Abstract
In order for us to survive, our behaviour has to be perched somewhere between stability and flexibility, or between exploitation and exploration of available resources. This requires the underlying spatiotemporal brain dynamics to be delicately balanced between order and disorder, drawing upon a large repertoire of available brain states. Beyond survival, in order to thrive the brain has to be sufficiently flexible to be able to seek novel trajectories and expand the dynamical repertoire. Here we propose that a key ingredient could be play, the active exploration of novelty beyond exploiting existing potentially scarce resources. Using a novel analysis method called ‘connectome harmonics’ we not only demonstrate that brain activity resides close to criticality—at the delicate balance between order (stability) and disorder (flexibility)—but this whole-brain criticality is also intrinsically linked to oscillatory brain dynamics. We show that compared to wakefulness, other conscious states are related to different connectome-harmonic repertoires and differ in their proximity to criticality, where the critical regime may enhance the ability to flexibly seek new brain states. In particular, we propose that these brain dynamics may underlie the creative process found in play and improvisation, and as such may shed new light on discovering how the brain optimizes the balance between exploitation and exploration needed for behavioural flexibility.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Chialvo, D.R.: Critical brain networks. Phys. A Stat. Mech. Appl. 340, 756–765 (2004)
Plenz, D.: Viewpoint: the critical brain. Physics 6, 47 (2013)
Shew, W.L., Plenz, D.: The functional benefits of criticality in the cortex. Neuroscientist 19, 88–100 (2013)
Priesemann, V., et al.: Spike avalanches in vivo suggest a driven, slightly subcritical brain state. Front. Syst. Neurosci. 8, 108 (2014)
Hesse, J., Gross, T.: Self-organized criticality as a fundamental property of neural systems. Front. Syst. Neurosci. 8, 166 (2015)
Kitzbichler, M.G., Smith, M.L., Christensen, S.R., Bullmore, E.: Broadband criticality of human brain network synchronization. PLoS Comput. Biol. 5, e1000314 (2009)
Tagliazucchi, E., et al.: Criticality in large-scale brain fMRI dynamics unveiled by a novel point process analysis. Front. Physiol. 3, 15 (2012)
Linkenkaer-Hansen, K., Nikouline, V.V., Palva, J.M., Ilmoniemi, R.J.: Long-range temporal correlations and scaling behavior in human brain oscillations. J. Neurosci. 21, 1370–1377 (2001)
Allegrini, P., Paradisi, P., Menicucci, D., Gemignani, A.: Fractal complexity in spontaneous EEG metastable-state transitions: new vistas on integrated neural dynamics. Front. Physiol. 1, 128 (2010)
Palva, J.M., et al.: Neuronal long-range temporal correlations and avalanche dynamics are correlated with behavioral scaling laws. Proc. Natl. Acad. Sci. 110, 3585–3590 (2013)
Shriki, O., et al.: Neuronal avalanches in the resting MEG of the human brain. J. Neurosci. 33, 7079–7090 (2013)
Priesemann, V., Valderrama, M., Wibral, M., Le Van Quyen, M.: Neuronal avalanches differ from wakefulness to deep sleep-evidence from intracranial depth recordings in humans. PLoS Comput. Biol. 9, e1002985 (2013)
Deco, G., Jirsa, V.K.: Ongoing cortical activity at rest: criticality, multistability, and ghost attractors. J. Neurosci. 32, 3366–3375 (2012)
Haimovici, A., Tagliazucchi, E., Balenzuela, P., Chialvo, D.R.: Brain organization into resting state networks emerges at criticality on a model of the human connectome. Phys. Rev. Lett. 110, 178101 (2013)
Stumpf, M.P., Porter, M.A.: Critical truths about power laws. Science 335, 665–666 (2012)
Beggs, J.M., Timme, N.: Being critical of criticality in the brain. Front. Physiol. 3, 163 (2012)
He, B.J.: Scale-free brain activity: past, present, and future. Trends Cogn. Sci. 18, 480–487 (2014)
Atasoy, S., Donnelly, I., Pearson, J.: Human brain networks function in connectome-specific harmonic waves. Nat. Commun. 7, 10340 (2016)
Atasoy, S., Deco, G., Kringelbach, M.L., Pearson, J.: Harmonic brain modes: a unifying framework for linking space and time in brain dynamics. Neuroscientist 24, 277–293 (2017). https://doi.org/10.1177/1073858417728032
Buzsáki, G., Draguhn, A.: Neuronal oscillations in cortical networks. Science 304, 1926–1929 (2004)
Fox, M.D., et al.: The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. USA 102, 9673–9678 (2005)
Fox, M.D., Raichle, M.E.: Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700–711 (2007)
Deco, G., Jirsa, V.K., McIntosh, A.R.: Emerging concepts for the dynamical organization of resting-state activity in the brain. Nat. Rev. Neurosci. 12, 43 (2011)
Chladni, E.F.F.: Die akustik. Breitkopf & Härtel (1830)
Roos, C.: Quantum physics: simulating magnetism. Nature 484, 461–462 (2012)
Britton, J.W., et al.: Engineered two-dimensional Ising interactions in a trapped-ion quantum simulator with hundreds of spins. Nature 484, 489–492 (2012)
Schrödinger, E.: An undulatory theory of the mechanics of atoms and molecules. Phys. Rev. 28, 1049 (1926)
