Distributed and Antagonistic Contributions of Ongoing Activity Fluctuations to Auditory Stimulus Detection

Abstract

Recent studies have shown that ongoing activity fluctuations influence trial-by-trial perception of identical stimuli. Some brain systems seem to bias toward better perceptual performance and others toward worse. We tested whether these observations generalize to another as of yet unassessed sensory modality, audition, and a nonspatial but memory-dependent paradigm. In a sparse event-related functional magnetic resonance imaging design, we investigated detection of auditory near-threshold stimuli as a function of prestimulus baseline activity in early auditory cortex as well as several distributed networks that were defined on the basis of resting state functional connectivity. In accord with previous studies, hits were associated with higher prestimulus activity in related early sensory cortex as well as in a system comprising anterior insula, anterior cingulate, and thalamus, which other studies have related to processing salience and maintaining task set. In contrast to previous studies, however, higher prestimulus activity in the so-called dorsal attention system of frontal and parietal cortex biased toward misses, whereas higher activity in the so-called default mode network that includes posterior cingulate and precuneus biased toward hits. These results contradict a simple dichotomic view on the function of these two latter brain systems where higher ongoing activity in the dorsal attention network would facilitate perceptual performance, and higher activity in the default mode network would deteriorate perceptual performance. Instead, we show that the way in which ongoing activity fluctuations impact on perception depends on the specific sensory (i.e., nonspatial) and cognitive (i.e., mnemonic) context that is relevant.

The prestimulus default mode network state predicts cognitive task performance levels on a mental rotation task

“…However, previous studies suggest that the nature of the relationship between the DMN and task performance has not been uniquely established. While the abovementioned studies show converging evidence for a beneficial role of a reduced DMN state before cognitive task onset, a number of other studies have recently shown a more variable role of the DMN for sensory tasks (Boly et al., 2007; Mayhew et al., 2013; Sadaghiani et al., 2009). These studies employed near‐threshold sensory tasks, on the one hand showing a lower prestimulus activation or connectivity predicted enhanced levels in detection performance (Boly et al., 2007), on the other hand showing a higher prestimulus DMN activation for more intense perception (e.g., more sensitive auditory stimulus detection, more extreme perception during thermal stimulation) of sensory stimuli (Mayhew et al., 2013; Sadaghiani et al., 2009, 2015).…”

“…This peri‐stimulus time window was chosen for the linear contrast analysis as previous research used time points just prior, at stimulus onset or one time point after stimulus onset (as the hemodynamic delay does not cause an effect of stimulus onset on the BOLD response at this time point, compare Hesselmann et al., 2010) to investigate prestimulus effects (e.g., Coste, Sadaghiani, Friston, & Kleinschmidt, 2011; Esterman et al., 2013; Giesbrecht et al., 2006; Hesselmann et al., 2010; Mayhew et al., 2013; Sadaghiani et al., 2009; Soravia et al., 2016). Hereby, the effects can be reliably disentangled from the previous trial and can be interpreted in light of the momentary DMN state just before task onset.…”

“…This evidence for a baseline “preparedness” of task‐related brain regions was soon extended to a more global dimension by uncovering that large‐scale networks constitute different baseline states contributing to different task‐performance levels. More specifically, it has been proposed that spontaneous fluctuations in these networks during the period prior to task onset influence task performance to various degrees, introducing the idea that specific network states affect subsequent performance levels (Colas & Hsieh, 2014; Li, Yan, Bergquist, & Sinha, 2007; Mayhew, Ostwald, Porcaro, & Bagshaw, 2013; Rahnev, Bahdo, de Lange, & Lau, 2012; Sadaghiani, Hesselmann, & Kleinschmidt, 2009; Sadaghiani, Poline, Kleinschmidt, & D'Esposito, 2015; Soravia et al., 2016; Vanhaudenhuyse et al., 2011). …”

“…In fact, it has been proposed that prestimulus activity in the DMN can be linked to subsequent task performance. It was shown that prestimulus DMN activity could predict somatosensory perception (Boly et al., 2007; Mayhew et al., 2013) and auditory stimulus detection (Sadaghiani et al., 2009). More specifically, in studies on prestimulus effects of the DMN on somatosensory and pain perception, Boly et al.…”

“…Conversely, there is other evidence for a higher prestimulus activation in the DMN preceding a more intense perception of painful thermal stimulation (Mayhew et al., 2013). In agreement to this study, auditory stimulus detection was shown to be facilitated when the DMN activation was enhanced before stimulus presentation (Sadaghiani et al., 2009). …”