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Featured ArticleArticles, Behavioral/Systems/Cognitive

Functional Magnetic Resonance Imaging-Assessed Brain Responses during an Executive Task Depend on Interaction of Sleep Homeostasis, Circadian Phase, and PER3 Genotype

Gilles Vandewalle, Simon N. Archer, Catherine Wuillaume, Evelyne Balteau, Christian Degueldre, André Luxen, Pierre Maquet and Derk-Jan Dijk
Journal of Neuroscience 24 June 2009, 29 (25) 7948-7956; DOI: https://doi.org/10.1523/JNEUROSCI.0229-09.2009
Gilles Vandewalle
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Simon N. Archer
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Catherine Wuillaume
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Evelyne Balteau
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Christian Degueldre
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André Luxen
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Pierre Maquet
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Derk-Jan Dijk
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  • Figure 1.
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    Figure 1.

    Schematic representation of the protocol and the homeostatic and circadian processes in PER34/4 and PER35/5 . All times are in clock time (h). a , Circadian arousal signal (Sleep-Wake) [arbitrary units (a.u.)], which promotes wakefulness during the day and sleep at night (based on data published in Dijk et al., 1997) oscillates independently from sleep-wake behavior and similarly in PER34/4 and PER3 5/5. The nadir of the circadian arousal rhythm is located in the early morning and its crest at the end of the habitual waking day. The time course of melatonin during the sleep deprivation condition (means + SE; SEs are not plotted for n ≤2) is plotted to the right. b , Homeostatic sleep pressure (a.u.) increases during wakefulness, declines during sleep, and increases further during sleep deprivation. Based on waking and sleep EEG data (Viola et al., 2007), homeostatic sleep pressure increases and declines more rapidly in PER35/5 . Vertical lines, Positions of the different fMRI sessions.

  • Figure 2.
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    Figure 2.

    Significant differences in brain response between the sessions recorded after 14 h and 1.5 h of wakefulness. a , PER35/5 significantly reduced response in the right posterior inferior frontal gyrus during ES compared with MS. Statistical results are overlaid to the population mean structural image (p uncorrected < 0.001). No significant changes were observed in PER34/4 . b , Mean activity estimates (a.u. ± SEM; in all figures * indicates the significant differences at p < 0.05 at the voxel level after correction for multiple comparisons).

  • Figure 3.
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    Figure 3.

    Significant differences in brain response between the sessions recorded after 25 h and 1.5 h of wakefulness. Middle panels, In PER34/4 (blue), only significant increased activations were found in MSD compared with MS. In PER35/5 (red), only significant reduced activations were found in MSD compared with MS (see Table 2 for the names corresponding to the letters in the structural image). The difference in overnight change in activity in the area circled in yellow (thalamus; Z 4 brain slice) on the nights with and without sleep was significantly and negatively correlated with the self-assessed likelihood to fall asleep in nonstimulating situations during a normal waking day. Lateral panels, Mean activity estimates (a.u. ± SEM). Note that in the left panels ( a–h ), for all areas indicated by an asterisk (*), there were significant increases in activation, i.e., only in PER34/4 , whereas in the right panels ( i–q ) for all areas indicated by an asterisk (*), there were decreases in activation, i.e., only in PER35/5 . Note that in the middle frontal gyrus ( i ), difference is also significant between MS and ES as reported in Figure 2.

  • Figure 4.
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    Figure 4.

    Significant differences in brain response between the sessions recorded after 25 and 14 h of wakefulness. Middle panels, In PER34/4 (blue), only significant increased activations were found in MSD compared with ESD. In PER35/5 (red), only significant reduced activations were found in MSD compared with ESD (see Table 3 for the names corresponding to the letters in the structural image). Lateral panels, Mean activity estimates (a.u. ± SEM) at ESD and MSD. Left ( a–c ) ESD < MSD; right ( d–p ) ESD > MSD. Note that in left panels, for all areas indicated by an asterisk (*), there were significant increases in activation, i.e., only in PER34/4 , whereas in right panels, for all areas indicated by an asterisk (*), there were significant decreases in activation, i.e., only in PER35/5 .