Moon, C.R., et al.: Quantum phase extraction in isospectral electronic nanostructures. Science 319, 782–787 (2008)
Turing, A.M.: The chemical basis of morphogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 237, 37–72 (1952)
Kondo, S., Miura, T.: Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329, 1616–1620 (2010)
Robinson, P.A., et al.: Eigenmodes of brain activity: neural field theory predictions and comparison with experiment. NeuroImage 142, 79–98 (2016)
Stewart, I.: Mathematics: holes and hot spots. Nature 401, 863–865 (1999)
Chung, F.R.: Spectral Graph Theory, vol. 92. American Mathematical Soc., Providence (1997)
Strogatz, S.H.: Sync: How Order Emerges from Chaos in the Universe, Nature, and Daily Life. Hachette, UK (2012)
Stanley, H.E.: Scaling, universality, and renormalization: three pillars of modern critical phenomena. Rev. Mod. Phys. 71, S358 (1999)
Kadanoff, L.P.: From Order to Chaos II: Essays: Critical, Chaotic and Otherwise. World Scientific (1999)
Marković, D., Gros, C.: Power laws and self-organized criticality in theory and nature. Phys. Rep. 536, 41–74 (2014)
Beggs, J.M.: The criticality hypothesis: how local cortical networks might optimize information processing. Philos. Trans. R. Soc. Lond. A Math. Phys. Eng. Sci. 366, 329–343 (2008)
Brochini, L., et al.: Phase transitions and self-organized criticality in networks of stochastic spiking neurons. Sci. Rep. 6, 35831 (2016)
Breakspear, M.: Dynamic models of large-scale brain activity. Nat. Neurosci. 20, 340 (2017)
Deco, G., Kringelbach, M.L.: Metastability and coherence: extending the communication through coherence hypothesis using a whole-brain computational perspective. Trends Neurosci 39, 125–135 (2016)
Cabral, J., et al.: Exploring mechanisms of spontaneous functional connectivity in meg: how delayed network interactions lead to structured amplitude envelopes of band-pass filtered oscillations. Neuroimage 90, 423–435 (2014)
Cabral, J., Kringelbach, M.L., Deco, G.: Functional connectivity dynamically evolves on multiple time-scales over a static structural connectome: models and mechanisms. NeuroImage 160, 84–96 (2017)
Carhart-Harris, R.L., et al.: The entropic brain: a theory of conscious states informed by neuroimaging research with psychedelic drugs. Front. Hum. Neurosci. 8 (2014)
Atasoy, S., et al.: Connectome-harmonic decomposition of human brain activity reveals dynamical repertoire re-organization under LSD. Sci. Rep. 7, 17661 (2017)
Deco, G., Tononi, G., Boly, M., Kringelbach, M.L.: Rethinking segregation and integration: contributions of whole-brain modelling. Nat. Rev. Neurosci. 16, 430–439 (2015)
Lee, U., et al.: Brain networks maintain a scale-free organization across consciousness, anesthesia, and recoveryevidence for adaptive reconfiguration. J. Am. Soc. Anesthesiol. 113, 1081–1091 (2010)
Pearlmutter, B.A., Houghton, C.J.: A new hypothesis for sleep: tuning for criticality. Neural Comput. 21, 1622–1641 (2009)
Meisel, C., Olbrich, E., Shriki, O., Achermann, P.: Fading signatures of critical brain dynamics during sustained wakefulness in humans. J. Neurosci. 33, 17363–17372 (2013)
Tinker, J., Perez Velazquez, J.: Power law scaling in synchronization of brain signals depends on cognitive load. Front. Syst. Neurosci. 8 (2015)
Meisel, C., Storch, A., Hallmeyer-Elgner, S., Bullmore, E., Gross, T.: Failure of adaptive self-organized criticality during epileptic seizure attacks. PLoS Comput. Biol. 8, e1002312 (2012)
Stewart, C.V., Plenz, D.: Inverted-u profile of dopamine-nmda-mediated spontaneous avalanche recurrence in superficial layers of rat prefrontal cortex. J. Neurosci. 26, 8148–8159 (2006)
Gireesh, E.D., Plenz, D.: Neuronal avalanches organize as nested theta-and beta/gamma-oscillations during development of cortical layer 2/3. Proc. Natl. Acad. Sci. 105, 7576–7581 (2008)
Pasquale, V., Massobrio, P., Bologna, L., Chiappalone, M., Martinoia, S.: Self-organization and neuronal avalanches in networks of dissociated cortical neurons. Neuroscience 153, 1354–1369 (2008)
Bilder, R.M., Knudsen, K.S.: Creative cognition and systems biology on the edge of chaos. Front. Psychol. 5 (2014)
Beaty, R.E., Benedek, M., Kaufman, S.B., Silvia, P.J.: Default and executive network coupling supports creative idea production. Sci. Rep. 5 (2015)
Limb, C.J., Braun, A.R.: Neural substrates of spontaneous musical performance: an fMRI study of jazz improvisation. PLoS One 3, e1679 (2008)
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Atasoy, S., Deco, G., Kringelbach, M.L. (2019). Playing at the Edge of Criticality: Expanded Whole-Brain Repertoire of Connectome-Harmonics. In: Tomen, N., Herrmann, J., Ernst, U. (eds) The Functional Role of Critical Dynamics in Neural Systems . Springer Series on Bio- and Neurosystems, vol 11. Springer, Cham. https://doi.org/10.1007/978-3-030-20965-0_2
Download citation
DOI: https://doi.org/10.1007/978-3-030-20965-0_2
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-20964-3
Online ISBN: 978-3-030-20965-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)