When Breathing Interferes with Cognition: Experimental Inspiratory Loading Alters Timed Up-and-Go Test in Normal Humans

Human breathing stems from automatic brainstem neural processes. It can also be operated by cortico-subcortical networks, especially when breathing becomes uncomfortable because of external or internal inspiratory loads. How the “irruption of breathing into consciousness” interacts with cognition remains unclear, but a case report in a patient with defective automatic breathing (Ondine's curse syndrome) has shown that there was a cognitive cost of breathing when the respiratory cortical networks were engaged. In a pilot study of putative breathing-cognition interactions, the present study relied on a randomized design to test the hypothesis that experimentally loaded breathing in 28 young healthy subjects would have a negative impact on cognition as tested by “timed up-and-go” test (TUG) and its imagery version (iTUG). Progressive inspiratory threshold loading resulted in slower TUG and iTUG performance. Participants consistently imagined themselves faster than they actually were. However, progressive inspiratory loading slowed iTUG more than TUG, a finding that is unexpected with regard to the known effects of dual tasking on TUG and iTUG (slower TUG but stable iTUG). Insofar as the cortical networks engaged in response to inspiratory loading are also activated during complex locomotor tasks requiring cognitive inputs, we infer that competition for cortical resources may account for the breathing-cognition interference that is evidenced here.

[1]  F. Hug,et al.  Simplified recording technique for the identification of inspiratory premotor potentials in humans , 2010, Respiratory Physiology & Neurobiology.

[2]  Lisa M Muratori,et al.  Cell phones change the way we walk. , 2012, Gait & posture.

[3]  C. Annweiler,et al.  Sleep-related breathing disorders and gait variability: a cross-sectional preliminary study , 2014, BMC Pulmonary Medicine.

[4]  T. Similowski,et al.  Sustained preinspiratory cortical potentials during prolonged inspiratory threshold loading in humans. , 2010, Journal of applied physiology.

[5]  C. Annweiler,et al.  Motor imagery of gait: a new way to detect mild cognitive impairment? , 2014, Journal of NeuroEngineering and Rehabilitation.

[6]  C. Annweiler,et al.  Hippocampal volume, early cognitive decline and gait variability: Which association? , 2015, Experimental Gerontology.

[7]  A. Hofman,et al.  Gait patterns in COPD: the Rotterdam Study , 2015, European Respiratory Journal.

[8]  Olivier Beauchet,et al.  Gait Changes with Anti-Dementia Drugs: A Prospective, Open-Label Study Combining Single and Dual Task Assessments in Patients with Alzheimer’s Disease , 2014, Drugs & Aging.

[9]  Mukul Mukherjee,et al.  Biomechanical analyses of stair-climbing while dual-tasking. , 2015, Journal of biomechanics.

[10]  Julien Doyon,et al.  Functional neuroanatomical networks associated with expertise in motor imagery , 2008, NeuroImage.

[11]  F. Hug,et al.  Electroencephalographic evidence for pre‐motor cortex activation during inspiratory loading in humans , 2007, The Journal of physiology.

[12]  Oliver Alan Kannape,et al.  Agency, gait and self-consciousness. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[13]  Diane Podsiadlo,et al.  The Timed “Up & Go”: A Test of Basic Functional Mobility for Frail Elderly Persons , 1991, Journal of the American Geriatrics Society.

[14]  T. Similowski,et al.  Does the Supplementary Motor Area Keep Patients with Ondine's Curse Syndrome Breathing While Awake? , 2014, PloS one.

[15]  Gary C. Sieck,et al.  ATS/ERS Statement on respiratory muscle testing. , 2002, American journal of respiratory and critical care medicine.

[16]  C. Morélot-Panzini,et al.  Electroencephalographic evidence for a respiratory-related cortical activity specific of the preparation of prephonatory breaths , 2014, Respiratory Physiology & Neurobiology.

[17]  C. Morélot-Panzini,et al.  Cortical drive to breathe in amyotrophic lateral sclerosis: a dyspnoea-worsening defence? , 2016, European Respiratory Journal.

[18]  B. Bloem,et al.  Neurological gait disorders in elderly people: clinical approach and classification , 2007, The Lancet Neurology.

[19]  马建新,et al.  用FEV6.0代替FVC诊断气道阻塞和肺功能受限[英]/Swanney MP…∥Am J Respir Crit Care Med. , 2002 .

[20]  C. Annweiler,et al.  Association between dual task-related decrease in walking speed and real versus imagined Timed Up and Go test performance , 2013, Aging Clinical and Experimental Research.

[21]  Roee Holtzer,et al.  Functional connectivity associated with gait velocity during walking and walking‐while‐talking in aging: A resting‐state fMRI study , 2015, Human brain mapping.

[22]  J B Poline,et al.  Neural substrates for the perception of acutely induced dyspnea. , 2001, American journal of respiratory and critical care medicine.

[23]  G. Allali,et al.  Gait abnormalities in obstructive sleep apnea and impact of continuous positive airway pressure , 2014, Respiratory Physiology & Neurobiology.

[24]  T. Similowski,et al.  Expiratory load compensation is associated with electroencephalographic premotor potentials in humans. , 2015, Journal of applied physiology.

[25]  Olivier Beauchet,et al.  Gait and motor imagery of gait in early schizophrenia , 2012, Psychiatry Research.

[26]  J. Gotman,et al.  Functional magnetic resonance imaging suggests automatization of the cortical response to inspiratory threshold loading in humans , 2013, Respiratory Physiology & Neurobiology.

[27]  Patrik Vuilleumier,et al.  The neural basis of age-related changes in motor imagery of gait: an fMRI study. , 2014, The journals of gerontology. Series A, Biological sciences and medical sciences.

[28]  Yunglin Gazes,et al.  Behavioral and neural correlates of imagined walking and walking‐while‐talking in the elderly , 2014, Human brain mapping.

[29]  Olaf Blanke,et al.  Respiratory Physiology & Neurobiology Breathing and Sense of Self: Visuo–respiratory Conflicts Alter Body Self-consciousness , 2022 .

[30]  P. Jones,et al.  Cognitive function in COPD , 2010, European Respiratory Journal.

[31]  John J. Foxe,et al.  Recalibration of inhibitory control systems during walking-related dual-task interference: A Mobile Brain-Body Imaging (MOBI) Study , 2014, NeuroImage.

[32]  Cédric Annweiler,et al.  Imagined Timed Up & Go test: A new tool to assess higher-level gait and balance disorders in older adults? , 2010, Journal of the Neurological Sciences.

[33]  D. Finn,et al.  The effect of pain on cognitive function: A review of clinical and preclinical research , 2011, Progress in Neurobiology.

[34]  T. Similowski,et al.  Cortical Drive to Breathe during Wakefulness in Patients with Obstructive Sleep Apnea Syndrome. , 2015, Sleep.

[35]  T. Similowski,et al.  Cerebral Cortex Activation during Experimentally Induced Ventilator Fighting in Normal Humans Receiving Noninvasive Mechanical Ventilation , 2007, Anesthesiology.

[36]  Yei-Yu Yeh,et al.  Cortical control of gait in healthy humans: an fMRI study , 2008, Journal of Neural Transmission.

[37]  O. Beauchet,et al.  Adapted Timed Up and Go: A Rapid Clinical Test to Assess Gait and Cognition in Multiple Sclerosis , 2012, European Neurology.

[38]  L. Cohen,et al.  The Cerebral Cost of Breathing: An fMRI Case-Study in Congenital Central Hypoventilation Syndrome , 2014, PloS one.