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Cortical state and attention

Key Points

  • Cortex operates in multiple states, which are characterized by varying amounts of fluctuation in spontaneous population activity.

  • The classical desynchronized and synchronized states that are associated with waking and slow-wave sleep, respectively, are two points on a continuum of states; the continuum is probably multidimensional.

  • More-desynchronized states exhibit decreases in low-frequency local field potential (LFP) power and lower pairwise spiking correlations than synchronized states.

  • Selective attention seems to involve desynchronization operating locally in a patch of cortex that represents the attended stimulus.

  • Local desynchronization may result from a combination of widespread neuromodulatory input, and tonic glutamatergic feedback focused on the patch representing the attended stimulus.

Abstract

The brain continuously adapts its processing machinery to behavioural demands. To achieve this, it rapidly modulates the operating mode of cortical circuits, controlling the way that information is transformed and routed. This article will focus on two experimental approaches by which the control of cortical information processing has been investigated: the study of state-dependent cortical processing in rodents and attention in the primate visual system. Both processes involve a modulation of low-frequency activity fluctuations and spiking correlation, and are mediated by common receptor systems. We suggest that selective attention involves processes that are similar to state change, and that operate at a local columnar level to enhance the representation of otherwise non-salient features while suppressing internally generated activity patterns.

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Figure 1: Population activity patterns vary with cortical state.
Figure 2: Cortical local field potential and behaviour.
Figure 3: Possible mechanisms of asynchronous and synchronous activity.
Figure 4: State-dependent responses to punctuate and extended stimuli.
Figure 5: Suggested mechanisms for desynchronization during state changes and attention.

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Acknowledgements

We thank J. Reynolds, H. Dringenberg, R. Malach, S. David and M. Okun for helpful conversations, and G. Buzsaki, M. Carandini and T. Mrsic-Flogel for comments on the manuscript. Research in the Harris laboratory is supported by the US National Institutes of Health (grants MH073245 and DC009947), US National Science Foundation (grant SBE-0542,013 to the Temporal Dynamics of Learning Center), UK Engineering and Physical Sciences Research Council (grant EP/I005102) and a Royal Society Wolfson Research Merit award. Research in the Thiele laboratory is supported by the UK Biotechnology and Biological Sciences Research Council (grant BBS/B/09,325) and the Wellcome Trust (grant 070,380/Z/03/Z).

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Glossary

Electroencephalogram

An electrical recording made from the scalp, which reflects the global structure of cortical synaptic activity.

Local field potential

(LFP). An electrical potential measured from extracellular space. LFP primarily reflects synaptic activity rather than action potential waveforms.

Population rate

The mean of the firing rates of all neurons in a population. The population rate does not denote an average over multiple presentations of a stimulus, but denotes the averaged activity of multiple neurons at a single moment in time.

Depth-negative waves

Local field potential (LFP) waves for which a negativity (or in the case of depth-positive waves, positivity) is seen in the subgranular layers. This laminar specification of the polarity of LFP waves is needed because cortical LFPs typically show a reversal around the middle layers.

Excitable systems

A class of dynamical system models that are used to describe various physical, chemical and biological phenomena. These systems reflect a combination of fast positive feedback that amplifies small perturbations and slower negative feedback that brings the system back to baseline once fluctuations become large.

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Harris, K., Thiele, A. Cortical state and attention. Nat Rev Neurosci 12, 509–523 (2011). https://doi.org/10.1038/nrn3084

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