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Arousal increases neural gain via the locus coeruleus–noradrenaline system in younger adults but not in older adults

Abstract

In younger adults, arousal amplifies attentional focus to the most salient or goal-relevant information while suppressing other information. A computational model of how the locus coeruleus–noradrenaline system can implement this increased selectivity under arousal and a functional magnetic resonance imaging (fMRI) study comparing how arousal affects younger and older adults’ processing indicate that the amplification of salient stimuli and the suppression of non-salient stimuli are separate processes, with ageing affecting suppression without affecting amplification under arousal. In the fMRI study, arousal increased processing of salient stimuli and decreased processing of non-salient stimuli for younger adults. By contrast, for older adults, arousal increased processing of both low- and high-salience stimuli, generally increasing excitatory responses to visual stimuli. Older adults also showed a decline in locus coeruleus functional connectivity with frontoparietal networks that coordinate attentional selectivity. Thus, among older adults, arousal increases the potential for distraction from non-salient stimuli.

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Fig. 1: A graphical depiction of the proposed mechanisms of the GANE model.
Fig. 2: Order of events during MRI session and during each experimental trial.
Fig. 3: Place area activity during the spatial detection task.
Fig. 4: Computational modelling.
Fig. 5: Age differences in the effects of arousal on frontoparietal activity and how the frontoparietal effects relate to pupil dilation.
Fig. 6: Functional connectivity seed regions and results.
Fig. 7: Comparisons of younger and older adults' functional connectivity patterns among the LC, PPA and frontoparietal network regions.

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Acknowledgements

This work was supported by grants from the National Institute on Aging RO1AG025340 awarded to M.M., JSPS KAKENHI 16H03750 and 15K21062 awarded to T.U., and JSPS KAKENHI 16H05959, 16KT0002 and 16H02053 and European Commission CIG618600 awarded to M.S. We thank C. Cho for assistance with Figs. 1 and 7. The funders had no role in the conceptualization, design, data collection, analysis, decision to publish or preparation of the manuscript.

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T.-H.L. and M.M. designed the study. T.-H.L., S.G.-G. and A.P. acquired the data. Data were analysed by T.-H.L. with S.G.-G., D.C. and M.M. Modelling was conducted by T.U. and M.S. All the authors contributed to the preparation of the manuscript.

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Correspondence to Mara Mather.

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Lee, TH., Greening, S.G., Ueno, T. et al. Arousal increases neural gain via the locus coeruleus–noradrenaline system in younger adults but not in older adults. Nat Hum Behav 2, 356–366 (2018). https://doi.org/10.1038/s41562-018-0344-1

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