Spontaneous Infra-slow Brain Activity Has Unique Spatiotemporal Dynamics and Laminar Structure

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2018 Apr 3

PMID 29606579

Citations 91

Authors

Anish Mitra

Andrew Kraft

Patrick Wright

Benjamin Acland

Abraham Z Snyder

Zachary Rosenthal

Leah Czerniewski

Adam Bauer

Lawrence Snyder

Joseph Culver

Jin-Moo Lee

Marcus E Raichle

Affiliations

Soon will be listed here.

Abstract

Systems-level organization in spontaneous infra-slow (<0.1Hz) brain activity, measured using blood oxygen signals in fMRI and optical imaging, has become a major theme in the study of neural function in both humans and animal models. Yet the neurophysiological basis of infra-slow activity (ISA) remains unresolved. In particular, is ISA a distinct physiological process, or is it a low-frequency analog of faster neural activity? Here, using whole-cortex calcium/hemoglobin imaging in mice, we show that ISA in each of these modalities travels through the cortex along stereotypical spatiotemporal trajectories that are state dependent (wake versus anesthesia) and distinct from trajectories in delta (1-4 Hz) activity. Moreover, mouse laminar electrophysiology reveals that ISA travels through specific cortical layers and is organized into unique cross-laminar temporal dynamics that are different from higher frequency local field potential activity. These findings suggest that ISA is a distinct neurophysiological process that is reflected in fMRI blood oxygen signals.

Citing Articles

The brain's action-mode network.

Dosenbach N, Raichle M, Gordon E Nat Rev Neurosci. 2025; 26(3):158-168.

PMID: 39743556 DOI: 10.1038/s41583-024-00895-x.

Symmetry breaking organizes the brain's resting state manifold.

Fousek J, Rabuffo G, Gudibanda K, Sheheitli H, Petkoski S, Jirsa V Sci Rep. 2024; 14(1):31970.

PMID: 39738729 PMC: 11686292. DOI: 10.1038/s41598-024-83542-w.

Hemodynamic cortical ripples through cyclicity analysis.

Abraham I, Shahsavarani S, Zimmerman B, Husain F, Baryshnikov Y Netw Neurosci. 2024; 8(4):1105-1128.

PMID: 39735496 PMC: 11674492. DOI: 10.1162/netn_a_00392.

Orthogonalization of spontaneous and stimulus-driven activity by hierarchical neocortical areal network in primates.

Matsui T, Hashimoto T, Murakami T, Uemura M, Kikuta K, Kato T Nat Commun. 2024; 15(1):10055.

PMID: 39632809 PMC: 11618767. DOI: 10.1038/s41467-024-54322-x.

Methods for and Use of Functional Magnetic Resonance Imaging in Psychiatry.

Lee J, Drysdale A, Srivastava A, Shi T, Patel G Adv Neurobiol. 2024; 40:89-117.

PMID: 39562442 DOI: 10.1007/978-3-031-69491-2_4.

References

van Kerkoerle T, Self M, Dagnino B, Gariel-Mathis M, Poort J, van der Togt C . Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex. Proc Natl Acad Sci U S A. 2014; 111(40):14332-41. PMC: 4210002. DOI: 10.1073/pnas.1402773111. View

Shimaoka D, Song C, Knopfel T . State-Dependent Modulation of Slow Wave Motifs towards Awakening. Front Cell Neurosci. 2017; 11:108. PMC: 5401891. DOI: 10.3389/fncel.2017.00108. View

Ma Y, Shaik M, Kozberg M, Kim S, Portes J, Timerman D . Resting-state hemodynamics are spatiotemporally coupled to synchronized and symmetric neural activity in excitatory neurons. Proc Natl Acad Sci U S A. 2016; 113(52):E8463-E8471. PMC: 5206542. DOI: 10.1073/pnas.1525369113. View

Marder E . Neuromodulation of neuronal circuits: back to the future. Neuron. 2012; 76(1):1-11. PMC: 3482119. DOI: 10.1016/j.neuron.2012.09.010. View

Sakata S, Harris K . Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron. 2009; 64(3):404-18. PMC: 2778614. DOI: 10.1016/j.neuron.2009.09.020. View

