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Cortical Travelling Waves: Mechanisms and Computational Principles

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Cortical Travelling Waves: Mechanisms and Computational Principles REVIEWS Cortical travelling waves: mechanisms and computational principles Lyle Muller1, Frédéric Chavane2, John Reynolds1 and Terrence J. Sejnowski1,3* Abstract | Multichannel recording technologies have revealed travelling waves of neural activity in multiple sensory, motor and cognitive systems. These waves can be spontaneously generated by recurrent circuits or evoked by external stimuli. They travel along brain networks at multiple scales, transiently modulating spiking and excitability as they pass. Here, we review recent experimental findings that have found evidence for travelling waves at single-area (mesoscopic) and whole-brain (macroscopic) scales. We place these findings in the context of the current theoretical understanding of wave generation and propagation in recurrent networks. During the large low-frequency rhythms of sleep or the relatively desynchronized state of the awake cortex, travelling waves may serve a variety of functions, from long-term memory consolidation to processing of dynamic visual stimuli. We explore new avenues for experimental and computational understanding of the role of spatiotemporal activity patterns in the cortex. Phase offsets Synchrony in the activity of neuronal populations has shape these waves so that they differ profoundly from 1,2 13 14 The differences in phase (an long been of interest in neuroscience , but its function sleep to wake . In turn, these waves transiently mod- amplitude-invariant measure of has remained elusive. Neural oscillations are rhythmic ulate neuronal excitability15–19 and shape responses to position in an oscillation cycle) fluctuations of spiking activity within neuronal popula- external input20 over a wide range of spatial and tempo- between two (or more) tions. It is proposed that synchrony of neural oscillations ral scales. They travel over spatial scales that range from oscillations. in different neural populations might be able to shape the mesoscopic (single cortical areas and millimetres of Travelling waves input gain and aid information transfer between these cortex) to the macroscopic (global patterns of activity over A disturbance that travels populations3,4 because the synchronous occurrence of several centimetres) and extend over temporal scales through a physical medium action potentials in many neurons is known to increase from tens to hundreds of milliseconds. Although, in that may be water, air or a 5,6 neural network. their ability to drive spikes in shared target neurons . initial studies, mesoscopic travelling waves were pro- Indeed, experimental evidence suggests that oscillation nounced only under conditions of low visual luminance synchrony modulates the effective connectivity of pop- contrast21,22 and were mostly reported in anaesthetized ulations in the cortex7,8, shapes plasticity between neu- states23–28, recent work has shown that stimulus-evoked rons9 and drives processing of stimulus features between mesoscopic travelling waves robustly appear in the visual cortex areas V1 and V4 (REF. 10). awake visual cortex14,29 and can influence intracortical These proposed functions have traditionally been dynamics during the viewing of natural stimuli30. thought to involve precise zero-lag synchrony11,12, in In vitro and in vivo cortical travelling waves have been which oscillations across single areas or distant regions reviewed previously22,31,32. In this article, we cover a series in the cortex are aligned perfectly in time. However, of recent studies that have led to important advances in 1 Salk Institute for Biological with the advent of simultaneous multichannel record- our understanding of travelling waves and the generality Studies, La Jolla, CA, USA. 2Institut de Neurosciences ing technologies, we have begun to appreciate that the of their role in cortical processing. We first summarize de la Timone (INT), Centre relative timing of neural population activity is constantly experimental observations of travelling waves in the National de la Recherche changing. Instead of precise zero-lag synchrony, a range cortex, focusing on advances in recording and analysis Scientifique (CNRS) and of flexible phase offsets is possible. These flexible phase techniques that have enabled the detection of waves in Aix-Marseille Université, travelling Marseille, France. relationships can, in their simplest form, be single cortical regions. Next, we briefly review the broad 3Division of Biological waves of various shapes (including plane, radial and spiral computational and mathematical literature on travelling Sciences, University of waves). The combination of multiple travelling waves waves in neural networks, focusing on theoretical