Altered superficial amygdala–cortical functional link in resting state after 36 hours of total sleep deprivation

Abstract

The superficial amygdala (SFA) is important in human emotion/affective processing via its strong connection with other limbic and cerebral cortex for receptive and expressive emotion processing. Few studies have investigated the functional connectivity changes of the SFA under extreme conditions, such as prolonged sleep loss, although the SFA showed a distinct functional connectivity pattern throughout the brain. In this study, resting-state functional magnetic resonance imaging (rs-fMRI) was employed to investigate the changes of SFA-cortical functional connectivity after 36 hr of total sleep deprivation (TSD). Fourteen healthy male volunteers aged 25.9 ± 2.3 years (range 18-28 years) enrolled in this within-subject crossover study. We found that the right SFA showed increased functional connectivity with the right medial prefrontal cortex (mPFC) and decreased functional connectivity with the right dorsal posterior cingulate cortex (dPCC) in the resting brain after TSD compared with that during rested wakefulness. For the left SFA, decreased connectivity with the right dorsal anterior cingulate cortex (dACC) and right dPCC was found. Further regression analysis indicated that the functional link between mPFC and SFA significantly correlated with the Profile of Mood State scores. Our results suggest that the amygdala cannot be treated as a single unit in human neuroimaging studies and that TSD may alter the functional connectivity pattern of the SFA, which in turn disrupts emotional regulation.

Intrinsic brain connectivity after partial sleep deprivation in young and older adults: results from the Stockholm Sleepy Brain study

“…Time courses were compared within each run using the DPARSFA toolbox and the resulting z-statistics were entered into a mixed-effects linear regression model with deviation coding for contrasts in R 66 . In addition, following Shao et al 12 , we defined a thalamus region of interest (ROI) using the Wake Forest University PickAtlas 67-69 , and following Shao et al 12,13 and Lei et al 14 , we selected right and left thalamus ROI:s as well as separate ROI:s for the superficial, centromedial, and basolateral amygdala, as defined by Amunts et al 70 , using the Jülich atlas [71][72][73] . Furthermore, at the suggestion of one reviewer, we investigated default mode network using seed-based methods.…”

“…Based on reports of effects of sleep deprivation on connectivity from the thalamus 12,22 and amygdala 13,14 , we investigated whether earlier results could be replicated. Seed regions are shown in supplemental figures 3 and 4 for thalamus and amygdala, respectively.…”

“…A consistent and robust finding is that sleep deprivation caused reduced connectivity within the default mode network and reduced anticorrelation to the task-positive network 8,10,22 . Other findings include increased regional homogeneity (ReHo) in different brain areas following sleep deprivation 9,18 , changes in connectivity between the thalamus 12 and amygdala 13,14 and cortical areas. We formulated a number of hypotheses to try to replicate these findings (see below).…”

Intrinsic brain connectivity after partial sleep deprivation in young and older adults: results from the Stockholm Sleepy Brain study

“…A consistent and robust finding is that sleep deprivation caused reduced connectivity within the default mode network and reduced anticorrelation to the task-positive network 8 , 10 , 22 . Other findings include increased regional homogeneity (ReHo) in different brain areas following sleep deprivation 9 , 18 , changes in connectivity between the thalamus 12 and amygdala 13 , 14 and cortical areas. We formulated a number of hypotheses to try to replicate and extend these findings (see below).…”

Tired and misconnected: A breakdown of brain modularity following sleep deprivation

“…For instance, several neuroimaging studies have now shown that SD results in hyper activation of the amygdala typically coupled with reduced amygdala‐prefrontal connectivity (see review by Goldstein and Walker []). Interestingly, resting‐state studies have also revealed significant alterations in the connectivity profile of the amygdala following 36 h of SD, reflecting preexisting changes in limbic network connectivity, prior to any task performance [Lei et al, ; Shao et al, ]. Changes in resting thalamic connectivity were also detected following SD, demonstrating a reduction in thalamic connectivity with multiple temporal and prefrontal regions [Shao et al, ], thought to reflect substantial changes in vigilance without sleep.…”