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Anterior–posterior dissociation of the default mode network in dogs

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Abstract

The default mode network (DMN) in humans has been extensively studied using seed-based correlation analysis (SCA) and independent component analysis (ICA). While DMN has been observed in monkeys as well, there are conflicting reports on whether they exist in rodents. Dogs are higher mammals than rodents, but cognitively not as advanced as monkeys and humans. Therefore, they are an interesting species in the evolutionary hierarchy for probing the comparative functions of the DMN across species. In this study, we sought to know whether the DMN, and consequently its functions such as self-referential processing, are exclusive to humans/monkeys or can we also observe the DMN in animals such as dogs. To address this issue, resting state functional MRI data from the brains of lightly sedated dogs and unconstrained and fully awake dogs were acquired, and ICA and SCA were performed for identifying the DMN. Since anesthesia can alter resting state networks, confirming our results in awake dogs was essential. Awake dog imaging was accomplished by training the dogs to keep their head still using reinforcement behavioral adaptation techniques. We found that the anterior (such as anterior cingulate and medial frontal) and posterior regions (such as posterior cingulate) of the DMN were dissociated in both awake and anesthetized dogs.

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References

  • Andrews-Hanna JR et al (2007) Disruption of large-scale brain systems in advanced aging. Neuron 56(5):924–935

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ashburner J, Friston KJ (1999) Nonlinear spatial normalization using basis functions. Human Brain Mapp 7:254–266

    Article  CAS  Google Scholar 

  • Auer DP (2008) Spontaneous low-frequency blood oxygenation level-dependent fluctuations and functional connectivity analysis of the ‘resting’ brain. Magn Reson Imaging 26(7):1055–1064

    Article  PubMed  Google Scholar 

  • Becerra L, Pendse G, Chang P-C, Bishop J, Borsook D (2011) Robust reproducible resting state networks in the awake rodent brain. PloS One 6(10):e25701. doi:10.1371/journal.pone.0025701

  • Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360:1001–1013

    Article  PubMed Central  PubMed  Google Scholar 

  • Bell AJ, Sejnowski TJ (1995) An information-maximization approach to blind separation and blind deconvolution. Neural Comput 7(6):1129–1159

    Article  CAS  PubMed  Google Scholar 

  • Berns G, Brooks A, Spivak M (2012) Functional MRI in awake unrestrained dogs. PloS One 7(5):e38027. doi:10.1371/journal.pone.0038027

  • Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541

    Article  CAS  PubMed  Google Scholar 

  • Bluhm RL et al (2008) Default mode network connectivity: effects of age, sex, and analytic approach. NeuroReport 19(8):887–891

    Article  PubMed  Google Scholar 

  • Bokde AL et al (2006) Functional connectivity of the fusiform gyrus during a face-matching task in subjects with mild cognitive impairment. Brain 129:1113–1124

    Article  CAS  PubMed  Google Scholar 

  • Bonnelle V et al (2011) Default mode network connectivity predicts sustained attention deficits after traumatic brain injury. J Neurosci 31(38):13442–13451

    Article  CAS  PubMed  Google Scholar 

  • Brant-Zawadzki M, Gillan GD, Nitz WR (1992) MP RAGE: a three-dimensional, T1-weighted, gradient-echo sequence–initial experience in the brain. Radiology 182:769–775

    Article  CAS  PubMed  Google Scholar 

  • Brown GD, Yamada S, Sejnowski TJ (2001) Independent component analysis at the neural cocktail party. Trends Neurosci 24(1):54–63

    Article  CAS  PubMed  Google Scholar 

  • Buckner RL, Carroll DC (2007) Self-projection and the brain. Trends Cogn Sci 11(2):49–57

    Article  PubMed  Google Scholar 

  • Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain’s default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1–38

    Article  PubMed  Google Scholar 

  • Butts K, Riederer SJ, Ehman RL, Thompson RM, Jack CR (1994) Interleaved echo planar imaging on a standard MRI system. Magn Reson Med 31:67–72

    Article  CAS  PubMed  Google Scholar 

  • Calhoun VD, Adali T, Pearlson GD, Pekar JJ (2001) A method for making group inferences from functional MRI data using independent component analysis. Human Brain Mapp 14(3):140–151

    Article  CAS  Google Scholar 

  • Calhoun VD, Kiehl KA, Pearlson GD (2008) Modulation of temporally coherent brain networks estimated using ICA at rest and during cognitive tasks. Human Brain Mapp 29(7):828–838

    Article  Google Scholar 

  • Castellanos FX et al (2008) Cingulate-precuneus interactions: a new locus of dysfunction in adult attention-deficit/hyperactivity disorder. Biol Psychiatry 63:332–337