mech- California, La Jolla, CA, USA. can form complex spatiotemporal patterns. anisms for wave generation and possible experimental *e-mail: [email protected] Stimulus-driven and internally generated travelling tests of these predictions. Finally, we discuss emerging doi:10.1038/nrn.2018.20 waves occur across different brain states and sensory computational roles for cortical travelling waves, from Published online 22 Mar 2018 conditions. Brain state and synaptic activity strongly sensory processing to memory consolidation. As we NATURE REVIEWS | NEUROSCIENCE VOLUME 19 | MAY 2018 | 255 ©2018 Mac millan Publishers Li mited, part of Spri nger Nature. All ri ghts reserved. REVIEWS describe, at the macroscopic scale, these waves allow is an anterior-to-posterior travelling wave44 (FIG. 1a) and the formation of the large-scale, distributed cell assem- that auditory-induced 30–80 Hz gamma oscillations blies thought to underlie long-term memory33,34. At the make a coherent anterior-to-posterior sweep across the mesoscopic scale, multiple lines of experimental evidence cortex (observed using magnetic field tomography)45. suggest that evoked waves are a way for neural circuits to Signal distortion by cranial tissues46 and volume conduc- flexibly store and use information from the recent past. In tion, however, pose substantial possible confounds for Complex spatiotemporal closing, we highlight open questions for new experiments detection of travelling waves in EEG. Understanding patterns and theoretical work to further elucidate the biological the generation of electric and magnetic fields by neural Patterns that can result from the summation of many mechanisms underlying cortical travelling waves and activity remains an active pursuit for experimental and 46,47 individual waves. Depending on their role in neural computation. theoretical research ; however, in the absence of a gen- the properties of the medium, eral physical theory48,49, the origin and interpretation of the pattern resulting from Travelling waves in neural systems travelling waves observed solely in EEG is problematic these interactions can differ Travelling waves were first observed at the macroscopic, (see REF. 50 for an initial comparison). greatly. whole-brain scale. More recently, new high-resolution In recent years, intracranial ECoG recordings in Mesoscopic optical and electrophysiological recording technologies clinical patients have made detailed analyses of human A scale between microscopic have led to the observation of travelling waves at the cortical dynamics possible. Following a technique devel- and macroscopic. In mesoscopic scale of single regions in the cortex. Distinct oped by Penfield and Jasper for mapping the cortical sites neuroscience, the mesoscopic 51 scale describes single regions axonal fibre tracts carry waves at the two scales, and there involved in generating epileptic seizures , surgeons typi- (such as cortical areas or are observable differences in the resulting dynamics — cally implant two-dimensional ECoG electrode arrays subcortical nuclei) spanning most notably, spatial extent and propagation speed — on the surface of one cortical hemisphere, with coverage millimetres to centimetres. that make clear distinctions between the two possible. of temporal, parietal and frontal lobes supplemented by Cortical networks at this scale Macroscopic waves are generally recorded using electro- additional linear strips of electrodes on the same or the can be imaged through encephalography electrocorticography recently developed recording (EEG) or (ECoG), contralateral hemisphere. ECoG recordings have a high technologies. in which arrays of electrodes either outside the skull signal-to-noise ratio and spatial localization, reflecting (EEG) or directly on the cortical surface (ECoG) record neural activity spanning less than 1 centimetre of the cor- Macroscopic potentials from neural populations with high temporal tex52,53. Furthermore, by capturing power in the 80–150 Hz The scale of the whole brain; traditionally recorded with (millisecond) resolution but low spatial (centimetre) high-gamma band, which serves as an index for neuronal 54 extracranial techniques (elec- resolution. These waves generally have propagation firing near the electrode , ECoG recordings can link troencephalography and mag- speeds from 1 to 10 metres per second, falling within oscillatory patterns with local population spiking activity. netoencephalography) and the range of the axonal conduction speeds of myelinated Analysis of ECoG recordings has revealed travelling more recently recorded with white matter fibres in the cortex35. Mesoscopic waves are waves during both awake and sleep states. The spatial intracranial methods local field potential (electrocorticography). generally observed in the (LFP) using range of these oscillatory patterns can vary from rela-
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