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.

Figure 1.

Distribution of percept repetitions. The incidence of repetitions for hits and misses is well approximated by a binomial distribution (goodness-of-fit R² = 0.93 for hits, R² = 0.83 for misses).

Figure 2.

Spatial distribution of evoked cortical responses during successful stimulus detection. Activations evoked in hit trials versus baseline are shown in cold colors (for details, compare supplemental Table 1, available at www.jneurosci.org as supplemental material). A direct comparison of greater responses during hits than misses (warm colors) revealed a very similar activation pattern. Threshold height p < 0.05 corrected at the cluster level using an auxiliary (uncorrected) voxel threshold of p < 0.0001. Group results (n = 11) are superimposed onto the lateral and medial aspects of an inflated cortical surface of a canonical average brain.

Figure 3.

Prestimulus fMRI time courses from bilateral auditory cortex. Left, Map of activation evoked by the near-threshold stimulus (independent of percept) assessed in a group analysis. This map served as the basis for subject-by-subject definition of the auditory ROI (shown on the group's average brain; threshold height p < 0.001 uncorrected; see Materials and Methods for details). Right, In accord with our previous findings, we tested the effect of prestimulus activity at time point 0 s and found significantly higher activity preceding hits than misses (as indicated by an asterisk). Error bars indicate ±SEM.

Figure 4.

Prestimulus time courses from resting-state functional connectivity (rs-fc) networks. Left, Time courses averaged over the complete rs-fc systems. Middle, Rs-fc networks as defined by seed-based analysis of a resting-state scanning session. Numbers indicate regions of interest for which peristimulus activity time courses are plotted in the right-hand panels. Right, Time courses of individual regions of the respective network. While higher signal levels in the default mode system (A) and the intrinsic alertness system (C) were found before successful stimulus detection, higher signal in the dorsal attention system (B) preceded misses. Asterisks indicate significant percept-dependent time course difference at time point 0 s. Error bars indicate ±SEM.

Figure 5.

Statistical parametric maps of difference in prestimulus activity between hit and miss trials. Signal at time point 0 s (as estimated in the FIR-model, see Materials and Methods) was contrasted between hit and miss trials. The resulting second-level maps are shown at p < 0.05 uncorrected to illustrate spatial specificity of prestimulus activity biasing for hits (left) and misses (right), respectively. Asterisks indicate regions with significant effects after correction for multiple comparisons. White arrows indicate Heschl's gyri. Signal time courses over the full peristimulus window are shown in Figures 3 and 4 for largely corresponding but independently defined ROIs and rs-fc networks.