Opinion
Low-frequency neuronal oscillations as instruments of sensory selection

https://doi.org/10.1016/j.tins.2008.09.012Get rights and content

Neuroelectric oscillations reflect rhythmic shifting of neuronal ensembles between high and low excitability states. In natural settings, important stimuli often occur in rhythmic streams, and when oscillations entrain to an input rhythm their high excitability phases coincide with events in the stream, effectively amplifying neuronal input responses. When operating in a ‘rhythmic mode’, attention can use these differential excitability states as a mechanism of selection by simply enforcing oscillatory entrainment to a task-relevant input stream. When there is no low-frequency rhythm that oscillations can entrain to, attention operates in a ‘continuous mode’, characterized by extended increase in gamma synchrony. We review the evidence for early sensory selection by oscillatory phase-amplitude modulations, its mechanisms and its perceptual and behavioral consequences.

Introduction

Over 75 years ago, Bishop [1] raised the fundamental proposition that neuroelectric oscillations reflect cyclical variations in neuronal excitability. In the ensuing decades, increasingly specific linkages have been drawn between neuronal oscillations in defined frequency bands and a variety of cognitive functions. Linkages include (i) theta-band oscillations with phase-encoding of spatial information in hippocampus [2] and with formation of mnemonic neuronal representations [3], (ii) alpha-band oscillations with ‘internally-directed’ cognitive processes [4] and (iii) gamma-band oscillations with feature binding [5] and attention or sensory selection [6]. Thus, although the issue is not without controversy (e.g. Ref. [7]), there is gathering consensus that neuronal oscillations have an important role in brain operations to the extent that understanding of neuronal oscillation ‘rhythms’ now seems to be essential to our understanding of brain function 8, 9.

We explore and advance the proposition that neuronal oscillations serve as crucial instruments of active input selection at the level of primary sensory cortex. Paradoxically, delta-band oscillations, long considered to index states of deep sleep and/or conditions of brain compromise [10], are at the heart of this phenomenon. In considering this proposition, we review findings about oscillations in four key areas: (i) their control of neuronal excitability, (ii) their mechanistic role in the amplification of sensory inputs, (iii) their control and utilization by attention and (iv) their variable modes of operation in response to task demands. We then describe how the conceptual framework generated by these findings converges with other theoretical positions and offers new explanation of prior behavioral and neurophysiological findings.

Section snippets

Oscillations control neuronal excitability

Local field potentials (LFPs) and their more macroscopic manifestations in the scalp electroencephalogram (EEG) are mainly generated by transmembrane currents occurring synchronously in ensembles of neurons 11, 12. Analysis of LFP distributions across cortical layers shows that the regular variations or ‘oscillations’ of voltage measured at any single point in the extracellular medium reflect the rhythmic (and synchronous) alternation of inward and outward transmembrane current flow in the

Rhythmic processing: converging theory and retrospection on earlier findings

A proposition most akin to rhythmic-mode operation and pre-dating it by several years is the dynamic attending theory. As developed by Jones, Large and colleagues 35, 40, 41 and in a more ‘motor perspective’ by Praamstra and colleagues [37], the idea is that attending itself can be an oscillatory process that entrains to environmental rhythms, thus improving discriminative performance (Figure 3c). Nobre and colleagues 42, 43, 44 suggest that ‘attention to time’ is one of several attentional

Generality of rhythmic-mode processing?

