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

Marie-Cécile Nierat,Capucine Morélot-Panzini,Dan Adler,Suela Demiri,Thomas Similowski,Elise Dupuis-Lozeron,Gilles Allali

doi:10.1371/journal.pone.0151625

Abstract

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.

Highlights

In healthy humans, normal breathing stems from automatic brainstem neural processes and does not give rise to conscious perception: it does not engage motor or sensory cortical resources
Participants consistently imagined themselves being faster to perform the task than they were, but the TUG-iTUG difference decreased with increasing inspiratory loading, which is unexpected
We did not record electroencephalograms to demonstrate that inspiratory loading did result in a respiratory-related cortical activity, but this is a safe assumption in view of prior results: the inspiratory loading paradigm that we used has repeatedly been shown to elicit a consistent pattern of EEG responses in normal subjects [2,3,4, 20, 21]

Summary

Introduction

Normal breathing stems from automatic brainstem neural processes and does not give rise to conscious perception: it does not engage motor or sensory cortical resources. This cognitive improvement was concomitant with a reduction in overall cortical activity, changes in brain functional connectivity (stronger connectivity between brainstem and frontal lobe during spontaneous breathing than during mechanical ventilation), and restoration of the default mode network that is associated with self-consciousness, mind-wandering, creativity and introspection [9] This was interpreted as the result of "competition for cortical resources", in the general frame of dual tasking interferences. Inspiratory loads give rise to respiratory discomfort and negative emotions (namely "dyspnea") This is associated with increased metabolic activities within the limbic cortex [10] and with deactivation of the default mode network [5]. We designed the present study with the aim of testing this hypothesis by measuring TUG and iTUG in healthy volunteers submitted to a range of inspiratory loads

Participants and ethical approval

Experiments

Results

Discussion