Causal links between parietal alpha activity and spatial auditory attention

Auditory spatial attention serves important functions in auditory source separation and selection. Although auditory spatial attention mechanisms have been generally investigated, the neural substrates encoding spatial information acted on by attention have not been identified in the human neocortex. We performed functional magnetic resonance imaging experiments to identify cortical regions that support auditory spatial attention and to test 2 hypotheses regarding the coding of auditory spatial attention: 1) auditory spatial attention might recruit the visuospatial maps of the intraparietal sulcus (IPS) to create multimodal spatial attention maps; 2) auditory spatial information might be encoded without explicit cortical maps. We mapped visuotopic IPS regions in individual subjects and measured auditory spatial attention effects within these regions of interest. Contrary to the multimodal map hypothesis, we observed that auditory spatial attentional modulations spared the visuotopic maps of IPS; the parietal regions activated by auditory attention lacked map structure. However, multivoxel pattern analysis revealed that the superior temporal gyrus and the supramarginal gyrus contained significant information about the direction of spatial attention. These findings support the hypothesis that auditory spatial information is coded without a cortical map representation. Our findings suggest that audiospatial and visuospatial attention utilize distinctly different spatial coding schemes.

Objective: To establish the modality specificity and generality of selective attention networks.Method: Forty-eight young adults completed a battery of four auditory and visual selective attention tests based upon the Attention Network framework: the visual and auditory Attention Network Tests (vANT, aANT), the Test of Everyday Attention (TEA), and the Test of Attention in Listening (TAiL). These provided independent measures for auditory and visual alerting, orienting, and conflict resolution networks. The measures were subjected to an exploratory factor analysis to assess underlying attention constructs.Results: The analysis yielded a four-component solution. The first component comprised of a range of measures from the TEA and was labeled “general attention.” The third component was labeled “auditory attention,” as it only contained measures from the TAiL using pitch as the attended stimulus feature. The second and fourth components were labeled as “spatial orienting” and “spatial conflict,” respectively—they were comprised of orienting and conflict resolution measures from the vANT, aANT, and TAiL attend-location task—all tasks based upon spatial judgments (e.g., the direction of a target arrow or sound location).Conclusions: These results do not support our a-priori hypothesis that attention networks are either modality specific or supramodal. Auditory attention separated into selectively attending to spatial and non-spatial features, with the auditory spatial attention loading onto the same factor as visual spatial attention, suggesting spatial attention is supramodal. However, since our study did not include a non-spatial measure of visual attention, further research will be required to ascertain whether non-spatial attention is modality-specific.

Top-down spatial attention is effective at selecting a target sound from a mixture. However, nonspatial features often distinguish sources in addition to location. This study explores whether redundant nonspatial features are used to maintain selective auditory attention for a spatially defined target. We recorded electroencephalography while subjects focused attention on one of three simultaneous melodies. In one experiment, subjects (n = 17) were given an auditory cue indicating both the location and pitch of the target melody. In a second experiment (n = 17 subjects), the cue only indicated target location, and we compared two conditions: one in which the pitch separation of competing melodies was large, and one in which this separation was small. In both experiments, responses evoked by onsets of events in sound streams were modulated by attention, and we found no significant difference in this modulation between small and large pitch separation conditions. Therefore, the evoked response reflected that target stimuli were the focus of attention, and distractors were suppressed successfully for all experimental conditions. In all cases, parietal alpha was lateralized following the cue, but before melody onset, indicating that subjects initially focused attention in space. During the stimulus presentation, this lateralization disappeared when pitch cues were strong but remained significant when pitch cues were weak, suggesting that strong pitch cues reduced reliance on sustained spatial attention. These results demonstrate that once a well-defined target stream at a known location is selected, top-down spatial attention plays a weak role in filtering out a segregated competing stream.

A short period of adaptation to a prismatic shift of the visual field to the right briefly but significantly improves left unilateral spatial neglect. Additionally, prism adaptation affects multiple modalities, including processes of vision, auditory spatial attention, and sound localization. This non-randomized, single-center, controlled trial aimed to examine the immediate effects of prism adaptation on the sound-localization abilities of patients with left unilateral spatial neglect using a simple source localization test. Subjects were divided by self-allocation into a prism-adaptation group (n = 11) and a control group (n = 12). At baseline, patients with left unilateral spatial neglect showed a rightward deviation tendency in the left space. This tendency to right-sided bias in the left space was attenuated after prism adaptation. However, no changes were observed in the right space of patients with left unilateral spatial neglect after prism adaptation, or in the control group. Our results suggest that prism adaptation improves not only vision and proprioception but also auditory attention in the left space of patients with left unilateral spatial neglect. Our findings demonstrate that a single session of prism adaptation can significantly improve sound localization in patients with left unilateral spatial neglect. However, in this study, it was not possible to accurately determine whether the mechanism was a chronic change in head orientation or a readjustment of the spatial representation of the brain; thus, further studies need to be considered.

