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J Neurosci. 2019 Jul 10;39(28):5506-5516. doi: 10.1523/JNEUROSCI.3052-18.2019. Epub 2019 May 8.

Interactions between Conscious and Subconscious Signals: Selective Attention under Feature-Based Competition Increases Neural Selectivity during Brain Adaptation.

Author information

1
Institute of Neuroscience, Henry Wellcome Building, Newcastle University, Framlington Place, Newcastle upon Tyne NE2 4HH, United Kingdom, and.
2
Department of Psychology, University of York, Heslington, York YO10 5DD, United Kingdom nick.barraclough@york.ac.uk quoc.vuong@ncl.ac.uk.
3
Institute of Neuroscience, Henry Wellcome Building, Newcastle University, Framlington Place, Newcastle upon Tyne NE2 4HH, United Kingdom, and nick.barraclough@york.ac.uk quoc.vuong@ncl.ac.uk.

Abstract

Efficient perception in natural environments depends on neural interactions between voluntary processes within cognitive control, such as attention, and those that are automatic and subconscious, such as brain adaptation to predictable input (also called repetition suppression). Although both attention and adaptation have been studied separately and there is considerable knowledge of the neurobiology involved in each of these processes, how attention interacts with adaptation remains equivocal. We examined how attention interacts with visual and auditory adaptation by measuring neuroimaging effects consistent with changes in either neural gain or selectivity. Male and female human participants were scanned with functional magnetic resonance imaging (fMRI) first while they discriminated repetition of morphed faces or voices and either directed their attention to stimulus identity or spatial location. Attention to face or voice identity, while ignoring stimulus location, solely increased the gain of respectively face- or voice-sensitive cortex. The results were strikingly different in an experiment when participants attended to voice identity versus stimulus loudness. In this case, attention to voice while ignoring sound loudness increased neural selectivity. The combined results show that how attention affects adaptation depends on the level of feature-based competition, reconciling prior conflicting observations. The findings are theoretically important and are discussed in relation to neurobiological interactions between attention and different types of predictive signals.SIGNIFICANCE STATEMENT Adaptation to repeated environmental events is ubiquitous in the animal brain, an automatic typically subconscious, predictive signal. Cognitive influences, such as by attention, powerfully affect sensory processing and can overcome brain adaptation. However, how neural interactions occur between adaptation and attention remains controversial. We conducted fMRI experiments regulating the focus of attention during adaptation to repeated stimuli with perceptually balanced stimulus expectancy. We observed an interaction between attention and adaptation consistent with increased neural selectivity, but only under conditions of feature-based competition, challenging the notion that attention interacts with brain adaptation by only affecting response gain. This demonstrates that attention retains its full complement of mechanistic influences on sensory cortex even as it interacts with more automatic or subconscious predictive processes.

KEYWORDS:

adaptation; attention; audition; automatic; prediction; vision

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