggest the validity of NIRS for this purpose. Studies on everyday tasks may serve as stepping stone toward understanding human activities in terms of cortical activations.

[1]  Richard Coppola,et al.  Regional cerebral blood flow during the wisconsin card sorting test in normal subjects studied by xenon-133 dynamic SPECT: Comparison of absolute values, percent distribution values and covariance analysis , 1993, Psychiatry Research: Neuroimaging.

[2]  R. J. Seitz,et al.  Conscious and Subconscious Sensorimotor Synchronization—Prefrontal Cortex and the Influence of Awareness , 2002, NeuroImage.

[3]  Richard Coppola,et al.  Physiological activation of a cortical network during performance of the Wisconsin Card Sorting Test: A positron emission tomography study , 1995, Neuropsychologia.

[4]  P. Roland,et al.  Regional cerebral blood flow changes in cortex and basal ganglia during voluntary movements in normal human volunteers. , 1982, Journal of neurophysiology.

[5]  E. Watanabe,et al.  Spatial and temporal analysis of human motor activity using noninvasive NIR topography. , 1995, Medical physics.

[6]  A. Kleinschmidt,et al.  Noninvasive Functional Imaging of Human Brain Using Light , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[7]  Takashi Kusaka,et al.  Functional imaging of the brain in sedated newborn infants using near infrared topography during passive knee movement , 2001, Neuroscience Letters.

[8]  E. Watanabe,et al.  Non-invasive functional mapping with multi-channel near infra-red spectroscopic topography in humans , 1996, Neuroscience Letters.

[9]  D. Delpy,et al.  Performance comparison of several published tissue near-infrared spectroscopy algorithms. , 1995, Analytical biochemistry.

[10]  E. Zarahn,et al.  The Role of Prefrontal Cortex in Sensory Memory and Motor Preparation: An Event-Related fMRI Study , 2000, NeuroImage.

[11]  Haruka Dan,et al.  EFFECTS OF TEXTURAL CHANGES IN COOKED APPLES ON THE HUMAN BITE, AND INSTRUMENTAL TESTS , 2003 .

[12]  K. Kubota,et al.  Cortical Mapping of Gait in Humans: A Near-Infrared Spectroscopic Topography Study , 2001, NeuroImage.

[13]  Dae-Shik Kim,et al.  Spatiotemporal dynamics of the BOLD fMRI signals: Toward mapping submillimeter cortical columns using the early negative response , 2000, Magnetic resonance in medicine.

[14]  E. Mohr,et al.  Neuropsychological Assessment. Third Edition , 1996 .

[15]  A. Maki,et al.  Activation of the visual cortex imaged by 24-channel near-infrared spectroscopy. , 2000, Journal of biomedical optics.

[16]  E. Gratton,et al.  Study of local cerebral hemodynamics by frequency-domain near-infrared spectroscopy and correlation with simultaneously acquired functional magnetic resonance imaging. , 2001, Optics express.

[17]  M. Land,et al.  The Roles of Vision and Eye Movements in the Control of Activities of Daily Living , 1998, Perception.

[18]  M. Ferrari,et al.  Human motor-cortex oxygenation changes induced by cyclic coupled movements of hand and foot , 1999, Experimental Brain Research.

[19]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[20]  A. Toga,et al.  Temporal spatial differences observed by functional MRI and human intraoperative optical imaging , 2001, NeuroImage.

[21]  A. Kleinschmidt,et al.  Simultaneous Recording of Cerebral Blood Oxygenation Changes during Human Brain Activation by Magnetic Resonance Imaging and Near-Infrared Spectroscopy , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[22]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. I. Frontal cortex and attention to action. , 1997, Journal of neurophysiology.

[23]  M. Schweiger,et al.  Theoretical and experimental investigation of near-infrared light propagation in a model of the adult head. , 1997, Applied optics.

[24]  A. Villringer,et al.  Cerebral oxygenation changes in response to motor stimulation. , 1996, Journal of applied physiology.

[25]  R. Passingham Attention to action. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[26]  E. Gratton,et al.  Investigation of human brain hemodynamics by simultaneous near-infrared spectroscopy and functional magnetic resonance imaging. , 2001, Medical physics.

[27]  David A. Boas,et al.  A Quantitative Comparison of Simultaneous BOLD fMRI and NIRS Recordings during Functional Brain Activation , 2002, NeuroImage.

[28]  A Villringer,et al.  Coupling of brain activity and cerebral blood flow: basis of functional neuroimaging. , 1995, Cerebrovascular and brain metabolism reviews.

[29]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[30]  J. Cummings,et al.  Executive control function: a review of its promise and challenges for clinical research. A report from the Committee on Research of the American Neuropsychiatric Association. , 2002, The Journal of neuropsychiatry and clinical neurosciences.

[31]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[33]  J. Binder,et al.  Functional magnetic resonance imaging of complex human movements , 1993, Neurology.

[34]  B. Manly Randomization, Bootstrap and Monte Carlo Methods in Biology , 2018 .

[35]  D. Delpy,et al.  Methods of quantitating cerebral near infrared spectroscopy data. , 1988, Advances in experimental medicine and biology.

[36]  D. A. Grant,et al.  A behavioral analysis of degree of reinforcement and ease of shifting to new responses in a Weigl-type card-sorting problem. , 1948, Journal of experimental psychology.

[37]  Mary M Hayhoe,et al.  Visual memory and motor planning in a natural task. , 2003, Journal of vision.

[38]  H. Flor,et al.  Non-invasive functional mapping of the human motor cortex using near-infrared spectroscopy. , 1996, Neuroreport.

[39]  M. Lezak Neuropsychological assessment, 3rd ed. , 1995 .

[40]  Y Hoshi,et al.  Visuospatial imagery is a fruitful strategy for the digit span backward task: a study with near-infrared optical tomography. , 2000, Brain research. Cognitive brain research.

[41]  J. Pelz,et al.  Oculomotor behavior and perceptual strategies in complex tasks , 2001, Vision Research.

[42]  E D Richardson,et al.  Assessment of frontal lobe functions. , 1994, The Journal of neuropsychiatry and clinical neurosciences.

[43]  K. Sakai,et al.  Lateralized activation in the inferior frontal cortex during syntactic processing: Event‐related optical topography study , 2002, Human brain mapping.

[44]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[45]  M. Tamura,et al.  Interpretation of near-infrared spectroscopy signals: a study with a newly developed perfused rat brain model. , 2001, Journal of applied physiology.

[46]  J. Mandeville,et al.  The Accuracy of Near Infrared Spectroscopy and Imaging during Focal Changes in Cerebral Hemodynamics , 2001, NeuroImage.

[47]  S. Arridge,et al.  Experimentally measured optical pathlengths for the adult head, calf and forearm and the head of the newborn infant as a function of inter optode spacing. , 1992, Advances in experimental medicine and biology.

[48]  Masako Okamoto,et al.  Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping , 2004, NeuroImage.

[49]  A. Villringer,et al.  Non-invasive optical spectroscopy and imaging of human brain function , 1997, Trends in Neurosciences.

[50]  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.