Review
The connectome
Neural correlates of establishing, maintaining, and switching brain states

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Although the study of brain states is an old one in neuroscience, there has been growing interest in brain state specification owing to MRI studies tracing brain connectivity at rest. In this review, we summarize recent research on three relatively well-described brain states: the resting, alert, and meditation states. We explore the neural correlates of maintaining a state or switching between states, and argue that the anterior cingulate cortex and striatum play a critical role in state maintenance, whereas the insula has a major role in switching between states. Brain state may serve as a predictor of performance in a variety of perceptual, memory, and problem solving tasks. Thus, understanding brain states is critical for understanding human performance.

Section snippets

Brain state

The ability to maintain a brain state (see Glossary) and to switch between states is vital for self-regulation and for adapting to the varying environments that humans occupy. Brain states refer to reliable patterns of brain activity that involve the co-activation and/or connectivity of multiple large-scale brain networks. In infancy, for example, sleep, wakefulness, passive and active alertness, and crying have usually been seen as ranging along a continuum of different levels of arousal [1].

The resting state

Human studies using fMRI have traditionally focused on task-evoked responses. In the past decade, however, the patterns of activity of the human brain during non-task processes (i.e., at rest) have become a focus of several studies 5, 6, 8, 9, 10. In experimental settings, the resting state follows an instruction to lie quietly, relax, and not carry out any task; the eyes may be closed or open, and either fixated or not. Although the resting state does not involve an external task, it shows

The alert state

One important approach to understanding state transitions is to address their relation to slow waves found in electrophysiological recordings. Slow waves, such as the contingent negative variation (CNV), are closely related to aspects of fMRI, since both result from synaptic activity that produces local field potentials 8, 26, 27. The influence of a warning signal on brain activation patterns allows study of the rapid transition to the high levels of alertness needed for rapid and efficient

The meditation state

Unlike the alert state, meditation requires specific training. It is, therefore, difficult to separate the meditation state from the training that produces it. There are many forms of meditation practice, including transcendental meditation, Buddhist meditation, mindfulness meditation, and others 42, 43, 44, 45. Whether the state induced by these various forms of training is the same is not known, so it is difficult to describe a meditation state independent of the training needed to reach it.

Neural correlates of brain state control

Following earlier proposals 76, 77, we hypothesize that the control of brain states includes the two components of switching and maintenance 76, 77. These two components are also present in the transition from rest to alertness and may be general characteristics of state control induced by instruction. The initial response to a warning signal involves an active voluntary response orchestrated by frontal areas including the ACC [30], whereas continued maintenance involves a direct current shift

The alert state and the meditation state

The three brain states are compared in Table 1. The meditation state differs from the alert state induced by a warning signal in several crucial ways. First, the alert state can be induced by the simple instruction to expect a target, without requiring any practice, whereas the meditation state requires specific instruction and practice. Second, the alert state requires an external target, whereas the meditation state may not involve a target event. Third, the alert state involves primarily the

Future directions and applications

In this review, we have examined three brain states: the resting, alert and meditative states. We now consider the significance of understanding these states and suggest directions for future research (Box 2).

Resting state data have been widely applied to the study of normal development 17, 18, 19, 20 and to a variety of neuropsychiatric disorders, including schizophrenia, anxiety, and autism 21, 22. Making use of the ability to image the connectivity of the brain's resting state will continue

Acknowledgements

We would like to thank Rongxiang Tang for assistance with artwork on all figures. This work was supported by 973 Program 2012CB518200, the Office of Naval Research, and NIH grants HD 060563 and R21DA030066 (to Y.Y.T. and M.I.P.).

Glossary

Alert state
the brain state that follows a warning related to a target event requiring a rapid response.
Brain state
the reliable patterns of brain activity that involve the activation and/or connectivity of multiple large-scale brain networks.
Contingent Negative Variation (CNV)
a negative direct current shift in electrophysiological recordings that occurs when a warning signal leads one to prepare for an upcoming target.
Default Mode Network (DMN)
a brain network that includes the medial prefrontal

References (93)

  • R.T. Marrocco

    Arousal systems

    Curr. Opin. Neurobiol.

    (1994)
  • K.C. Berridge et al.

    Parsing reward

    Trends Neurosci.

    (2003)
  • A. Lutz

    Attention regulation and monitoring in meditation

    Trends Cogn. Sci.

    (2008)
  • F. Travis et al.

    Focused attention, open monitoring and automatic self-transcending: Categories to organize meditations from Vedic, Buddhist and Chinese traditions

    Conscious. Cogn.