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    Table 1.

    Behavioral results (mean ± SD)

    Subjective sleepiness (Karolinska Sleepiness Scale) Accuracy on the task (% correct responses) Reaction times (ms)
    PER34/4 PER35/5 PER34/4 PER35/5 PER34/4 PER35/5
    MS3.8 ± 1.13.7 ± 1.189.7 ± 6.488.6 ± 5.71003 ± 1581108 ± 255
    ES4.1 ± 1.44.3 ± 1.387.9 ± 6.286.7 ± 5.21060 ± 1561162 ± 242
    ESD3.7 ± 1.23.8 ± 1.283.7 ± 9.486.4 ± 8.81123 ± 2041133 ± 250
    MSD7.6 ± 0.87.4 ± 1.684.1 ± 882.4 ± 11.91060 ± 1761132 ± 258
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    Table 2.

    Significant differences between sessions recorded after 25 h (MSD) and 1.5 h (MS) of wakefulness in brain activity related to the 3-back task in PER34/4 and PER35/5 genotypes

    Brain areasSideX, Y, ZZ scoreBrodmann's areapcorrected value
    Increase in brain activity in PER34/4 (MSD > MS)
        Inferior frontal gyrus (a)R40, 42, 03.94460.003 ¶ , #
        Middle temporal gyrus (b)R54, −44, −63.26210.023 ¶ , #
        Parahippocampus (c,d)L−30, −34, −143.910.003 ¶ , #
    R30, −38, −83.180.028
        Thalamus (e,f)L−26, −30, 63.810.005 #
    L−14, −24, 103.390.016
    L−20, −18, 43.250.022
    R8, −8, 43.270.024
        Superior colliculus (g)L−4, −40, −44.000.002
        Cerebellum (h)L−32, −76, −263.800.005 ¶ , #
    Decrease in brain activity in PER34/4 (MSD < MS)
        No significant voxels (p uncorrected < 0.001)
    Increase in brain activity in PER35/5 (MSD > MS)
        No significant voxels (p uncorrected < 0.001)
    Decrease in brain activity in PER35/5 (MSD < MS)
        Middle frontal gyrus (i,j)R44, 24, 223.5844/450.009 ¶ , #
    L−30, 46, 343.1590.030
        Superior parietal cortex (k)L−24, −52, 603.5570.010 ¶ , #
    L−24, −62, 523.9170.003
    R30, −48, 663.1470.031 ¶ , #
        Postcentral gyrus/anterior intraparietal sulcus (l,m)L−54, −22, 403.10400.035
    R42, −32, 363.31400.020 #
        Superior temporal sulcus (n,o)L−64, −34, 44.64220.05 ¶
    L−56, −46, 84.2921/220.011 #
    L−56, 6, −203.52210.001
    R60, −22, −44.64220.05
    R54, −38, −24.08210.002 ¶ , #
        Middle occipital gyrus (p,q)L−44, −72, −83.87370.013 ¶ , #
    L−22, −88, −63.46180.004 ¶ , #
    L−44, −86, 43.37370.017 ¶
    L−34, −90, −63.23180.025 ¶ , #
    R40, −76, −83.47370.013 ¶
    • Letters in parentheses (a–q): refer to Figure 3. L, Left; R, right.

    • ↵ ¶Significant interaction between session and genotype: [(MSD > MS) * (PER34/4 > PER35/5 )].

    • ↵ #Significant interaction between session, segment, and genotype: [(MSD > ESD) > (MS > ES) * (PER34/4 > PER35/5 )] (see supplemental Table S6, available at www.jneurosci.org as supplemental material, for complete results of this interaction).

    • View popup
    Table 3.