    Article  PubMed Central  PubMed  Google Scholar 

  • Chao-Gan Y, Yu-Feng Z (2010) DPARSF: A MATLAB Toolbox for “Pipeline” Data Analysis of Resting-State fMRI.” Frontiers Syst Neurosci 4(13). doi:10.3389/fnsys.2010.00013

  • Cole, DM, Smith SM, Beckmann CF (2010) Advances and pitfalls in the analysis and interpretation of resting-state FMRI data. Frontiers Syst Neurosci 4(8). doi:10.3389/fnsys.2010.00008

  • Cordes D, Haughton VM, Arfanakis K, Wendt GJ, Turski PA (2000) Mapping functionally related regions of brain with functional connectivity. Am J Neuroradiol 21(9):1636–1644

    CAS  PubMed  Google Scholar 

  • Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103:13848–13853

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Damoiseaux JS et al (2008) Reduced resting-state brain activity in the ‘‘default network’’ in normal aging. Cereb Cortex 18(8):1856–1864

    Article  CAS  PubMed  Google Scholar 

  • Danielson NB, Guo JN, Blumenfeld H (2011) The default mode network and altered consciousness in epilepsy. Behav Neurol 24(1):55–65

    Article  PubMed Central  PubMed  Google Scholar 

  • Datta R et al (2012) A digital atlas of the dog brain. PLoS ONE 7(12):e52140

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Deshpande G, Santhanam P, Hu X (2011) Instantaneous and causal connectivity in resting state brain networks derived from functional MRI data. Neuroimage 54(2):1043–1052

    Article  PubMed Central  PubMed  Google Scholar 

  • Esposito F et al (2009) Does the default-mode functional connectivity of the brain correlate with working-memory performances? Arch Ital Biol 147(1–2):11–20

    CAS  PubMed  Google Scholar 

  • Fair DA et al (2009) Functional brain networks develop from a “local to distributed” organization.” PLoS Comput Biol 5(5):e1000381

    Google Scholar 

  • Fornito A, Bullmore ET (2010) What can spontaneous fluctuations of the blood oxygenation-level-dependent signal tell us about psychiatric disorders? Curr Opin Psychiatry 23(3):239–249

    Article  PubMed  Google Scholar 

  • Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711

    Article  CAS  PubMed  Google Scholar 

  • Fransson P et al (2007) Resting-state networks in the infant brain. Proc Natl Acad Sci USA 104(39):15531–15536

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith C, Frackowiak J (1995) Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapp 2(4):189–210

    Article  Google Scholar 

  • Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R (1996) Movement-related effects in fMRI time-series. Magn Reson Med 35(3):346–355

    Article  CAS  PubMed  Google Scholar 

  • George MS, Ketter TA, Parekh PI, Horwitz B, Herscovitch P, Post RM (1995) Brain activity during transient sadness and happiness in healthy women. Am J Psychiatry 152(3):341–351

    Article  CAS  PubMed  Google Scholar 

  • George MS, Ketter TA, Parekh PI, Herscovitch P, Post RM (1996) Gender differences in regional cerebral blood flow during transient self-induced sadness or happiness. Biol Psychiatry 40(9):859–871

    Article  CAS  PubMed  Google Scholar 

  • Gilbert DT, Wilson TD (2007) Prospection: experiencing the future. Science 317(5843):1351–1354

    Article  CAS  PubMed  Google Scholar 

  • Greicius M (2008) Resting-state functional connectivity in neuropsychiatric disorders. Curr Opin Neurol 21:424–430

    Article  PubMed  Google Scholar 

  • Greicius MD, Krasnow B, Reiss AL, Menon V (2003) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 100:253–258

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Greicius MD, Srivastava G, Reiss AL, Menon V (2004) Default-mode network activity distinguishes Alzheimer’s disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci USA 101:4637–4642

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Greicius MD et al (2007) Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol Psychiatry 62:429–437

    Article  PubMed Central  PubMed  Google Scholar 

  • Greicius MD et al (2008) Persistent default-mode network connectivity during light sedation. Hum Brain Mapp 29(7):839–847

    Article  PubMed Central  PubMed  Google Scholar 

  • Gusnard DA, Raichle ME (2001) Searching for a baseline: functional imaging and the resting human brain. Nat Rev Neurosci 2:685–694

    Article  CAS  PubMed  Google Scholar 

  • Hampson M, Driesen NR, Skudlarski P, Gore JC, Constable RT (2006) Brain connectivity related to working memory performance. J Neurosci 26(51):13338–13343

