We used pupil diameter as a proxy for arousal ( Beatty, 1982 Bradshaw, 1967 Hess and Polt, 1964 Kahneman et al., 1967 Kahneman and Beatty, 1966). In this report, we comprehensively show how this structural and molecular heterogeneity translates into a multitude of arousal effects on neuronal population activity across the human cortex. In addition, neuromodulator receptors exhibit a rich and diverse distribution across the cortex ( Burt et al., 2018 van den Brink et al., 2019). More recently, however, this view has been challenged: Several neuronal subpopulations with distinct projection targets have been found in both the LC and BF ( Chandler et al., 2013 Chandler et al., 2019 Sarter et al., 2009 Schwarz and Luo, 2015 Totah et al., 2018 Zaborszky et al., 2015 Záborszky et al., 2018). This has led to the idea that the arousal system acts as a global ‘ broadcast signal’ and uniform controller of cortical state ( Aston-Jones and Cohen, 2005 Harris and Thiele, 2011 Leopold et al., 2003 Turchi et al., 2018). It has long been thought that these nuclei are organized homogeneously and innervate cortical target regions diffusely, and indiscriminately across cortical regions. Two key mediators of arousal-dependent variations are the brainstem nucleus locus coeruleus (LC), which supplies noradrenaline (NE), and the basal forebrain (BF), which supplies acetylcholine (ACh) ( Harris and Thiele, 2011 Hasselmo, 1995 Lee and Dan, 2012 Steriade, 1996). These variations occur continuously due to subtle fluctuations in the level of arousal, and even in the absence of changes in overt behavior ( Harris and Thiele, 2011 McGinley et al., 2015b). Variations in cortical state profoundly shape information processing and, thus, cognition ( Busse et al., 2017 Fu et al., 2014 Zagha et al., 2013). Our results provide a novel basis for studying the arousal modulation of cognitive computations in cortical circuits. Pupil-linked arousal also coincided with widespread changes in the structure of the aperiodic component of cortical population activity, indicative of changes in the excitation-inhibition balance in underlying microcircuits. We found a cascade of effects relative to the peak timing of spontaneous pupil dilations: Decreases in low-frequency (2–8 Hz) activity in temporal and lateral frontal cortex, followed by increased high-frequency (>64 Hz) activity in mid-frontal regions, followed by monotonic and inverted U relationships with intermediate frequency-range activity (8–32 Hz) in occipito-parietal regions. Exploiting the established link between pupil size and central arousal systems, we performed concurrent magnetoencephalographic (MEG) and pupillographic recordings in a large number of participants, pooled across three laboratories. Here, we provide a comprehensive account of the relationships between fluctuations in arousal and neuronal population activity across the human brain. Recent insights, however, point to a higher specificity of arousal effects on different components of neural activity and across cortical regions. Traditional accounts conceptualize arousal as a homogeneous modulator of neural population activity across the cerebral cortex. Yet, how arousal signals influence cortical population activity in detail has so far only been characterized for a few selected brain regions. Fluctuations in arousal, controlled by subcortical neuromodulatory systems, continuously shape cortical state, with profound consequences for information processing.
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