    (2010)
  • Y.Y. Tang et al.

    Attention training and attention state training

    Trends Cogn. Sci.

    (2009)
  • M. Roy

    Ventromedial prefrontal-subcortical systems and the generation of affective meaning

    Trends Cogn. Sci.

    (2012)
  • W. Hasenkamp

    Mind wandering and attention during focused meditation: a fine-grained temporal analysis of fluctuating cognitive states

    Neuroimage

    (2012)
  • B.K. Hölzel

    Differential engagement of anterior cingulated and adjacent medial frontal cortex in adept meditators and nonmeditators

    Neurosci. Lett.

    (2007)
  • F. Zeidan

    Mindfulness meditation improves cognition: evidence of brief mental training

    Conscious. Cogn.

    (2010)
  • J.H. Jang

    Increased default mode network connectivity associated with meditation

    Neurosci. Lett.

    (2011)
  • S.L. Bressler et al.

    Large-scale brain networks in cognition: emerging methods and principles

    Trends Cogn. Sci.

    (2010)
  • M.R. Harter et al.

    Attention to pattern orientation-negative cortical potentials, reaction-time, and the selection process

    Electroencephalogr. Clin. Neurophysiol.

    (1980)
  • F. Rosler

    Slow negative brain potentials as reflections of specific modular resources of cognition

    Biol. Psychiatry

    (1997)
  • G. Bush

    Cognitive and emotional influences in anterior cingulate cortex

    Trends Cogn. Sci.

    (2000)
  • J.M. Halperin et al.

    The influences of environmental enrichment, cognitive enhancement, and physical exercise on brain development: can we alter the developmental trajectory of ADHD?

    Neurosci. Biobehav. Rev.

    (2011)
  • A. Lutz

    BOLD signal in insula is differentially related to cardiac function during compassion meditation in experts vs. novices

    Neuroimage

    (2009)
  • A. Baldassarre

    Individual variability in functional connectivity predicts performance of a perceptual task

    Proc. Natl. Acad. Sci. U.S.A.

    (2012)
  • J. Kounios et al.

    Aha! The cognitive neuroscience of insight

    Curr. Dir. Psychol. Sci.

    (2009)
  • G. Deco

    Emerging concepts for the dynamical organization of resting-state activity in the brain

    Nat. Rev. Neurosci.

    (2011)
  • D.A. Gusnard et al.

    Searching for a baseline: functional imaging and the resting human brain

    Nat. Rev. Neurosci.

    (2001)
  • M.E. Raichle

    A default mode of brain function

    Proc. Natl. Acad. Sci. U.S.A.

    (2001)
  • B.T. Yeo

    The organization of the human cerebral cortex estimated by intrinsic functional connectivity

    J. Neurophysiol.

    (2011)
  • R. Stickgold

    Sleep-dependent memory consolidation

    Nature

    (2005)
  • M.P. Walker et al.

    Sleep, memory, and plasticity

    Annu. Rev. Psychol.

    (2006)
  • K.D. Harris et al.

    Cortical state and attention

    Nat. Rev. Neurosci.

    (2011)
  • J.L. Vincent

    Intrinsic functional architecture in the anaesthetized monkey brain

    Nature

    (2007)
  • D.A. Fair

    The maturing architecture of the brain's default network

    Proc. Natl. Acad. Sci. U.S.A.

    (2008)
  • W. Gao

    Evidence on the emergence of the brain's default network from 2-week-old to 2-year-old healthy pediatric subjects

    Proc. Natl. Acad. Sci. U.S.A.

    (2009)
  • D. Zhang et al.

    Disease and the brain's dark energy

    Nat. Rev. Neurol.

    (2010)
  • H. Laufs

    Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest

    Proc. Natl. Acad. Sci. U.S.A.

    (2003)
  • D. Mantini

    Electrophysiological signatures of resting state networks in the human brain

    Proc. Natl. Acad. Sci. U.S.A.

    (2007)
  • B.J. He

    Electrophysiological correlates of the brain's intrinsic large-scale functional architecture

    Proc. Natl. Acad. Sci. U.S.A.

    (2008)
  • J.H. Lee

    Global and local fMRI signals driven by neurons defined optogenetically by type and wiring

    Nature

    (2010)
  • N.K. Logothetis

    Neurophysiological investigation of the basis of the fMRI signal

    Nature

    (2001)
  • D. Kahneman

    Attention and Effort

    (1973)
  • W.G. Walter

    Slow potential waves in the human brain associated with expectancy, attention and decision

    Arch. Psychiatr. Nervenkr.

    (1964)
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