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Research ArticleNew Research, Integrative Systems

Effects of Chronic Sleep Restriction during Early Adolescence on the Adult Pattern of Connectivity of Mouse Secondary Motor Cortex

Yazan N. Billeh, Alexander V. Rodriguez, Michele Bellesi, Amy Bernard, Luisa de Vivo, Chadd M. Funk, Julie Harris, Sakiko Honjoh, Stefan Mihalas, Lydia Ng, Christof Koch, Chiara Cirelli and Giulio Tononi
eNeuro 22 April 2016, 3 (2) ENEURO.0053-16.2016; https://doi.org/10.1523/ENEURO.0053-16.2016
Yazan N. Billeh
1Computation and Neural Systems Program, California Institute of Technology, Pasadena, California 91125
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Alexander V. Rodriguez
2Department of Psychiatry, University of Wisconsin-Madison, Madison, Wisconsin 53719
3Neuroscience Training Program, University of Wisconsin-Madison, Madison, Wisconsin 53705
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Michele Bellesi
2Department of Psychiatry, University of Wisconsin-Madison, Madison, Wisconsin 53719
4Department of Experimental and Clinical Medicine, Section of Neuroscience and Cell Biology, Università Politecnica delle Marche, Torrette di Ancona, Ancona, Italy 60020
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Amy Bernard
5 Allen Institute for Brain Science, Seattle, Washington 98109
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Luisa de Vivo
2Department of Psychiatry, University of Wisconsin-Madison, Madison, Wisconsin 53719
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Chadd M. Funk
2Department of Psychiatry, University of Wisconsin-Madison, Madison, Wisconsin 53719
3Neuroscience Training Program, University of Wisconsin-Madison, Madison, Wisconsin 53705
6Medical Scientist Training Program, University of Wisconsin-Madison, Health Sciences Learning Center, Madison, Wisconsin 53705
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Julie Harris
5 Allen Institute for Brain Science, Seattle, Washington 98109
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Sakiko Honjoh
2Department of Psychiatry, University of Wisconsin-Madison, Madison, Wisconsin 53719
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Stefan Mihalas
5 Allen Institute for Brain Science, Seattle, Washington 98109
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Lydia Ng
5 Allen Institute for Brain Science, Seattle, Washington 98109
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Christof Koch
5 Allen Institute for Brain Science, Seattle, Washington 98109
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Chiara Cirelli
2Department of Psychiatry, University of Wisconsin-Madison, Madison, Wisconsin 53719
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Giulio Tononi
2Department of Psychiatry, University of Wisconsin-Madison, Madison, Wisconsin 53719
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    Figure 1.

    Experimental Timeline and MOs Projections. A, Experimental timeline. Between P25 and P30, mice were allowed to sleep normally (C) or subjected to CSR. All mice were injected with AAV-GFP between P44 and P47, and each mouse was perfused exactly 3 weeks later. Middle, Right, The location of the viral injections on the skull and in a coronal brain section. A, Anterior; P, posterior; D, dorsal; V ventral; B, bregma. B, Example of projections from MOs in two representative mice (C and CSR) 3 weeks after injection of AAV-GFP. Measurements are given in millimeters from bregma. Final analysis included 14 mice in each group.

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    Figure 2.

    Projection Fractions in Controls and CSR Mice. A, A plot of projection fractions (normalized by injection volume) across all mice (y-axis) and all regions (x-axis). B, Correlations of projection fraction patterns in mice with injection site. The mouse with the most extreme distance in injection location is taken as the basis for correlation (and is by definition equal to one). All regions were first normalized to have unit means to account for differences between injections. Without this normalization, the mean pairwise correlation of all animals is 0.903 ± 0.07. Distance in micrometers is measured to the center of the injection site from the midline (826 ± 140, left), the midline merging of the anterior commissure (1771 ± 262, middle) or the pial surface (636± 60, right). Values are given for Pearson’s rho. C, Left, Box plot of the condition influence, Embedded Image , of the GLM for all regions. A positive Embedded Image indicates that the control group has a higher connectivity than the CSR group (see Results for details). Right, An expanded version that is aligned and color-coded to match the subdivision in major anatomical regions.

