Cortical gradients of functional connectivity are robust to state-dependent changes following sleep deprivation

NeuroImage, Vol. 226 (2021)

Mots clés
Authors
  • Nathan Cross
  • PERFORM Centre, Concordia University, Montreal, Canada; Center for Studies in Behavioral Neurobiology, Department of Health, Kinesiology and Applied Physiology, Concordia University, Montreal, Canada; Institut Universitaire de Gériatrie de Montréal and CRIUGM, CIUSSS du Centre-Sud-de-l’Île-de-Montréal, Montreal, Canada; Corresponding authors at: PERFORM Centre, Concordia University, 7141 Sherbrooke St. West, SP 165.30, Montreal H4B 1R6, Canada.
  • Casey Paquola
  • Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada
  • Florence B. Pomares
  • PERFORM Centre, Concordia University, Montreal, Canada; Center for Studies in Behavioral Neurobiology, Department of Health, Kinesiology and Applied Physiology, Concordia University, Montreal, Canada; Institut Universitaire de Gériatrie de Montréal and CRIUGM, CIUSSS du Centre-Sud-de-l’Île-de-Montréal, Montreal, Canada
  • Aurore A. Perrault
  • PERFORM Centre, Concordia University, Montreal, Canada; Center for Studies in Behavioral Neurobiology, Department of Health, Kinesiology and Applied Physiology, Concordia University, Montreal, Canada; Institut Universitaire de Gériatrie de Montréal and CRIUGM, CIUSSS du Centre-Sud-de-l’Île-de-Montréal, Montreal, Canada
  • Aude Jegou
  • PERFORM Centre, Concordia University, Montreal, Canada; Multimodal Functional Imaging lab, Department of Physics, Concordia University, Montreal, Canada
  • Alex Nguyen
  • PERFORM Centre, Concordia University, Montreal, Canada; Center for Studies in Behavioral Neurobiology, Department of Health, Kinesiology and Applied Physiology, Concordia University, Montreal, Canada
  • Umit Aydin
  • PERFORM Centre, Concordia University, Montreal, Canada; Multimodal Functional Imaging lab, Department of Physics, Concordia University, Montreal, Canada; Multimodal Funational Imaging Lab, Biomedical Engineering Dpt, Neurology and Neurosurgery Dpt, McGill University, Montreal, Quebec, Canada
  • Boris C. Bernhardt
  • Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada
  • Christophe Grova
  • PERFORM Centre, Concordia University, Montreal, Canada; Multimodal Functional Imaging lab, Department of Physics, Concordia University, Montreal, Canada; Multimodal Funational Imaging Lab, Biomedical Engineering Dpt, Neurology and Neurosurgery Dpt, McGill University, Montreal, Quebec, Canada; Corresponding authors at: Multimodal Functional Imaging lab, Department of Physics, Concordia University, Montreal, Canada.
  • Thien Thanh Dang-Vu
  • PERFORM Centre, Concordia University, Montreal, Canada; Center for Studies in Behavioral Neurobiology, Department of Health, Kinesiology and Applied Physiology, Concordia University, Montreal, Canada; Institut Universitaire de Gériatrie de Montréal and CRIUGM, CIUSSS du Centre-Sud-de-l’Île-de-Montréal, Montreal, Canada; Corresponding authors at: PERFORM Centre, Concordia University, 7141 Sherbrooke St. West, SP 165.30, Montreal H4B 1R6, Canada.

Résumé

Sleep deprivation leads to significant impairments in cognitive performance and changes to the interactions between large scale cortical networks, yet the hierarchical organization of cortical activity across states is still being explored. We used functional magnetic resonance imaging to assess activations and connectivity during cognitive tasks in 20 healthy young adults, during three states: (i) following a normal night of sleep, (ii) following 24hr of total sleep deprivation, and (iii) after a morning recovery nap. Situating cortical activity during cognitive tasks along hierarchical organizing gradients based upon similarity of functional connectivity patterns, we found that regional variations in task-activations were captured by an axis differentiating areas involved in executive control from default mode regions and paralimbic cortex. After global signal regression, the range of functional differentiation along this axis at baseline was significantly related to decline in working memory performance (2-back task) following sleep deprivation, as well as the extent of recovery in performance following a nap. The relative positions of cortical regions within gradients did not significantly change across states, except for a lesser differentiation of the visual system and increased coupling of the posterior cingulate cortex with executive control areas after sleep deprivation. This was despite a widespread increase in the magnitude of functional connectivity across the cortex following sleep deprivation. Cortical gradients of functional differentiation thus appear relatively insensitive to state-dependent changes following sleep deprivation and recovery, suggesting that there are no large-scale changes in cortical functional organization across vigilance states. Certain features of particular gradient axes may be informative for the extent of decline in performance on more complex tasks following sleep deprivation, and could be beneficial over traditional voxel- or parcel-based approaches in identifying realtionships between state-dependent brain activity and behavior.

Read more: fulltext