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harrison BJ et al (2008) Consistency and functional specialization in the default mode brain network. Proc Natl Acad Sci USA 105(28):9781–9786

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Johnson SC, Baxter LC, Wilder LS, Pipe JG, Heiserman JE, Prigatano GP (2002) Neural correlates of self-reflection. Brain 125(Pt 8):1808–1814

    Article  PubMed  Google Scholar 

  • Knyazev GG (2012) Extraversion and anterior vs. posterior DMN activity during self-referential thoughts. Frontiers Human Neurosci 6(348). doi:10.3389/fnhum.2012.00348

  • Leech R, Kamourieh S, Beckmann CF, Sharp DJ (2011) Fractionating the default mode network: distinct contributions of the ventral and dorsal posterior cingulate cortex to cognitive control. J Neurosci 31(9):3217–3224

    Article  CAS  PubMed  Google Scholar 

  • Lei X, Zhao Z, Chen H (2013) Extraversion is encoded by scale-free dynamics of default mode network. Neuroimage 74:52–57

    Article  PubMed  Google Scholar 

  • Liang Z, King J, Zhang N (2011) Uncovering intrinsic connectional architecture of functional networks in awake rat brain. J Neurosci 31(10):3776–3783

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412(6843):150–157

    Article  CAS  PubMed  Google Scholar 

  • Long XY et al (2008) Default mode network as revealed with multiple methods for resting-state functional MRI analysis. J Neurosci Methods 171(2):349–355

    Article  PubMed  Google Scholar 

  • Lou HC et al (2004) Parietal cortex and representation of the mental Self. Proc Natl Acad Sci USA 101(17):6827–6832

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lu H et al (2007) Synchronized delta oscillations correlate with the resting-state functional MRI signal. Proc Natl Acad Sci USA 104(46):18265–18269

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lu H, Zou Q, Gu H, Raichle ME, Steina EA, Yanga Y (2011) Rat brains also have a default mode network. Proc Natl Acad Sci USA 109(10):3979–3984

    Article  Google Scholar 

  • Lundstrom BN, Ingvar M, Petersson KM (2005) The role of precuneus and left inferior frontal cortex during source memory episodic retrieval. Neuroimage 27(4):824–834

    Article  PubMed  Google Scholar 

  • Ma L, Wang B, Chen X, Xiong J (2007) Detecting functional connectivity in the resting brain: a comparison between ICA and CCA. Magn Reson Imaging 25(1):47–56

    Article  PubMed  Google Scholar 

  • Mantini D et al (2011) Default mode of brain function in monkeys. J Neurosci 31(36):12954–12962

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mayberg HS et al (1999) Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry 156(5):675–682

    CAS  PubMed  Google Scholar 

  • Mitchell JP, Heatherton T, Macrae CN (2002) Distinct neural systems subserve person and object knowledge. Proc Natl Acad Sci USA 99(23):15238–15243

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Neafsey EJ, Terreberry RR, Hurley KM, Ruit KG, Frysztak RJ (1993) Anterior cingulate cortex in rodents: connections, visceral control functions, and implications for emotion. In: Vogt BA, Gabriel M (eds) Neurobiology of cingulate cortex and limbic thalamus. Birkhäuser, Boston, pp 207–223

    Google Scholar 

  • Northoff G, Heinzel A, de Greck M, Bermpohl F, Dobrowolny H, Panksepp J (2006) Self-referential processing in our brain–a meta-analysis of imaging studies on the self. Neuroimage 31(1):440–457

    Article  PubMed  Google Scholar 

  • Phan KL, Wager T, Taylor SF, Liberzon I (2002) Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16(2):331–348

    Article  PubMed  Google Scholar 

  • Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci USA 98:676–682

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rombouts S, Scheltens P (2005) Functional connectivity in elderly controls and AD patients using resting state fMRI: a pilot study. Curr Alzheimer Res 2:115–116

    Article  CAS  PubMed  Google Scholar 

  • Seeley WW et al (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27(9):2349–2356

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shattuck DW, Leahy RM (2002) BrainSuite: an automated cortical surface identification tool. Medical Image Anal 6(2):129–142

    Article  Google Scholar 

  • Song X-W et al (2011) REST: A toolkit for resting-state functional magnetic resonance imaging data processing. PloS One 6(9):e25031. doi:10.1371/journal.pone.0025031

  • Stamatakis EA, Adapa RM, Absalom AR, Menon DK (2010) Changes in resting neural connectivity during propofol sedation. PloS One 5(12):e14224