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    Table 1.

    Statistics

    PropertyData StructureType of testp value
    Fig 2B: medial–lateral effect on injectionsNormally distributedStudent’s t test<0.0001
    Fig 2B: anterior–posterior effect on injectionsNormally distributedStudent’s t test0.004
    Fig 2B: dorsal–ventral effect on injectionsNormally distributedStudent’s t test0.796
    Control/CSR influence on connectivity (Embedded Image Embedded Image )Normality not assumedOne-tailed bootstrap0.252
    Males: control/CSR influence on connectivity (Embedded Image Embedded Image )Normality not assumedOne-tailed bootstrap0.491
    Females: control/CSR influence on connectivity (Embedded Image Embedded Image )Normality not assumedOne-tailed bootstrap0.258
    Control/CSR influence on weight (control > CSR)Normally distributedPaired t test<0.0001
    Control: male/female weight gain (male > female)Normally distributedPaired t test0.007
    CSR: male/female weight gain (male > female)Accuracy of classification algorithmNormally distributedBinomial distributedPaired t testBinomial cumulative distribution function test0.0080.0005
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    Table 2.

    List of brain regions

    Region no.Region abbreviationRegion nameRegion category
    1FRPFrontal pole, cerebral cortexIsocortex
    2MOpPrimary motor areaIsocortex
    3MOsSecondary motor areaIsocortex
    4SSp-nPrimary somatosensory area, noseIsocortex
    5SSp-bfdPrimary somatosensory area, barrel fieldIsocortex
    6SSp-llPrimary somatosensory area, lower limbIsocortex
    7SSp-mPrimary somatosensory area, mouthIsocortex
    8SSp-ulPrimary somatosensory area, upper limbIsocortex
    9SSp-trPrimary somatosensory area, trunkIsocortex
    10SSp-unPrimary somatosensory area, unassignedIsocortex
    11SSsSupplemental somatosensory areaIsocortex
    12GUGustatory areasIsocortex
    13VISCVisceral areaIsocortex
    14AUDdDorsal auditory areaIsocortex
    15AUDpPrimary auditory areaIsocortex
    16AUDpoPosterior auditory areaIsocortex
    17AUDvVentral auditory areaIsocortex
    18VISalAnterolateral visual areaIsocortex
    19VISamAnteromedial visual areaIsocortex
    20VISlLateral visual areaIsocortex
    21VISpPrimary visual areaIsocortex
    22VISplPosterolateral visual areaIsocortex
    23VISpmPosteromedial visual areaIsocortex
    24VISliIsocortex
    25VISporIsocortex
    26ACAdAnterior cingulate area, dorsal partIsocortex
    27ACAvAnterior cingulate area, ventral partIsocortex
    28PLPrelimbic areaIsocortex
    29ILAInfralimbic areaIsocortex
    30ORBlOrbital area, lateral partIsocortex
    31ORBmOrbital area, medial partIsocortex
    32ORBvlOrbital area, ventrolateral partIsocortex
    33AIdAgranular insular area, dorsal partIsocortex
    34AIpAgranular insular area, posterior partIsocortex
    35AIvAgranular insular area, ventral partIsocortex
    36RSPaglRetrosplenial area, lateral agranular partIsocortex
    37RSPdRetrosplenial area, dorsal partIsocortex
    38RSPvRetrosplenial area, ventral partIsocortex
    39VISaIsocortex
    40VISrlIsocortex
    41TEaTemporal association areasIsocortex
    42PERIPerirhinal areaIsocortex
    43ECTEctorhinal areaIsocortex
    45AOBAccessory olfactory bulbOlfactory areas
    46AONAnterior olfactory nucleusOlfactory areas
    47TTTaenia tectaOlfactory areas
    48DPDorsal peduncular areaOlfactory areas
    49PIRPiriform areaOlfactory areas
    50NLOTNucleus of the lateral olfactory tractOlfactory areas
    51COAaCortical amygdalar area, anterior partOlfactory areas