The foregoing framework makes numerous empirical predictions. Sensory selection in a typical ERP spatial attention paradigm, for example, could be accomplished by entraining low-frequency oscillations in the neuronal representations of the relevant locations to the basic rhythm of stimulus presentation. The representations of all other locations could be left to wander in random phase, thus passively and stochastically degrading the processing of an irrelevant event stream, or could be pushed

Concluding comments

Natural stimulation acquired through our own motor behavior or produced by that of another animal is usually rhythmic, in part because motor behavior is itself patterned by oscillatory mechanisms such as the 10 Hz mu rhythm 59, 60. In these and other common circumstances, when there is a relevant stimulus rhythm(s) that intrinsic brain oscillations can entrain to, attention operates in a rhythmic mode putting the range of ambient neuronal oscillations to work in amplifying relevant inputs and

Acknowledgements

We are grateful to our colleagues in the Columbia University Oscillation Journal Club for helpful commentary. We thank J.M. Palva, P. Fries, T. Womelsdorf, R. Desimone, E.G. Jones, E.W. Large and M.R. Jones for advice and help in preparing illustrations. This work is supported the National Institute of Mental Health (MH 060358 and MH 061989; www.nimh.nih.gov).

References (68)

  • A. Nobre

    The hazards of time

    Curr. Opin. Neurobiol.

    (2007)
  • R.M. Klein

    Inhibition of return

    Trends Cogn. Sci.

    (2000)
  • A.A. Ghazanfar et al.

    Is neocortex essentially multisensory?

    Trends Cogn. Sci.

    (2006)
  • M.A. Kramer

    Sharp edge artifacts and spurious coupling in EEG frequency comodulation measures

    J. Neurosci. Methods

    (2008)
  • S. Yuval-Greenberg

    Transient induced gamma-band response in EEG as a manifestation of miniature saccades

    Neuron

    (2008)
  • G. Pfurtscheller

    Functional dissociation of lower and upper frequency mu rhythms in relation to voluntary limb movement

    Clin. Neurophysiol.

    (2000)
  • J.A. Pineda

    The functional significance of mu rhythms: translating “seeing” and “hearing” into “doing”

    Brain Res. Brain Res. Rev.

    (2005)
  • H. Luo et al.

    Phase patterns of neuronal responses reliably discriminate speech in human auditory cortex

    Neuron

    (2007)
  • W.J. Freeman

    Spatial spectra of scalp EEG and EMG from awake humans

    Clin. Neurophysiol.

    (2003)
  • J. Csicsvari

    Mechanisms of gamma oscillations in the hippocampus of the behaving rat

    Neuron

    (2003)
  • G. Bishop

    Cyclical changes in excitability of the optic pathway of the rabbit

    Am. J. Physiol.

    (1933)
  • W. Singer et al.

    Visual feature integration and the temporal correlation hypothesis

    Annu. Rev. Neurosci.

    (1995)
  • P. Fries

    Oscillatory neuronal synchronization in primary visual cortex as a correlate of stimulus selection

    J. Neurosci.

    (2002)
  • G. Buzsaki et al.

    Neuronal oscillations in cortical networks

    Science

    (2004)
  • G. Buzsaki

    The structure of consciousness

    Nature

    (2007)
  • U. Mitzdorf

    Current source-density method and application in cat cerebral cortex: Investigation of evoked potentials and EEG phenomena

    Physiol. Rev.

    (1985)
  • C.E. Schroeder

    Localization of ERP generators and identification of underlying neural processes

    Electroencephalogr. Clin. Neurophysiol. Suppl.

    (1995)
  • P. Lakatos

    An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex

    J. Neurophysiol.

    (2005)
  • T. Womelsdorf

    Gamma-band synchronization in visual cortex predicts speed of change detection

    Nature

    (2006)
  • M. Steriade

    A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components

    J. Neurosci.

    (1993)
  • D. Contreras

    Mechanisms of long-lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks

    J. Physiol.

    (1996)
  • M.V. Sanchez-Vives et al.

    Cellular and network mechanisms of rhythmic recurrent activity in neocortex

    Nat. Neurosci.

    (2000)
  • S.M. Sherman et al.

    The role of the thalamus in the flow of information to the cortex

    Philos. Trans. R. Soc. Lond. B. Biol. Sci.

    (2002)
  • A.S. Shah

    Neural dynamics and fundamental mechanisms of event-related potentials

    Cereb. Cortex

    (2004)
  • Cited by (1127)

    View all citing articles on Scopus
    View full text