Examination of the development and aging of brain deactivation using a unimanual motor task

In the central nervous system, regional neuronal inhibition plays important roles in functional segregation. Here, we showed how brain deactivation, which is a putative index of neuronal inhibition, develops and ages using a unimanual motor task. Healthy right-handed children (8–11 years), adolescents (12–15 years), young adults (20–24 years), and older adults (69–75 years; 21 participants in each group) underwent functional magnetic resonance imaging with their eyes closed while they performed 1-Hz alternating extension–flexion of the right wrist. In young adults, we found deactivations in the hand/arm section of the ipsilateral primary sensorimotor cortices (SM1) including the dorsal premotor cortex (interhemispheric inhibition), foot and face SM1 sections (cross-somatotopic inhibition), visual and auditory cortices (cross-modal inhibition), and precuneus and medial prefrontal cortex of the default mode network (DMN; DMN inhibition). Interhemispheric, cross-modal, and DMN inhibitions developed from childhood to adulthood, but cross-somatotopic inhibition showed no developmental changes. Conversely, interhemispheric, cross-somatotopic, and cross-modal inhibitions, but not DMN inhibition, decreased with aging. Thus, neuronal inhibition generally progresses with development and deteriorates with aging, with some noted regional differences. This was the first study to systematically describe the development and aging of brain deactivation, which may reflect regional neuronal inhibition. GRAPHICAL ABSTRACT

[1]  N. Logothetis,et al.  Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1 , 2006, Nature Neuroscience.

[2]  Masaya Hirashima,et al.  Selective activation and deactivation of the human brain structures between speeded and precisely timed tapping responses to identical visual stimulus: an fMRI study , 2004, NeuroImage.

[3]  S. M. Daselaar,et al.  When less means more: deactivations during encoding that predict subsequent memory , 2004, NeuroImage.

[4]  D. Johnston,et al.  Negative Blood Oxygen Level Dependence in the Rat:A Model for Investigating the Role of Suppression in Neurovascular Coupling , 2010, The Journal of Neuroscience.

[5]  M. D’Esposito,et al.  The Inferential Impact of Global Signal Covariates in Functional Neuroimaging Analyses , 1998, NeuroImage.

[6]  Jeffrey R. Binder,et al.  Interrupting the “stream of consciousness”: An fMRI investigation , 2006, NeuroImage.

[7]  T. Flash,et al.  Negative blood oxygenation level dependent homunculus and somatotopic information in primary motor cortex and supplementary motor area , 2012, Proceedings of the National Academy of Sciences.

[8]  Alex R. Wade,et al.  Early Suppressive Mechanisms and the Negative Blood Oxygenation Level-Dependent Response in Human Visual Cortex , 2010, The Journal of Neuroscience.

[9]  Deanna M. Barch,et al.  When less is more: TPJ and default network deactivation during encoding predicts working memory performance , 2010, NeuroImage.

[10]  K. D. Singh,et al.  Negative BOLD in the visual cortex: Evidence against blood stealing , 2004, Human brain mapping.

[11]  Jutta S. Mayer,et al.  Specialization in the default mode: Task‐induced brain deactivations dissociate between visual working memory and attention , 2009, Human brain mapping.

[12]  J C Rothwell,et al.  Neural correlates of age-related changes in cortical neurophysiology , 2008, NeuroImage.

[13]  M. Asada,et al.  Local-to-distant development of the cerebrocerebellar sensorimotor network in the typically developing human brain: a functional and diffusion MRI study , 2019, Brain Structure and Function.

[14]  S. Sten,et al.  Neural inhibition can explain negative BOLD responses: A mechanistic modelling and fMRI study , 2017, NeuroImage.

[15]  Richard S. Frackowiak,et al.  Aging is associated with contrasting changes in local and distant cortical connectivity in the human motor system , 2006, NeuroImage.

[16]  Charles Capaday,et al.  Neural mechanisms involved in the functional linking of motor cortical points , 2002, Experimental Brain Research.

[17]  Alvaro Pascual-Leone,et al.  Ipsilateral motor cortex activation on functional magnetic resonance imaging during unilateral hand movements is related to interhemispheric interactions , 2003, NeuroImage.

[18]  G. Geffen,et al.  Interhemispheric control of manual motor activity , 1994, Behavioural Brain Research.

[19]  Mauro DiNuzzo,et al.  On the origin of sustained negative BOLD response. , 2012, Journal of neurophysiology.

[20]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[21]  Alberto Bacci,et al.  Assortment of GABAergic Plasticity in the Cortical Interneuron Melting Pot , 2011, Neural plasticity.

[22]  Karl J. Friston,et al.  Generalisability, Random Effects & Population Inference , 1998, NeuroImage.

[23]  Abraham Z. Snyder,et al.  A default mode of brain function: A brief history of an evolving idea , 2007, NeuroImage.

[24]  T. Davidson,et al.  Age and hemispheric differences in transcallosal inhibition between motor cortices: an ispsilateral silent period study , 2013, BMC Neuroscience.

[25]  Alan C. Evans,et al.  An MRI-Based Probabilistic Atlas of Neuroanatomy , 1994 .

[26]  Stephen D. Mayhew,et al.  Evidence that the negative BOLD response is neuronal in origin: A simultaneous EEG–BOLD–CBF study in humans , 2014, NeuroImage.

[27]  J. Morris,et al.  Functional deactivations: Change with age and dementia of the Alzheimer type , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[28]  B. Day,et al.  Interhemispheric inhibition of the human motor cortex. , 1992, The Journal of physiology.

