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Intrinsic functional architecture in the anaesthetized monkey brain

Nature volume 447, pages 8386 (03 May 2007) | Download Citation

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Abstract

The traditional approach to studying brain function is to measure physiological responses to controlled sensory, motor and cognitive paradigms. However, most of the brain’s energy consumption is devoted to ongoing metabolic activity not clearly associated with any particular stimulus or behaviour1. Functional magnetic resonance imaging studies in humans aimed at understanding this ongoing activity have shown that spontaneous fluctuations of the blood-oxygen-level-dependent signal occur continuously in the resting state. In humans, these fluctuations are temporally coherent within widely distributed cortical systems that recapitulate the functional architecture of responses evoked by experimentally administered tasks2,3,4,5,6. Here, we show that the same phenomenon is present in anaesthetized monkeys even at anaesthetic levels known to induce profound loss of consciousness. We specifically demonstrate coherent spontaneous fluctuations within three well known systems (oculomotor, somatomotor and visual) and the ‘default’ system, a set of brain regions thought by some to support uniquely human capabilities. Our results indicate that coherent system fluctuations probably reflect an evolutionarily conserved aspect of brain functional organization that transcends levels of consciousness.

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References

  1. 1.

    & Brain work and brain imaging. Annu. Rev. Neurosci. 29, 449–476 (2006)

  2. 2.

    , , & Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537–541 (1995)

  3. 3.

    et al. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl Acad. Sci. USA 102, 9673–9678 (2005)

  4. 4.

    , , & Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl Acad. Sci. USA 100, 253–258 (2003)

  5. 5.

    et al. Consistent resting-state networks across healthy subjects. Proc. Natl Acad. Sci. USA 103, 13848–13853 (2006)

  6. 6.

    et al. Coherent spontaneous activity identifies a hippocampal-parietal memory network. J. Neurophysiol. 96, 3517–3531 (2006)

  7. 7.

    & Does the brain have a baseline? Why we should be resisting a rest. Neuroimage (in the press)

  8. 8.

    , , , & Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. Proc. Natl Acad. Sci. USA 103, 10046–10051 (2006)

  9. 9.

    , , & Distribution of activity across the monkey cerebral cortical surface, thalamus and midbrain during rapid, visually guided saccades. Cereb. Cortex 16, 447–459 (2006)

  10. 10.

    & Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J. Comp. Neurol. 428, 112–137 (2000)

  11. 11.

    & Topographic organization of the middle temporal visual area in the macaque monkey: representational biases and the relationship to callosal connections and myeloarchitectonic boundries. J. Comp. Neurol. 266, 535–555 (1987)

  12. 12.

    , & The pattern of interhemispheric connections and its relationship to extrastriate visual areas in the macaque monkey. J. Neurosci. 2, 265–283 (1982)

  13. 13.

    et al. A default mode of brain function. Proc. Natl Acad. Sci. USA 98, 676–682 (2001)

  14. 14.

    & People thinking about thinking people. The role of the temporo-parietal junction in “theory of mind”. Neuroimage 19, 1835–1842 (2003)

  15. 15.

    & Neural correlates of the first-person-perspective. Trends Cogn. Sci. 7, 38–42 (2003)

  16. 16.

    , , , & An fMRI investigation of emotional engagement in moral judgment. Science 293, 2105–2108 (2001)

  17. 17.

    , , & Parietal lobe contributions to episodic memory retrieval. Trends Cogn. Sci. 9, 445–453 (2005)

  18. 18.

    , & Remembering the past and imagining the future: Common and distinct neural substrates during event construction and elaboration. Neuropsychologia 45, 1363–1377 (2007)

  19. 19.

    in The Missing Link in Cognition: Origins of Self-Reflective Consciousness (eds Terrace, H. S. & Metcalfe, J.) 3–56 (Oxford Univ. Press, New York, 2005).

  20. 20.

    & Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. J. Comp. Neurol. 350, 497–533 (1994)

  21. 21.

    New insights into the functions of the superior temporal cortex. Nature Rev. Neurosci. 2, 568–576 (2001)

  22. 22.

    Localisation in the Cerebral Cortex (Smith-Gordon, London, 1994)

  23. 23.

    , , & Internal dynamics determine the cortical response to thalamic stimulation. Neuron 48, 811–823 (2005)

  24. 24.

