Altered salience network connectivity predicts macronutrient intake after sleep deprivation

Abstract

Although insufficient sleep is a well-recognized risk factor for overeating and weight gain, the neural mechanisms underlying increased caloric (particularly fat) intake after sleep deprivation remain unclear. Here we used resting-state functional magnetic resonance imaging and examined brain connectivity changes associated with macronutrient intake after one night of total sleep deprivation (TSD). Compared to the day following baseline sleep, healthy adults consumed a greater percentage of calories from fat and a lower percentage of calories from carbohydrates during the day following TSD. Subjects also exhibited increased brain connectivity in the salience network from the dorsal anterior cingulate cortex (dACC) to bilateral putamen and bilateral anterior insula (aINS) after TSD. Moreover, dACC-putamen and dACC-aINS connectivity correlated with increased fat and decreased carbohydrate intake during the day following TSD, but not during the day following baseline sleep. These findings provide a potential neural mechanism by which sleep loss leads to increased fat intake.

Figure 1. Caloric and macronutrient intake.

Caloric intake was ad libitum during the study. (a) Despite consuming nearly 1000 kcal during the overnight period of wakefulness, sleep-deprived subjects consumed a similar amount of calories during the day following total sleep deprivation (TSD) as during the day following baseline sleep (BL). Subjects randomized to the control condition consumed a similar amount of calories during corresponding days (BL and CD1). (b) Sleep-deprived subjects consumed a larger percentage of calories from fat and a smaller percentage of calories from carbohydrates during the day following TSD compared to the day following BL sleep. Macronutrient intake did not differ between corresponding days in control subjects (BL and CD1). Data presented as Mean ± SEM; *p<0.05.

Figure 2. dACC-seed functional connectivity.

Compared to the scan following baseline sleep, resting-state FC between dorsal anterior cingulate cortex (dACC) and the following regions was increased during the scan following total sleep deprivation (TSD-BL): bilateral putamen, bilateral anterior insula (aINS), bilateral inferior frontal gyrus (IFG), bilateral parietal lobe, and medial frontal cortex (MFC). All of these areas survived whole brain cluster-level FWE corrected p<0.005. There were no significant changes in dACC connectivity between corresponding days in the control condition (CD1-BL).

Figure 3. Salience network functional connectivity.

Region of interests (ROI) analyses confirmed altered dorsal anterior cingulate (dACC)-bilateral putamen and dACC-bilateral insula resting-state FC after total sleep deprivation (TSD). Anatomical bilateral putamen and bilateral insula were defined as the ROIs using wfupickatlas tool box. The correlation coefficients between these regions and the dACC were then extracted. Compared to the scan following baseline sleep (BL), resting-state FC was significantly increased between the dACC and bilateral putamen (a) and between the dACC and bilateral insula (b) after TSD. No changes in dACC connectivity with bilateral putamen or bilateral insula were observed between corresponding days in the control condition (BL and CD1). Data presented as Mean ± SEM; **p<0.005.

Figure 4. Correlation between dACC-Putamen connectivity and macronutrient intake after TSD.

During the day following total sleep deprivation (TSD), dorsal anterior cingulate cortex (dACC)-putamen connectivity was positively correlated with fat intake (a) and negatively correlated with carbohydrate intake (b) but was not significantly related to protein intake.

Figure 5. Correlation between dACC-aINS connectivity and macronutrient intake after TSD.

During the day following total sleep deprivation (TSD), dorsal anterior cingulate cortex (dACC)-bilateral anterior insula (aINS) connectivity was positively correlated with fat intake (a) and negatively correlated with carbohydrate intake (b) but was not significantly related to protein intake.

Figure 6. Protocol summary.

Subjects arrived at the laboratory in the afternoon and were provided 9h time-in-bed (TIB) for their baseline sleep night. The first functional magnetic resonance imaging (fMRI) scan session took place the next morning (Baseline [BL] day) from 0700h-1000h. Subjects were then randomized to either a total sleep deprivation (TSD) or control condition. During the second night of the study, sleep-deprived subjects were kept awake and control subjects were allowed 8 h TIB to sleep. The second fMRI scan session took place the next morning from 0700h-1000h (total sleep deprivation [TSD] day or control day 1 [CD1]). Sleep-deprived subjects were then allowed 12 TIB for recovery sleep and control subjects were allowed 8 h TIB to sleep. Each subject was scanned at the same time for each scan to avoid potential time-of-day differences between scans. Subjects had ad libitum to food/drink during the study. Subjects remained in the laboratory for the duration of the study and were monitored by trained staff at all times to ensure adherence to the protocol.