Is a Responsive Default Mode Network Required for Successful Working Memory Task Performance?
In studies of cognitive processing using tasks with externally directed attention, regions showing increased (external-task-positive) and decreased or "negative" [default-mode network (DMN)] fMRI responses during task performance are dynamically responsive to increasing task difficulty. Responsiveness (modulation of fMRI signal by increasing load) has been linked directly to successful cognitive task performance in external-task-positive regions but not in DMN regions. To investigate whether a responsive DMN is required for successful cognitive performance, we compared healthy human subjects (n = 23) with individuals shown to have decreased DMN engagement (chronic pain patients, n = 28). Subjects performed a multilevel working-memory task (N-back) during fMRI. If a responsive DMN is required for successful performance, patients having reduced DMN responsiveness should show worsened performance; if performance is not reduced, their brains should show compensatory activation in external-task-positive regions or elsewhere. All subjects showed decreased accuracy and increased reaction times with increasing task level, with no significant group differences on either measure at any level. Patients had significantly reduced negative fMRI response (deactivation) of DMN regions (posterior cingulate/precuneus, medial prefrontal cortex). Controls showed expected modulation of DMN deactivation with increasing task difficulty. Patients showed significantly reduced modulation of DMN deactivation by task difficulty, despite their successful task performance. We found no evidence of compensatory neural recruitment in external-task-positive regions or elsewhere. Individual responsiveness of the external-task-positive ventrolateral prefrontal cortex, but not of DMN regions, correlated with task accuracy. These findings suggest that a responsive DMN may not be required for successful cognitive performance; a responsive external-task-positive network may be sufficient.


CONCLUSIONS
We studied the relationship between responsiveness of the brain to increasing task demand and successful cognitive performance, using chronic pain patients as a probe. fMRI working memory studies show that two main cognitive networks ["external-task positive" and "default-mode network" (DMN)] are responsive to increasing task difficulty. The responsiveness of both of these brain networks is suggested to be required for successful task performance. The responsiveness of external-task-positive regions has been linked directly to successful cognitive task performance, as we also show here. However, pain patients show decreased engagement and responsiveness of the DMN but can perform a working memory task as well as healthy subjects, without demonstrable compensatory neural recruitment. Therefore, a responsive DMN might not be needed for successful cognitive performance.
National Center for Complementary and Integrative Health, National Institutes of Health, Bethesda, Maryland 20892.
Marta
M
Čeko
National Center for Complementary and Integrative Health, National Institutes of Health, Bethesda, Maryland 20892.
John L
JL
Gracely
Rheumatology, McGill University, Montreal, Quebec H3A 0G4, Canada, and.
Mary-Ann
MA
Fitzcharles
Department of Neural and Pain Sciences, School of Dentistry, University of Maryland, Baltimore, Maryland 21201.
David A
http://orcid.org/0000-0003-3111-3756
DA
Seminowicz
Alan Edwards Centre for Research on Pain, Dentistry, Neurology and Neurosurgery, and.
Petra
P
Schweinhardt
National Center for Complementary and Integrative Health, National Institutes of Health, Bethesda, Maryland 20892, mary.bushnell@nih.gov.
M Catherine
MC
Bushnell
D000328:Adult; D001921:Brain / Q000503:physiopathology*; D001931:Brain Mapping; D059350:Chronic Pain / Q000150:complications / Q000503:physiopathology; D003071:Cognition; D058245:Cognitive Reserve; D005260:Female; D006801:Humans; D008279:Magnetic Resonance Imaging; D008569:Memory Disorders / Q000209:etiology / Q000503:physiopathology*; D008570:Memory, Short-Term; D008875:Middle Aged; D009415:Nerve Net / Q000503:physiopathology*; D013647:Task Performance and Analysis
FMRI; chronic pain; default mode; external-task-positive; task performance; working memory