Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2012 May 16;32(20):6937-46.
doi: 10.1523/JNEUROSCI.3553-11.2012.

Sleep deprivation is associated with attenuated parametric valuation and control signals in the midbrain during value-based decision making

Affiliations

Sleep deprivation is associated with attenuated parametric valuation and control signals in the midbrain during value-based decision making

Mareike M Menz et al. J Neurosci. .

Abstract

Sleep deprivation (SD) has detrimental effects on cognition, but the affected psychological processes and underlying neural mechanisms are still essentially unclear. Here we combined functional magnetic resonance imaging and computational modeling to examine how SD alters neural representation of specific choice variables (subjective value and decision conflict) during reward-related decision making. Twenty-two human subjects underwent two functional neuroimaging sessions in counterbalanced order, once during rested wakefulness and once after 24 h of SD. Behaviorally, SD attenuated conflict-dependent slowing of response times, which was reflected in an attenuated conflict-induced decrease in drift rates in the drift diffusion model. Furthermore, SD increased overall choice stochasticity during risky choice. Model-based functional neuroimaging revealed attenuated parametric subjective value signals in the midbrain, parietal cortex, and ventromedial prefrontal cortex after SD. Conflict-related midbrain signals showed a similar downregulation. Findings are discussed with respect to changes in dopaminergic signaling associated with the sleep-deprived state.

PubMed Disclaimer

Figures

Figure 1.
Figure 1.
a, Overview of the procedure. Subjects were scanned twice in counterbalanced order using fMRI, once after normal sleep (rested wakefulness), and once after 24 h of SD. After the second scan, one trial from all sessions was randomly selected and paid out for real. b, Outline of a single trial. Participants made choices between a fixed sure-gain reference reward of 20€ and larger options with reduced probability.
Figure 2.
Figure 2.
a, Participants' log-transformed probability discount rates showed highly significant test–retest reliability. b, c, RTs were binned depending on the value difference between options. For CON (b), a quadratic function provided a significantly better fit to the RT data than a linear function, which was not the case for SD (c). Solid lines in b and c depict the best quadratic fit, and dashed lines depict the best linear fit. Error bars indicate SEM.
Figure 3.
Figure 3.
Results from the RDM, which was fit to aggregate data from all subjects (see Materials and Methods). Hard trials (those 50% of trials on which the value of the risky option was closest to the 20€ reference) and easy trials (all other trials) were modeled separately. Drift rates (a, reflecting the rate of evidence accumulation) were greater for easy than hard trials, but this effect was more pronounced in control than after SD. Estimated boundary separation (b, reflecting response accuracy) showed a similar effect, whereas response bias (c) was primarily unaffected by sleep state. Error bars denote SEs of the bootstrap parameter estimates.
Figure 4.
Figure 4.
Neural activity related to the onset of the decision option (conjunction analysis control + sleep-deprived, pFWE < 0.05 corrected for whole-brain volume) projected onto a glass brain (a). The most prominently activated clusters were located in the lateral occipital cortex (LOC), ACC, and inferior frontal gyrus (IFG) (b). In these regions, task-related responses were of similar magnitude in CON and SD. c, Right insula activation was greater in CON than SD, whereas a posterior mOFC cluster showed greater activity for SD than CON. Activations are projected onto the mean normalized T1 image.
Figure 5.
Figure 5.
Regions in which neural activity showed a positive correlation with subjective value in the control condition (rested wakefulness) of the present study (blue) and in the probability discounting condition of our previous study (green) (Peters and Buechel, 2009). Note the overlap in activations. Both contrasts are thresholded at p < 0.001 uncorrected and projected onto the mean normalized T1 from the present study for visualization. Valuation-related activity was observed in regions of the dopaminergic system (SN/VTA and ventral striatum) and an extensive frontoparietal network.
Figure 6.
Figure 6.
Parametric neuroimaging results (top row, hyperbolic model; bottom row, Prelec model). All images depict conjunction contrasts reflecting a positive correlation with the respective parameter in the control condition and an attenuated correlation after SD (all contrasts thresholded at p < .001 uncorrected). SD was associated with a significant reduction in value coding (left) and decision conflict coding (middle) in the SN/VTA. Subjective value coding of the chosen option (right) in was attenuated in the vmPFC. Midbrain and vmPFC activations survive correction for multiple comparisons across a priori regions of interest (see Materials and Methods) and are projected on the mean normalized T1 image. SV, Subjective value.
Figure 7.
Figure 7.
Results from additional fMRI models. a, ACC activity was associated with decision conflict even when conflict was orthogonalized with respect to chosen − unchosen value. b, Attenuated conflict effects in the midbrain (conjunction analysis: correlation with conflict in CON and significant reduction after SD) also survived controlling for variance attributable to chosen − unchosen value. c, A network of anterior and posterior midline regions was positively correlated with chosen − unchosen value (FitzGerald et al., 2009), even when this regressor was orthogonalized with respect to the conflict regressor. Display thresholds a, c: p < 0.001, uncorrected, k ≥ 10 voxels; b: p < 0.005, uncorrected, k ≥ 10 voxels.

References

    1. Acheson A, Richards JB, de Wit H. Effects of sleep deprivation on impulsive behaviors in men and women. Physiol Behav. 2007;91:579–587. - PubMed
    1. Balkin TJ, Braun AR, Wesensten NJ, Jeffries K, Varga M, Baldwin P, Belenky G, Herscovitch P. The process of awakening: a PET study of regional brain activity patterns mediating the re-establishment of alertness and consciousness. Brain. 2002;125:2308–2319. - PubMed
    1. Bilder RM, Volavka J, Lachman HM, Grace AA. The catechol-O-methyltransferase polymorphism: relations to the tonic-phasic dopamine hypothesis and neuropsychiatric phenotypes. Neuropsychopharmacology. 2004;29:1943–1961. - PubMed
    1. Boehler CN, Hopf JM, Krebs RM, Stoppel CM, Schoenfeld MA, Heinze HJ, Noesselt T. Task-load-dependent activation of dopaminergic midbrain areas in the absence of reward. J Neurosci. 2011a;31:4955–4961. - PMC - PubMed
    1. Boehler CN, Bunzeck N, Krebs RM, Noesselt T, Schoenfeld MA, Heinze HJ, Münte TF, Woldorff MG, Hopf JM. Substantia nigra activity level predicts trial-to-trial adjustments in cognitive control. J Cogn Neurosci. 2011b;23:362–373. - PMC - PubMed

Publication types

MeSH terms

LinkOut - more resources