    57CA3Field CA3Hippocampal formation
    59FCFasciola cinereaHippocampal formation
    60IGInduseum griseumHippocampal formation
    61ENTlEntorhinal area, lateral partHippocampal formation
    65POSTPostsubiculumHippocampal formation
    66PREPresubiculumHippocampal formation
    67SUBSubiculumHippocampal formation
    68CLAClaustrumClaustrum + amygdala
    69EPdEndopiriform nucleus, dorsal partClaustrum + amygdala
    70EPvEndopiriform nucleus, ventral partClaustrum + amygdala
    71LALateral amygdalar nucleusClaustrum + amygdala
    72BLABasolateral amygdalar nucleusClaustrum + amygdala
    73BMABasomedial amygdalar nucleusClaustrum + amygdala
    74PAPosterior amygdalar nucleusClaustrum + amygdala
    75CPCaudoputamenStriatum + pallidum
    76ACBNucleus accumbensStriatum + pallidum
    77FSFundus of striatumStriatum + pallidum
    78OTOlfactory tubercleStriatum + pallidum
    79LScLateral septal nucleus, caudal (caudodorsal) partStriatum + pallidum
    80LSrLateral septal nucleus, rostral (rostroventral) partStriatum + pallidum
    83SHSeptohippocampal nucleusStriatum + pallidum
    84AAAAnterior amygdalar areaStriatum + pallidum
    86CEACentral amygdalar nucleusStriatum + pallidum
    87IAIntercalated amygdalar nucleusStriatum + pallidum
    88MEAMedial amygdalar nucleusStriatum + pallidum
    89GPeGlobus pallidus, external segmentStriatum + pallidum
    90GPiGlobus pallidus, internal segmentStriatum + pallidum
    91SISubstantia innominataStriatum + pallidum
    92MAMagnocellular nucleusStriatum + pallidum
    94NDBDiagonal band nucleusStriatum + pallidum
    96BSTBed nuclei of the stria terminalisStriatum + pallidum
    97BACBed nucleus of the anterior commissureStriatum + pallidum
    98VALVentral anterior-lateral complex of the thalamusThalamus
    99VMVentral medial nucleus of the thalamusThalamus
    100VPLVentral posterolateral nucleus of the thalamusThalamus
    101VPLpcVentral posterolateral nucleus of the thalamus, parvicellular partThalamus
    102VPMVentral posteromedial nucleus of the thalamusThalamus
    103VPMpcVentral posteromedial nucleus of the thalamus, parvicellular partThalamus
    104SPFmSubparafascicular nucleus, magnocellular partThalamus
    105SPFpSubparafascicular nucleus, parvicellular partThalamus
    106SPASubparafascicular areaThalamus
    107PPPeripeduncular nucleusThalamus
    108MGMedial geniculate complexThalamus
    110LPLateral posterior nucleus of the thalamusThalamus
    111POPosterior complex of the thalamusThalamus
    112POLPosterior limiting nucleus of the thalamusThalamus
    113SGNSuprageniculate nucleusThalamus
    114AVAnteroventral nucleus of thalamusThalamus
    115AMAnteromedial nucleusThalamus
    116ADAnterodorsal nucleusThalamus
    117IAMInteranteromedial nucleus of the thalamusThalamus
    118IADInteranterodorsal nucleus of the thalamusThalamus
    119LDLateral dorsal nucleus of thalamusThalamus
    120IMDIntermediodorsal nucleus of the thalamusThalamus
    121MDMediodorsal nucleus of thalamusThalamus
    122SMTSubmedial nucleus of the thalamusThalamus
    123PRPerireunensis nucleusThalamus
    124PVTParaventricular nucleus of the thalamusThalamus
    125PTParataenial nucleusThalamus
    126RENucleus of reunionsThalamus
    127RHRhomboid nucleusThalamus
    128CMCentral medial nucleus of the thalamusThalamus
    129PCNParacentral nucleusThalamus
    130CLCentral lateral nucleus of the thalamusThalamus
    131PFParafascicular nucleusThalamus
    132RTReticular nucleus of the thalamusThalamus