    I of the Vortex: From Neurons to Self (MIT Press, Cambridge, Massachusetts, 2001)

  25. 25.

    & Neuronal oscillations in cortical networks. Science 304, 1926–1929 (2004)

  26. 26.

    , , , & Spontaneously emerging cortical representations of visual attributes. Nature 425, 954–956 (2003)

  27. 27.

    Neuroscience. The brain’s dark energy. Science 314, 1249–1250 (2006)

  28. 28.

    , & Small modulation of ongoing cortical dynamics by sensory input during natural vision. Nature 431, 573–578 (2004)

  29. 29.

    , & The visual field representation in striate cortex of the macaque monkey: asymmetries, anisotropies, and individual variability. Vision Res. 24, 429–448 (1984)

  30. 30.

    , & Visuotopic organization and extent of V3 and V4 of the macaque. J. Neurosci. 8, 1831–1845 (1988)

  31. 31.

    , , & Atlas template images for nonhuman primate neuroimaging: baboon and macaque. Methods Enzymol. 385, 91–102 (2004)

  32. 32.

    , & Template images for neuroimaging in Macaca fascicularis. Program No. 454.18. Abstract Viewer and Itinerary Planner 〈〉 (Society for Neuroscience, Washington DC, 2005)

  33. 33.

    , , & Moving GLM ballistocardiogram artifact reduction for EEG data acquired simultaneously with fMRI. Clin. Neurophysiol. 118, 981–998 (2007)

  34. 34.

    et al. Anatomic localization and quantitative analysis of gradient refocused echo-planar fMRI susceptibility artifacts. Neuroimage 6, 156–167 (1997)

  35. 35.

    & Primate Brain Maps: Structure of the Macaque Brain (Elsevier, Amsterdam, 2000)

  36. 36.

    & Co-planar Stereotaxic Atlas of the Human Brain (Thieme Medical Publishers, New York, 1988)

  37. 37.

    et al. A modality-independent approach to spatial normalization of tomographic images of the human brain. Hum. Brain Mapp. 3, 209–223 (1995)

  38. 38.

    & Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipital cortex. J. Comp. Neurol. 428, 79–111 (2000)

  39. 39.

    et al. Common blood flow changes across visual tasks: II. Decreases in cerebral cortex. J. Cogn. Neurosci. 9, 648–663 (1997)

  40. 40.

    Biostatistical Analysis (Prentice-Hall, Upper Saddle River, New Jersey, 1996)

  41. 41.

    & Spectral Analysis and its Applications (Emerson-Adams Press, Boca Raton, 1968)

  42. 42.

    et al. A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage 23, 724–738 (2004)

  43. 43.

    et al. An integrated software suite for surface-based analyses of cerebral cortex. J. Am. Med. Inform. Assoc. 8, 443–459 (2001)

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Acknowledgements

We thank J. L. Price, J. S. Perlmutter and G. C. DeAngelis for discussion and for allowing us to scan their monkeys; L. J. Larson-Prior for providing the human data; J. Harwell for Caret software enhancements used in data analysis; and K. J. Black for providing the monkey atlas target. Grants from the US National Institute of Health, US National Science Foundation, Washington University Silvio Conte Center, and Mallinckrodt Institute of Radiology supported these studies.

Author information

Affiliations

  1. Departments of Radiology,

    • J. L. Vincent
    • , G. H. Patel
    • , M. D. Fox
    • , A. Z. Snyder
    • , M. Corbetta
    •  & M. E. Raichle
  2. Neurology,

    • G. H. Patel
    • , A. Z. Snyder
    • , J. M. Zempel
    • , M. Corbetta
    •  & M. E. Raichle
  3. Anatomy and Neurobiology, and,

    • G. H. Patel
    • , J. T. Baker
    • , D. C. Van Essen
    • , L. H. Snyder
    • , M. Corbetta
    •  & M. E. Raichle
  4. Biomedical Engineering, Washington University in St Louis, Missouri 63110, USA

    • M. E. Raichle
  5. Department of Psychology, Center for Brain Science, Harvard University, Cambridge, Massachusetts 02138, USA

    • J. L. Vincent
  6. Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, Massachusetts 02129, USA

    • J. L. Vincent

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Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Corresponding author

Correspondence to M. E. Raichle.

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https://doi.org/10.1038/nature05758

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