Functional imaging of working memory after 24 hr of total sleep deprivation

Abstract

The neurobehavioral effects of 24 hr of total sleep deprivation (SD) on working memory in young healthy adults was studied using functional magnetic resonance imaging. Two tasks, one testing maintenance and the other manipulation and maintenance, were used. After SD, response times for both tasks were significantly slower. Performance was better preserved in the more complex task. Both tasks activated a bilateral, left hemisphere-dominant frontal-parietal network of brain regions reflecting the engagement of verbal working memory. In both states, manipulation elicited more extensive and bilateral (L>R) frontal, parietal, and thalamic activation. After SD, there was reduced blood oxygenation level-dependent signal response in the medial parietal region with both tasks. Reduced deactivation of the anterior medial frontal and posterior cingulate regions was observed with both tasks. Finally, there was disproportionately greater activation of the left dorsolateral prefrontal cortex and bilateral thalamus when manipulation was required. This pattern of changes in activation and deactivation bears similarity to that observed when healthy elderly adults perform similar tasks. Our data suggest that reduced activation and reduced deactivation could underlie cognitive impairment after SD and that increased prefrontal and thalamic activation may represent compensatory adaptations. The additional left frontal activation elicited after SD is postulated to be task dependent and contingent on task complexity. Our findings provide neural correlates to explain why task performance in relatively more complex tasks is better preserved relative to simpler ones after SD.

Figure 1.

Schematic showing exemplars of stimuli used in LTR and PLUS and presentation timings. The control condition was identical for both tasks.

Figure 2.

Statistical activation maps of BOLD signal change for LTR and PLUS in RW and SD. Activations are projected onto the unfolded cortical surface of an individual volunteer's brain. Regions showing greater activation for PLUS than LTR for each state appear in the bottom panels.

Figure 3.

Reduced task-related deactivation in the anterior medial frontal (a) and posterior cingulate (b) regions after SD. Error bars denote SE (c) The correlation between RTs and BOLD signal change in the anterior medial frontal region jointly activated in both states and tasks. d, ROI from which the extent of deactivation was determined.

Figure 4.

Statistical activation maps showing differences in activation elicited by each task during SD and RW. a, Parietal region that showed reduced activation after SD; b, left prefrontal region that showed increased activation after SD. The deactivated areas are not shown.

Figure 5.

Parameter estimates obtained from individual subjects' ROI in the left dorsolateral prefrontal cortex. A main effect of task on activation and disproportionately higher activation in response to PLUS during SD are illustrated. Error bars denote ± 1 SE.

Figure 6.

Thalamic regions jointly activated in both tasks and both states. Parameter estimates from the thalamic region indicated (peak coordinate, -16, -21, 2) are shown. Error bars denote ± 1 SE.