    133IGLIntergeniculate leaflet of the lateral geniculate complexThalamus
    134LGvVentral part of the lateral geniculate complexThalamus
    135SubGSubgeniculate nucleusThalamus
    137LHLateral habenulaThalamus
    138SOSupraoptic nucleusHypothalamus
    140PVHParaventricular hypothalamic nucleusHypothalamus
    142PViPeriventricular hypothalamic nucleus, intermediate partHypothalamus
    145AVPAnteroventral preoptic nucleusHypothalamus
    147DMHDorsomedial nucleus of the hypothalamusHypothalamus
    158VLPOVentrolateral preoptic nucleusHypothalamus
    160LMLateral mammillary nucleusHypothalamus
    161MMMedial mammillary nucleusHypothalamus
    162SUMSupramammillary nucleusHypothalamus
    163TMdTuberomammillary nucleus, dorsal partHypothalamus
    164TMvTuberomammillary nucleus, ventral partHypothalamus
    166PMdDorsal premammillary nucleusHypothalamus
    168PVHdParaventricular hypothalamic nucleus, descending divisionHypothalamus
    170PHPosterior hypothalamic nucleusHypothalamus
    171LHALateral hypothalamic areaHypothalamus
    172LPOLateral preoptic areaHypothalamus
    173PSTPreparasubthalamic nucleusHypothalamus
    174PSTNParasubthalamic nucleusHypothalamus
    176STNSubthalamic nucleusHypothalamus
    177TUTuberal nucleusHypothalamus
    178ZIZona incertaHypothalamus
    179SCsSuperior colliculus, sensory relatedMidbrain + pons
    180ICInferior colliculusMidbrain + pons
    181NBNucleus of the brachium of the inferior colliculusMidbrain + pons
    182SAGNucleus sagulumMidbrain + pons
    183PBGParabigeminal nucleusMidbrain + pons
    184MEVMidbrain trigeminal nucleusMidbrain + pons
    185SNrSubstantia nigra, reticular partMidbrain + pons
    186VTAVentral tegmental areaMidbrain + pons
    187RRMidbrain reticular nucleus, retrorubral areaMidbrain + pons
    188MRNMidbrain reticular nucleusMidbrain + pons
    189SCmSuperior colliculus, motor relatedMidbrain + pons
    190PAGPeriaqueductal grayMidbrain + pons
    191APNAnterior pretectal nucleusMidbrain + pons
    192MPTMedial pretectal areaMidbrain + pons
    193NOTNucleus of the optic tractMidbrain + pons
    194NPCNucleus of the posterior commissureMidbrain + pons
    195OPOlivary pretectal nucleusMidbrain + pons
    196PPTPosterior pretectal nucleusMidbrain + pons
    197CUNCuneiform nucleusMidbrain + pons
    198RNRed nucleusMidbrain + pons
    199IIIOculomotor nucleusMidbrain + pons
    200EWEdinger–Westphal nucleusMidbrain + pons
    201IVTrochlear nucleusMidbrain + pons
    202VTNVentral tegmental nucleusMidbrain + pons
    203ATAnterior tegmental nucleusMidbrain + pons
    204LTLateral terminal nucleus of the accessory optic tractMidbrain + pons
    205SNcSubstantia nigra, compact partMidbrain + pons
    206PPNPedunculopontine nucleusMidbrain + pons
    207IFInterfascicular nucleus rapheMidbrain + pons
    208IPNInterpeduncular nucleusMidbrain + pons
    209RLRostral linear nucleus rapheMidbrain + pons
    210CLICentral linear nucleus rapheMidbrain + pons
    211DRDorsal nucleus rapheMidbrain + pons
    212NLLNucleus of the lateral lemniscusMidbrain + pons
    213PSVPrincipal sensory nucleus of the trigeminalMidbrain + pons
    214PBParabrachial nucleusMidbrain + pons
    215SOCSuperior olivary complexMidbrain + pons
    216BBarringtons nucleusMidbrain + pons
    217DTNDorsal tegmental nucleusMidbrain + pons
    218PCGPontine central grayMidbrain + pons
    219PGPontine grayMidbrain + pons
    220PRNcPontine reticular nucleus, caudal partMidbrain + pons
    221SGSupragenual nucleusMidbrain + pons