[29]  R. Malach,et al.  Negative BOLD Differentiates Visual Imagery and Perception , 2005, Neuron.

[30]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[31]  M. Asada,et al.  Developmental Changes in Task‐Induced Brain Deactivation in Humans Revealed by a Motor Task , 2019, Developmental neurobiology.

[32]  Cody Jensen,et al.  Motor deactivation in the human cortex and basal ganglia , 2007, NeuroImage.

[33]  Michael D. Greicius,et al.  Distinct Cerebellar Contributions to Intrinsic Connectivity Networks , 2009, NeuroImage.

[34]  G. Curio,et al.  Imperceptible Stimuli and Sensory Processing Impediment , 2003, Science.

[35]  Y. Yen,et al.  Deactivation of Sensory-Specific Cortex by Cross-Modal Stimuli , 2002, Journal of Cognitive Neuroscience.

[36]  S. Ogawa,et al.  Biophysical and Physiological Origins of Blood Oxygenation Level-Dependent fMRI Signals , 2012, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[37]  John D. E. Gabrieli,et al.  Development of deactivation of the default-mode network during episodic memory formation , 2013, NeuroImage.

[38]  P. Matthews,et al.  Functional MRI cerebral activation and deactivation during finger movement , 2000, Neurology.

[39]  A. Shmuel,et al.  Sustained Negative BOLD, Blood Flow and Oxygen Consumption Response and Its Coupling to the Positive Response in the Human Brain , 2002, Neuron.

[40]  Amir Amedi,et al.  Combined activation and deactivation of visual cortex during tactile sensory processing. , 2007, Journal of neurophysiology.

[41]  Michael Alexander,et al.  Age-Related Differences in Movement Representation , 2002, NeuroImage.

[42]  Jeffrey R. Binder,et al.  Task-induced deactivation and the "resting" state , 2012, NeuroImage.

[43]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[44]  M. N. Rajah,et al.  Maintenance, reserve and compensation: the cognitive neuroscience of healthy ageing , 2018, Nature Reviews Neuroscience.

[45]  Srikantan S. Nagarajan,et al.  Motor-induced Suppression of the Auditory Cortex , 2009, Journal of Cognitive Neuroscience.

[46]  M. Larkum,et al.  The Cellular Basis of GABAB-Mediated Interhemispheric Inhibition , 2012, Science.

[47]  E. DeYoe,et al.  A comparison of visual and auditory motion processing in human cerebral cortex. , 2000, Cerebral cortex.

[48]  KM Jacobs,et al.  Reshaping the cortical motor map by unmasking latent intracortical connections , 1991, Science.

[49]  Jörn Diedrichsen,et al.  Functional boundaries in the human cerebellum revealed by a multi-domain task battery , 2019, Nature Neuroscience.

[50]  M. Lotze,et al.  Non-effective increase of fMRI-activation for motor performance in elder individuals , 2011, Behavioural Brain Research.

[51]  Alan Sunderland,et al.  fMRI signal decreases in ipsilateral primary motor cortex during unilateral hand movements are related to duration and side of movement , 2005, NeuroImage.

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

[53]  Michael W. Cole,et al.  The role of default network deactivation in cognition and disease , 2012, Trends in Cognitive Sciences.

[54]  K. Meador,et al.  Functional MRI cerebral activation and deactivation during finger movement , 2000, Neurology.

[55]  R. Gruetter,et al.  Mapping and characterization of positive and negative BOLD responses to visual stimulation in multiple brain regions at 7T , 2018, Human brain mapping.

[56]  L. Jäncke,et al.  Cortical activations during paced finger-tapping applying visual and auditory pacing stimuli. , 2000, Brain research. Cognitive brain research.

[57]  Otto W. Witte,et al.  Functional significance of age-related differences in motor activation patterns , 2006, NeuroImage.

[58]  N. Ward,et al.  Age-dependent changes in the neural correlates of force modulation: An fMRI study , 2008, Neurobiology of Aging.

[59]  J. Binder,et al.  A Parametric Manipulation of Factors Affecting Task-induced Deactivation in Functional Neuroimaging , 2003, Journal of Cognitive Neuroscience.

[60]  E. Darcy Burgund,et al.  Comparison of functional activation foci in children and adults using a common stereotactic space , 2003, NeuroImage.

[61]  Brian N. Pasley,et al.  Analysis of oxygen metabolism implies a neural origin for the negative BOLD response in human visual cortex , 2007, NeuroImage.

[62]  B. Mazoyer,et al.  Cortical networks for working memory and executive functions sustain the conscious resting state in man , 2001, Brain Research Bulletin.

[63]  S. Stone-Elander,et al.  Coexistence of Attention-Based Facilitation and Inhibition in the Human Cortex , 1998, NeuroImage.

[64]  Tatsuya Asai,et al.  Hemispheric Asymmetry of Frequency-Dependent Suppression in the Ipsilateral Primary Motor Cortex During Finger Movement: A Functional Magnetic Resonance Imaging Study , 2008, Cerebral cortex.

[65]  K. Sakamoto,et al.  Negative BOLD responses during hand and foot movements: An fMRI study , 2019, PloS one.

[66]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[67]  M. Asada,et al.  Importance of the Primary Motor Cortex in Development of Human Hand/Finger Dexterity , 2020, Cerebral cortex communications.

[68]  Jonathan D. Power,et al.  Statistical improvements in functional magnetic resonance imaging analyses produced by censoring high‐motion data points , 2014, Human brain mapping.

[69]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[70]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

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

[72]  Xiaoping Hu,et al.  Short-term visual deprivation alters neural processing of tactile form , 2005, Experimental Brain Research.