Opinion
Temporal binding and the neural correlates of sensory awareness

https://doi.org/10.1016/S1364-6613(00)01568-0Get rights and content

Abstract

Theories of binding have recently come into the focus of the consciousness debate. In this review, we discuss the potential relevance of temporal binding mechanisms for sensory awareness. Specifically, we suggest that neural synchrony with a precision in the millisecond range may be crucial for conscious processing, and may be involved in arousal, perceptual integration, attentional selection and working memory. Recent evidence from both animal and human studies demonstrates that specific changes in neuronal synchrony occur during all of these processes and that they are distinguished by the emergence of fast oscillations with frequencies in the gamma-range.

Section snippets

Binding and consciousness

The notion of binding has been introduced first in the context of feature integration 9 and perceptual segmentation 10. Subsequently, the concept of binding has been applied to other domains and is now employed in theories on object recognition 11, attention 12, memory formation and recall 13, motor control 14, sensorimotor integration 15, language processing 16 and logical inference 17. In all these domains, a set of related computational requirements has been identified which, taken together,

Temporal binding

The concept of dynamic binding by synchronization of neuronal discharges has been developed mainly in the context of perceptual processing. Clearly, sensory systems (at least those of mammals) provide paradigmatic examples for functional architectures that give rise to binding problems of the kind defined above. The most dramatic case is represented by the primate visual system where anatomical and physiological studies have led to the identification of more than 30 distinct visual cortical

Animal studies on synchrony and awareness

By now, the synchronization phenomena predicted by the temporal binding hypothesis have been documented for a wide variety of neural systems. It is well established that neurons in both cortical and subcortical centers can synchronize their discharges with a precision in the millisecond range. The results available from animal studies show that synchronization of neural discharges occurs with a surprising degree of ubiquity, both across systems and species. Box 1 presents an overview of studies

Human studies on timing and perceptual consciousness

In humans, numerous studies using the technique of electroencephalographic (EEG) or magnetoencephalographic (MEG) recording have provided evidence supporting the conclusions drawn above. An important methodological difference is that the signals recorded in EEG/MEG studies result from spatial averaging across large neuronal assemblies and, thus, at this macroscopic level the cellular processes of synchronization and oscillatory response structure cannot be dissociated. Rather, both phenomena

Conclusions: synchrony and conscious states

The studies reviewed above strongly suggest that the temporal dynamics in neuronal activity may be critical for the production of conscious states. The experiments on binocular rivalry make it very likely that only strongly synchronized neuronal signals contribute to awareness. They suggest that activation of feature-detecting cells is per se not sufficient to grant access of the encoded information to consciousness (as indicated by the fact that cells representing a non-perceived stimulus are

Outstanding questions

  • Why does selection based on temporal binding lead to awareness in some cases but not in others? For instance, both the attentive search for a particular object as well as the visuomotor coordination in a frequently practised task such as driving require context-dependent selection. However, although in the former case the selection process usually leads to awareness, this does not necessarily hold for the latter. What makes the difference?

  • Assuming that the processes discussed here constitute

Acknowledgements

We thank Thomas Metzinger, Peter König and Olivier Bertrand for critical reading and comments on the manuscript. We are obliged to Matthias Munk, Pascal Fries and Michael Brecht for permission to use their data in Fig. 1–3. The authors’ research was supported by the Max-Planck-Society and the German Research Council (DFG grants EN 203/4-2 and EN 203/5-1/5-2).

References (62)

  • R. Srinivasan

    Increased synchronization of neuromagnetic responses during conscious perception

    J. Neurosci.

    (1999)
  • J. Delacour

    Neurobiology of consciousness: an overview

    Behav. Brain Res.

    (1997)
  • G.B. Young et al.

    Neurobiological basis of consciousness

    Arch. Neurol.

    (1999)
  • A.K. Engel

    Temporal coding in the visual cortex: new vistas on integration in the nervous system

    Trends Neurosci.

    (1992)
  • W. Singer

    Neuronal assemblies: necessity, significance, and detectability

    Trends Cognit. Sci.

    (1997)
  • F. Crick et al.

    Towards a neurobiological theory of consciousness

    Semin. Neurosci.

    (1990)
  • J. Newman et al.

    A neural attentional model for access to consciousness: a global workspace perspective

    Concepts Neurosci.

    (1993)
  • G. Tononi et al.

    Consciousness and complexity

    Science

    (1998)
  • A.K. Engel

    Temporal binding, binocular rivalry, and consciousness

    Conscious. Cognit.

    (1999)
  • A. Treisman

    The binding problem

    Curr. Opin. Neurobiol.

    (1996)
  • C. von der Malsburg

    The Correlation Theory of Brain Function. (Internal Report 81-2), Max Planck Institute for Biophysical Chemistry

  • J.E. Hummel et al.

    Dynamic binding in a neural network for shape recognition

    Psychol. Rev.

    (1992)
  • E. Niebur

    An oscillation-based model for the neuronal basis of attention

    Vis. Res.

    (1993)
  • A.R. Damasio

    Synchronous activation in multiple cortical regions: a mechanism for recall

    Semin. Neurosci.

    (1990)
  • V.N. Murthy et al.

    Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys

    Proc. Natl. Acad. Sci. USA

    (1992)
  • P.R. Roelfsema

    The role of neuronal synchronization in response selection: a biologically plausible theory of structured representation in the visual cortex

    J. Cogn. Neurosci.

    (1996)
  • F. Pulvermüller

    Words in the brain's language

    Behav. Brain Sci.

    (1999)
  • L. Shastri et al.

    From simple associations to systematic reasoning: a connectionist representation of rule, variables and dynamic bindings using temporal synchrony

    Behav. Brain Sci.

    (1993)
  • J.A. Fodor et al.

    Connectionism and cognitive architecture: a critical analysis

    Cognition

    (1988)
  • T. Metzinger

    Faster than thought. Holism, homogeneity and temporal coding

  • R. Llinás et al.

    Perception as an oneiric-like state modulated by the senses

  • Cited by (0)

    View full text