    222SUTSupratrigeminal nucleusMidbrain + pons
    223TRNTegmental reticular nucleusMidbrain + pons
    224VMotor nucleus of trigeminalMidbrain + pons
    225CSSuperior central nucleus rapheMidbrain + pons
    226LCLocus ceruleusMidbrain + pons
    227LDTLaterodorsal tegmental nucleusMidbrain + pons
    228NINucleus incertusMidbrain + pons
    229PRNrPontine reticular nucleusMidbrain + pons
    230RPONucleus raphe pontisMidbrain + pons
    231SLCSubceruleus nucleusMidbrain + pons
    232SLDSublaterodorsal nucleusMidbrain + pons
    236CUCuneate nucleusMedulla
    239NTBNucleus of the trapezoid bodyMedulla
    240NTSNucleus of the solitary tractMedulla
    241SPVCSpinal nucleus of the trigeminal, caudal partMedulla
    242SPVISpinal nucleus of the trigeminal, interpolar partMedulla
    243SPVOSpinal nucleus of the trigeminal, oral partMedulla
    244VIAbducens nucleusMedulla
    245VIIFacial motor nucleusMedulla
    246ACVIIAccessory facial motor nucleusMedulla
    247AMBNucleus ambiguusMedulla
    248DMXDorsal motor nucleus of the vagus nerveMedulla
    249GRNGigantocellular reticular nucleusMedulla
    250ICBInfracerebellar nucleusMedulla
    251IOInferior olivary complexMedulla
    252IRNIntermediate reticular nucleusMedulla
    253ISNInferior salivatory nucleusMedulla
    254LINLinear nucleus of the medullaMedulla
    255LRNLateral reticular nucleusMedulla
    256MARNMagnocellular reticular nucleusMedulla
    257MDRNdMedullary reticular nucleus, dorsal partMedulla
    258MDRNvMedullary reticular nucleus, ventral partMedulla
    259PARNParvicellular reticular nucleusMedulla
    260PASParasolitary nucleusMedulla
    261PGRNdParagigantocellular reticular nucleus, dorsal partMedulla
    262PGRNlParagigantocellular reticular nucleus, lateral partMedulla
    263NRNucleus of RollerMedulla
    264PRPNucleus prepositusMedulla
    265PPYParapyramidal nucleusMedulla
    266LAVLateral vestibular nucleusMedulla
    267MVMedial vestibular nucleusMedulla
    268SPIVSpinal vestibular nucleusMedulla
    269SUVSuperior vestibular nucleusMedulla
    270xNucleus xMedulla
    271XIIHypoglossal nucleusMedulla
    272yNucleus yMedulla
    273RMNucleus raphe magnusMedulla
    274RPANucleus raphe pallidusMedulla
    275RONucleus raphe obscurusMedulla
    290FNFastigial nucleusCerebellum
    291IPInterposed nucleusCerebellum
    292DNDentate nucleusCerebellum
    293fiber tractsFiber tractsFiber tracts
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Effects of Chronic Sleep Restriction during Early Adolescence on the Adult Pattern of Connectivity of Mouse Secondary Motor Cortex
Yazan N. Billeh, Alexander V. Rodriguez, Michele Bellesi, Amy Bernard, Luisa de Vivo, Chadd M. Funk, Julie Harris, Sakiko Honjoh, Stefan Mihalas, Lydia Ng, Christof Koch, Chiara Cirelli, Giulio Tononi
eNeuro 22 April 2016, 3 (2) ENEURO.0053-16.2016; DOI: 10.1523/ENEURO.0053-16.2016

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Effects of Chronic Sleep Restriction during Early Adolescence on the Adult Pattern of Connectivity of Mouse Secondary Motor Cortex
Yazan N. Billeh, Alexander V. Rodriguez, Michele Bellesi, Amy Bernard, Luisa de Vivo, Chadd M. Funk, Julie Harris, Sakiko Honjoh, Stefan Mihalas, Lydia Ng, Christof Koch, Chiara Cirelli, Giulio Tononi
eNeuro 22 April 2016, 3 (2) ENEURO.0053-16.2016; DOI: 10.1523/ENEURO.0053-16.2016
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Keywords

  • adolescence
  • sensitive period
  • secondary motor cortex
  • sleep loss

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