Dynamic oscillatory processes governing cued orienting and allocation of auditory attention

Abstract

In everyday listening situations, we need to constantly switch between alternative sound sources and engage attention according to cues that match our goals and expectations. The exact neuronal bases of these processes are poorly understood. We investigated oscillatory brain networks controlling auditory attention using cortically constrained fMRI-weighted magnetoencephalography/EEG source estimates. During consecutive trials, participants were instructed to shift attention based on a cue, presented in the ear where a target was likely to follow. To promote audiospatial attention effects, the targets were embedded in streams of dichotically presented standard tones. Occasionally, an unexpected novel sound occurred opposite to the cued ear to trigger involuntary orienting. According to our cortical power correlation analyses, increased frontoparietal/temporal 30-100 Hz gamma activity at 200-1400 msec after cued orienting predicted fast and accurate discrimination of subsequent targets. This sustained correlation effect, possibly reflecting voluntary engagement of attention after the initial cue-driven orienting, spread from the TPJ, anterior insula, and inferior frontal cortices to the right FEFs. Engagement of attention to one ear resulted in a significantly stronger increase of 7.5-15 Hz alpha in the ipsilateral than contralateral parieto-occipital cortices 200-600 msec after the cue onset, possibly reflecting cross-modal modulation of the dorsal visual pathway during audiospatial attention. Comparisons of cortical power patterns also revealed significant increases of sustained right medial frontal cortex theta power, right dorsolateral pFC and anterior insula/inferior frontal cortex beta power, and medial parietal cortex and posterior cingulate cortex gamma activity after cued versus novelty-triggered orienting (600-1400 msec). Our results reveal sustained oscillatory patterns associated with voluntary engagement of auditory spatial attention, with the frontoparietal and temporal gamma increases being best predictors of subsequent behavioral performance.

Figure 1

Task and stimuli. During 10-s trials, subjects heard a cue in the ear where a subsequent target, a harmonic sound within pure-tone trains consisting of randomly ordered 800-Hz left-ear and 1500-Hz right-ear tones (Hillyard et al., 1973), was likely to appear. The task was to shift attention to the cued ear, wait for the target, and to press a button as quickly as possible upon hearing the target. Novel sounds, which occasionally occurred opposite to the cued ear, were to be ignored. Each trial ended to a 2.18-s sound, the fMRI scanning noise or recorded simulation during MEG/EEG (i.e., fMRI was obtained with a sparse-sampling approach with other sounds presented in-between scans). Four types of trials were utilized similarly during fMRI and MEG/EEG, including Cue/Target (40%), Cue/Novel (20%), Cue/No target (20%), and Standards Only (20%). The stimulus-onset asynchrony (SOA) was jittered at 350–750 ms to mitigate expectancy confounds such as omission responses (there was at least 650 ms period after cues, targets, and novels).

Figure 2

Goal-driven engagement of attention estimated by correlation analyses between post-cue/pre-target oscillations and behavioral performance. Fast and accurate behavioral performance, as measured with IES (RT/HR, unit ms, smaller value represents improved performance) (Townsend & Ashby, 1978), correlated with increased oscillatory power at the lower (30–60 Hz) and higher (60–100 Hz) gamma bands. Significant correlations (cluster-based Monte Carlo simulation test) started earlier (0.2–0.6 s) in the right hemisphere, and subsequently (0.6–1.4 s) spread also to the left hemisphere. These gamma correlation patterns emerged first in the temporoparietal junction, auditory cortices, anterior temporal cortex, anterior insula, and inferior frontal cortex. In the later time window, a strong correlation at the higher gamma band emerged also in an area corresponding to the right frontal eye fields. No significant correlations were observed in the other frequency bands. The figure shows the significance of initial GLM, masked to the locations that survived the post-hoc correction based on the cluster-based Monte Carlo simulation test. All estimates are normalized relative to a 500-ms pre-stimulus baseline before statistical analyses.

Figure 3

Lateralized power changes after engagement of attention to left vs. right ears. The clearest lateralization pattern is observed at the alpha band, 200-600 ms after cue onset. A significant (cluster-based Monte Carlo simulation test) increase of alpha power is observed when attention is directed to the ipsilateral vs. contralateral ear, as reflected by a positive Attend Left vs. Attend Right contrast in the left and negative Attend Left vs. Attend Right contrast in the right hemisphere. This ipsilateral alpha enhancement effect seems to be more widespread and longer lasting in the right hemisphere, where it also extends to the theta and beta ranges. At the theta range, an early power decrease was also observed in the left sensorimotor areas that are close to the right-hand representation, as well as in the left secondary somatosensory area. In these areas, the power is significantly increased when attention is directed to the contralateral hemisphere (i.e., Attend Right > Attend Left). Finally, indices of lateralized gamma power increases were observed in the right inferior temporal visual cortices when attention is directed to the contralateral ear. The figure shows the significance values of initial GLM, masked to the locations that survived the post-hoc correction based on the cluster-based Monte Carlo simulation test. All estimates are normalized relative to a 500-ms pre-stimulus baseline before statistical analyses.

Figure 4

Comparisons of power estimates to cued vs. novelty-triggered attention shifting. At the theta range, an increase of right medial frontal cortex/ACC theta power was observed during 0.6–1.4 s (encircled with white rectangle), consistent with previous observations of midline theta increases after allocation of selective attention. This effect coincided with a beta power increase in the right anterior insular /DLPFC regions (white rectangle on the right). In addition, there was evidence for suppression of sensorimotor mu rhythm power (alpha/beta ranges) near the right hand representations, possibly reflecting motor preparation for the upcoming target. In the posterior medial surfaces (the precuneus and retrosplenial complex), alpha and beta power increased at 0.2-0.6 s, and this effect was followed by a bilateral lower gamma-band power increase at 0.6–1.4 s. This later gamma pattern also extended to the posterior cingulate cortex. No significant effects emerged at the higher gamma band (not shown). The figure shows the significance values of initial GLM, masked to the locations that survived the post-hoc correction based on the cluster-based Monte Carlo simulation test. All estimates are normalized relative to a 500-ms pre-stimulus baseline before statistical analyses.