Canolty R, Edwards E, Dalal S, Soltani M, Nagarajan S, Kirsch H . High gamma power is phase-locked to theta oscillations in human neocortex. Science. 2006; 313(5793):1626-8. PMC: 2628289. DOI: 10.1126/science.1128115. View

He B, Snyder A, Zempel J, Smyth M, Raichle M . Electrophysiological correlates of the brain's intrinsic large-scale functional architecture. Proc Natl Acad Sci U S A. 2008; 105(41):16039-44. PMC: 2564983. DOI: 10.1073/pnas.0807010105. View

ALADJALOVA N . Infra-slow rhythmic oscillations of the steady potential of the cerebral cortex. Nature. 1957; 179(4567):957-9. DOI: 10.1038/179957a0. View

Xiao D, Vanni M, Mitelut C, Chan A, LeDue J, Xie Y . Mapping cortical mesoscopic networks of single spiking cortical or sub-cortical neurons. Elife. 2017; 6. PMC: 5328594. DOI: 10.7554/eLife.19976. View

10.

Mitra A, Snyder A, Tagliazucchi E, Laufs H, Raichle M . Propagated infra-slow intrinsic brain activity reorganizes across wake and slow wave sleep. Elife. 2015; 4. PMC: 4737658. DOI: 10.7554/eLife.10781. View

11.

Fox M, Raichle M . Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci. 2007; 8(9):700-11. DOI: 10.1038/nrn2201. View

12.

Stroh A, Adelsberger H, Groh A, Ruhlmann C, Fischer S, Schierloh A . Making waves: initiation and propagation of corticothalamic Ca2+ waves in vivo. Neuron. 2013; 77(6):1136-50. DOI: 10.1016/j.neuron.2013.01.031. View

13.

Massimini M, Huber R, Ferrarelli F, Hill S, Tononi G . The sleep slow oscillation as a traveling wave. J Neurosci. 2004; 24(31):6862-70. PMC: 6729597. DOI: 10.1523/JNEUROSCI.1318-04.2004. View

14.

Pan W, Thompson G, Magnuson M, Jaeger D, Keilholz S . Infraslow LFP correlates to resting-state fMRI BOLD signals. Neuroimage. 2013; 74:288-97. PMC: 3615090. DOI: 10.1016/j.neuroimage.2013.02.035. View

15.

Silasi G, Xiao D, Vanni M, Chen A, Murphy T . Intact skull chronic windows for mesoscopic wide-field imaging in awake mice. J Neurosci Methods. 2016; 267:141-9. PMC: 5075450. DOI: 10.1016/j.jneumeth.2016.04.012. View

16.

de Zwart J, Silva A, van Gelderen P, Kellman P, Fukunaga M, Chu R . Temporal dynamics of the BOLD fMRI impulse response. Neuroimage. 2005; 24(3):667-77. DOI: 10.1016/j.neuroimage.2004.09.013. View

17.

Monto S, Palva S, Voipio J, Palva J . Very slow EEG fluctuations predict the dynamics of stimulus detection and oscillation amplitudes in humans. J Neurosci. 2008; 28(33):8268-72. PMC: 6670577. DOI: 10.1523/JNEUROSCI.1910-08.2008. View

18.

Huang L, Liu Y, Li M, Hu D . Hemodynamic and electrophysiological spontaneous low-frequency oscillations in the cortex: directional influences revealed by Granger causality. Neuroimage. 2013; 85 Pt 2:810-22. DOI: 10.1016/j.neuroimage.2013.07.061. View

19.

Matsui T, Murakami T, Ohki K . Transient neuronal coactivations embedded in globally propagating waves underlie resting-state functional connectivity. Proc Natl Acad Sci U S A. 2016; 113(23):6556-61. PMC: 4988587. DOI: 10.1073/pnas.1521299113. View

20.

Nelson L, Lu J, Guo T, Saper C, Franks N, Maze M . The alpha2-adrenoceptor agonist dexmedetomidine converges on an endogenous sleep-promoting pathway to exert its sedative effects. Anesthesiology. 2003; 98(2):428-36. DOI: 10.1097/00000542-200302000-00024. View