    Google Scholar 

  • Supekar K, Uddin LQ, Prater K, Amin H, Greicius MD, Menon V (2010) Development of functional and structural connectivity within the default mode network in young children. Neuroimage 52(1):290–301

    Article  PubMed Central  PubMed  Google Scholar 

  • Tian L et al (2006) Altered resting-state functional connectivity patterns of anterior cingulate cortex in adolescents with attention deficit hyperactivity disorder. Neurosci Lett 400:39–43

    Article  CAS  PubMed  Google Scholar 

  • Upadhyay J et al (2011) Default-mode-like network activation in awake rodents. PloS One 6(11):e27839

    Google Scholar 

  • Van den Heuvel MP, Hulshoff Pol HE (2010) Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 20:519–534

    Article  PubMed  Google Scholar 

  • Van den Heuvel MP, Mandl RC, Luigjes J, Pol Hulshoff HE (2008a) Microstructural organization of the cingulum tract and the level of default mode functional connectivity. J Neurosci 28(43):10844–10851

    Article  PubMed  Google Scholar 

  • Van den Heuvel MP, Mandl RC, HulshoffPol HE (2008b) Normalized group clustering of resting-state fMRI data. PloS One 3(4):e2001

    Google Scholar 

  • Vogt BA, Vogt L, Laureys S (2006) Cytology and functionally correlated circuits of human posterior cingulate areas. Neuroimage 29(2):452–466

    Article  PubMed Central  PubMed  Google Scholar 

  • Wager TD, Phan KL, Liberzon I, Taylor SF (2003) Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging. Neuroimage 19(3):513–531

    Google Scholar 

  • Wang K et al (2011) Temporal scaling properties and spatial synchronization of spontaneous blood oxygenation level-dependent (BOLD) signal fluctuations in rat sensorimotor network at different levels of isoflurane anesthesia. NMR Biomed 24(1):61–67

    Article  PubMed  Google Scholar 

  • Wei L et al (2011) The synchronization of spontaneous BOLD activity predicts extraversion and neuroticism. Brain Res 1419:68–75

    Article  CAS  PubMed  Google Scholar 

  • Whalley HC et al (2005) Functional disconnectivity in subjects at high genetic risk of schizophrenia. Brain 128:2097–2108

    Article  PubMed  Google Scholar 

  • Yang Z et al (2012) Generalized RAICAR: discover homogeneous subject (sub)groups by reproducibility of their intrinsic connectivity networks. Neuroimage 63(1):403–414

    Article  PubMed  Google Scholar 

  • Zhang N et al (2010) Mapping resting-state brain networks in conscious animals. J Neurosci Methods 189(2):186–196

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank Yang Zhi from National Institutes of Health for providing gRAICAR code and assisting with its analysis. The authors acknowledge financial support for this work from Auburn University Intramural Level-3 research grant from the Office of the Vice President for Research, Auburn University. This work was also supported by The Defense Advanced Research Projects Agency (government contract/grant number W911QX-13-C-0123). The views, opinions, and/or findings contained in this article are those of the authors and should not be interpreted as representing the official views or policies, either expressed or implied, of the Defense Advanced Research Projects Agency, Department of Defense or the United States Government.

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Authors and Affiliations

  1. AU MRI Research Center, Department of Electrical and Computer Engineering, Auburn University, Auburn, AL, USA

    Sreenath P. Kyathanahally, Hao Jia, Ronald Beyers, Nouha Salibi, Thomas S. Denney & Gopikrishna Deshpande

  2. Department of Anatomy, Physiology and Pharmacology, Auburn University, Auburn, AL, USA

    Oleg M. Pustovyy, Edward E. Morrison & Vitaly J. Vodyanoy

  3. Canine Detection Research Institute, Auburn University, Auburn, AL, USA

    Paul Waggoner

  4. Department of Clinical Sciences, Auburn University, Auburn, AL, USA

    John Schumacher

  5. College of Veterinary Medicine, Auburn University, Auburn, AL, USA

    Jay Barrett

  6. MR R&D, Siemens Healthcare, Malvern, PA, USA

    Nouha Salibi

  7. Department of Psychology, Auburn University, Auburn, AL, USA

    Thomas S. Denney & Gopikrishna Deshpande

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  1. Sreenath P. Kyathanahally
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  2. Hao Jia
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Correspondence to Gopikrishna Deshpande.

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Kyathanahally, S.P., Jia, H., Pustovyy, O.M. et al. Anterior–posterior dissociation of the default mode network in dogs. Brain Struct Funct 220, 1063–1076 (2015). https://doi.org/10.1007/s00429-013-0700-x

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