    Significant differences between sessions recorded after 25 h (MSD) and 14 h (ESD) of wakefulness in brain activity related to the 3-back task in PER34/4 and PER35/5 genotypes

    Brain areasSideX, Y, ZBrodmann's areaZpcorrected value
    Increase in brain activity in PER34/4 (MSD > ESD)
        Thalamus (a)L−6, −12, 83.100.039 ¶
        Parahippocampus (b)L−24, −42, −103.130.036 ¶
        Cerebellum (c)L−30, −76, −263.260.026 ¶
    Decrease in brain activity in PER34/4 (MSD < ESD)
        No significant voxels (p uncorrected < 0.001)
    Increase in brain activity in PER35/5 (MSD > ESD)
        No significant voxels (p uncorrected <0.001)
    Decrease in brain activity in PER35/5 (MSD < ESD)
        Inferior frontal gyrus (d)L−54, 32, 12464.750.038 ¶
        Inferior frontal gyrus/middle frontal gyrus (e)R46, 32, 4464.670.05 ¶
    R44, 32, 14463.930.003
    R40, 18, 2244/453.920.004
        Superior frontal sulcusL−22, 54, 0103.600.010
        Superior parietal cortex (f,g)L−24, −54, 6273.870.004
    L−26, −64, 5673.800.005
    R24, −52, 6073.480.018
    R14, −54, 6673.330.022 ¶
        Postcentral gyrus/anterior intraparietal sulcus (h,i)R42, −32, 40404.080.002
    L−38, −24, 42403.390.018
        Superior temporal sulcus (j,k)L−52, 12, −26214.850.026 ¶
    L−52, −48, 821/224.65< 0.001 ¶
    R52, −36, −8214.020.003 ¶
        Middle occipital gyrus (l,m)R30, −86, −4194.420.002 ¶
    R32, −84, 10193.630.009 ¶
    L−38, −72, −219/374.360.001 ¶
    L−24, −86, −4184.120.001 ¶
    L−22, −76, 18193.470.015 ¶
        Fusiform gyrusR42, −58, −1819/374.070.002 ¶
    R28, −66, −12193.670.008
        Cingulate cortex (n)L−10, −18, 3624/313.870.004 ¶
    R16, 46, 10323.430.016
        Insula (o)L−38 −10 123.730.007
        Putamen (p)L−22, 2, 23.500.013 ¶
        Globus pallidusR20, 0, 03.350.020 ¶
    • Letters in parentheses (a–v): Reference to Figure 4. L, Left; R, right.

    • ↵ ¶Significant interaction between session and genotype: [(MSD > ESD) * (PER34/4 > PER35/5 )].

Additional Files

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    Files in this Data Supplement:

    • supplemental material - Supplemental Material
    • supplemental material - Supplemental Figure 1
    • supplemental material - Supplemental Figure 2
    • supplemental material - Supplemental Figure 3
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The Journal of Neuroscience: 29 (25)
Journal of Neuroscience
Vol. 29, Issue 25
24 Jun 2009
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Functional Magnetic Resonance Imaging-Assessed Brain Responses during an Executive Task Depend on Interaction of Sleep Homeostasis, Circadian Phase, and PER3 Genotype
Gilles Vandewalle, Simon N. Archer, Catherine Wuillaume, Evelyne Balteau, Christian Degueldre, André Luxen, Pierre Maquet, Derk-Jan Dijk
Journal of Neuroscience 24 June 2009, 29 (25) 7948-7956; DOI: 10.1523/JNEUROSCI.0229-09.2009

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Functional Magnetic Resonance Imaging-Assessed Brain Responses during an Executive Task Depend on Interaction of Sleep Homeostasis, Circadian Phase, and PER3 Genotype
Gilles Vandewalle, Simon N. Archer, Catherine Wuillaume, Evelyne Balteau, Christian Degueldre, André Luxen, Pierre Maquet, Derk-Jan Dijk
Journal of Neuroscience 24 June 2009, 29 (25) 7948-7956; DOI: 10.1523/JNEUROSCI.0229-09.2009
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