Impact of inspiratory threshold loading on brain activity and cognitive performances in healthy humans

Abstract

In healthy humans, inspiratory threshold loading deteriorates cognitive performances. This can result from motor-cognitive interference (activation of motor respiratory-related cortical networks vs. executive resources allocation), sensory-cognitive interference (dyspnea vs. shift in attentional focus), or both. We hypothesized that inspiratory loading would concomitantly induce dyspnea, activate motor respiratory-related cortical networks, and deteriorate cognitive performance. We reasoned that a concomitant activation of cortical networks and cognitive deterioration would be compatible with motor-cognitive interference, particularly in case of a predominant alteration of executive cognitive performances. Symmetrically, we reasoned that a predominant alteration of attention-depending performances would suggest sensory-cognitive interference. Twenty-five volunteers (12 men; 19.5-51.5 years) performed the Paced Auditory Serial Addition test (PASAT-A and B; calculation capacity, working memory, attention), the Trail Making Test (TMT-A, visuospatial exploration capacity; TMT-B, visuospatial exploration capacity and attention), and the Corsi block-tapping test (visuospatial memory, short-term and working memory) during unloaded breathing and inspiratory threshold loading in random order. Loading consistently induced dyspnea and respiratory-related brain activation. It was associated with deteriorations inPASAT A (52 [45.5;55.5] (median [interquartile range]) to 48 [41;54.5], p=0.01), PASAT B (55 [47.5;58] to 51 [44.5;57.5], p=0.01), and TMT B (44s [36;54.5] to 53s [42;64], p=0.01), but did not affect TMT-A and Corsi. The concomitance of cortical activation and cognitive performance deterioration is compatible with competition for cortical resources (motor-cognitive interference), while the profile of cognitive impairment (PASAT and TMT-B but not TMT-A and Corsi) is compatible with a contribution of attentional distraction (sensory-cognitive interference). Both mechanisms are therefore likely at play.

Inspiratory threshold loading negatively impacts attentional performance

“…activate motor respiratory-related cortical networks, leading to diminished cognitive performance (Taytard et al, 2021). Indeed, pilot work by our group suggests increasing inspiratory effort sensation may prolong the period of central information processing during complex reaction time tasks.…”

Short-term cognitive loading deteriorates breathing pattern and gas exchange in adult patients with congenital central hypoventilation syndrome

“…Given the size of the population, the data from the resulting groups were then pooled: no between-group comparisons were conducted. Also to limit the impact of learning effect, two versions of the Paced Auditory Serial Addition Test (PASAT) were performed according to a XYYX plan (unassisted breathing -ventilatory support -ventilatory support -unassisted breathing) [5]. Under ventilatory support, the patients used their usual ventilatory support devices and settings (controlled mode in all cases; non-invasive ventilation in pressure control mode in 6 patients, volume controlled ventilation through a tracheotomy in 1 patient).…”

“…All the patients confirmed being familiar with the corresponding mode of mechanical ventilation during wakefulness. Because CCHS patients exhibit a respiratory-related cortical activity during unassisted breathing [2] that decreases during ventilatory support [3] and because changes in a respiratory-related cortical activity have been shown to occur concomitantly with changes in cognitive performances during inspiratory loading in normal humans [5], electroencephalogram (EEG) recordings were acquired during the first and last 10 minutes of the evaluations (Figure 1). The aim of these recordings were to document that ventilatory support was associated with changes in brain activity.…”

“…Among the many existing neuropsychological tests, we chose three on which the impact of changes in respiratory-related cortical activation has been studied before [5]. The participants underwent:…”

“…-1) the Paced Auditory Serial Addition Test (PASAT) version A and B [12], during which patients were given a number from 0 to 9 every 3 seconds and asked to recall the two most recent numbers (3-minute fixed duration) ; the PASAT evaluates calculation capacity, working memory, sustained and divided attention; respiratory-related brain activation has been associated with PASAT deterioration in healthy subjects [5]; -2) the Trail Making Test (TMT) A and B [13][14][15], during which patients were asked to connect a set of dots as quickly and as accurately as possible (TMT duration varied between 15-20version A-to 60-90 seconds -version B-) ; the TMT evaluates visuospatial exploration capacity, and cognitive processing speed (version A), plus attentional flexibility (version B); attentional flexibility alone was evaluated by subtracting TMT-B time from TMT-A time; respiratory-related brain activation has been associated with deterioration of TMT-A without effect on TMT-B in healthy subjects [5];…”