There has been no consistent conclusion concerning whether auditory spatial attention or visual spatial attention could be modulated by auditory aversive cues. In three experiments, we used direct aversive auditory stimuli (white noise) as cues and explored which subcomponents of attentional bias contribute to auditory and cross-modal spatial attention in unselected samples. In Experiment 1, in a dot-probe paradigm, we adopted auditory stimuli (aversive or neutral) as cues and a tick sound as target, and we set two stimulus onset asynchrony (SOA) conditions: 150 ms and 500 ms. The results of experiment 1 showed that participants performed faster on congruent trials than on incongruent trials and participants exhibited an auditory emotional attentional bias to aversive auditory stimuli in 150 ms SOA condition. Subsequently, in experiment 2 and experiment 3, we employed an auditory emotional spatial cueing task using neutral and negative auditory stimuli as cues. Targets were auditory stimuli (Experiment 2) or visual stimuli (Experiment 3). The results of experiment 2 showed that participants performed faster to targets primed by negative cues than to those primed by neutral cues in valid condition; and performed slower to targets primed by negative cues than to those primed by neutral cues in invalid condition in 150 ms SOA condition. Experiment 2 revealed that speeded engagement with and delayed disengagement from aversive auditory stimuli were both present at a 150 ms SOA condition; at 500 ms SOA condition, only the former effect was present, and auditory inhibition of return was also observed. Experiment 3 produced similar results cross-modally, but cross-modal inhibition of return was not observed. In all experiments, we conclude that emotional attention can operate within the auditory modality and across sensory modalities, and that both engagement and disengagement bias contribute to auditory and cross-modal emotional attention.

Autism Spectrum Disorder (ASD) is a developmental condition characterized by difficulties in social interaction, communication, and sensory processing. The ability to orient towards sounds is a key component of social interactions, yet auditory spatial attention remains relatively understudied in ASD, despite prior research indicating differences in this domain. Here, we investigate the neural signatures associated with passive auditory spatial attention in children with ASD (n = 21, ages 6-17) relative to age- and IQ-matched Typically Developing (TD) children (n = 31), using source-localized magnetoencephalography (MEG). Participants listened passively, while watching a silenced movie, to non-social auditory stimuli designed to either remain lateralized to one hemifield (stay trials) or to change in location from one side to the contralateral hemifield (jump trials). Linear mixed effects modeling showed lower cortical activation in the auditory cortex in the ASD group in response to jump trials, relative to the TD group. Additionally, functional connectivity analyses showed higher alpha-band functional connectivity in the ASD group between left auditory cortex seeds and right prefrontal and left parietal regions known to be recruited during auditory spatial attention. Right prefrontal alpha-band connectivity estimates were associated with behaviorally assessed auditory processing scores, whereas left parietal connectivity estimates were associated with ASD symptomatology. Our results align with the hypothesis that auditory spatial attention generally, and specifically orientation to sounds even when experienced passively, differs in ASD versus TD children.

Early blind people compensate for their lack of vision by developing superior abilities in the remaining senses such as audition (Collignon et al., 2006; Gougoux et al., 2004; Wan et al., 2010). Previous studies reported supra-normal abilities in auditory spatial attention, particularly for the localization of peripheral stimuli in comparison with frontal stimuli (Lessard et al., 1998; Röder et al., 1999). However, it is unknown whether this specific supra-normal ability extends to the non-spatial attention domain. Here we compared the performance of early blind subjects and sighted controls, who were blindfolded, during an auditory non-spatial attention task: target detection among distractors according to tone frequency. We paid a special attention to the potential effect of the sound source location, comparing the accuracy and speed in target detection in the peripheral and frontal space. Blind subjects displayed shorter reaction times than sighted controls for both peripheral and frontal stimuli. Moreover, in the two groups of subjects, we observed an interaction effect between the target location and the distractors location: the target was detected faster when its location was different from the location of the distractors. However, this effect was attenuated in early blind subjects and even cancelled in the condition with frontal targets and peripheral distractors. We conclude that early blind people compensate for the lack of vision by enhancing their ability to process auditory information but also by changing the spatial distribution of their auditory attention resources.

Auditory spatial attention was investigated by manipulating spatial and temporal relations between an auditory spatial cue and an auditory target. The principal findings were that performance improved as time available to shift attention to a cued spatial position increased, accurate spatial cues facilitated performance more than inaccurate cues, performance was virtually identical for shifts of attention ranging from 0 degrees and 180 degrees, and performance declined as the distance of an unexpected target from a cued spatial location increased. The experiments provided evidence that auditory attention may be allocated to a specific location in response to an auditory spatial cue and that the time required to shift attention does not appear to depend on the distance of the shift. Furthermore, the findings suggest that the spatial distribution of auditory attention may be described most accurately by a gradient model in which attentional resources decline gradually with distance from a focal point.

Recent work in our laboratory has suggested that human caudal lateral frontal cortex contains four interleaved regions in each hemisphere that exhibit strong sensory-specific biases in attention tasks (Michalka et al, 2014). Two visually-biased attention regions, superior and inferior pre-central sulcus (sPCS, iPCS), anatomically alternate with two auditory-biased attention regions, caudal inferior frontal sulcus (cIFS) and the transverse gyrus intersection the precentral sulcus (tgPCS). These small regions were identified in fMRI studies in a small number of individual subjects. Here, we have investigated these regions and their putative networks by mining the WashU-Minn Human Connectome Project (HCP) dataset. We used data from the 482 HCP participants with both diffusion-weighted imaging and resting-state fMRI. We defined seed regions from our individual subject data in a task that contrasted auditory and visual spatial attention. Probabilistic activation maps were constructed and thresholded to generate ROIs. These ROIs served as seed regions for resting state and tractography analyses of the HCP dataset. Stronger functional connectivity was observed for the sPCS and iPCS than for tgPCS and cIFS with superior parietal lobule visual attention regions, and conversely stronger connectivity was observed for the tgPCS and cIFS than for sPCS and iPCS with superior temporal lobe auditory attention regions. A similar pattern was observed with tractography for all ROIs, except for tgPCS. We next analyzed the whole-brain connectivity patterns of these ROIs using a multivariate approach; we found that the modality of sensory-bias can be predicted well above chance in both hemispheres at a voxelwise scale (L:71%, R:80%), using only the connectivity pattern of an individual voxel. A long-term goal of this analysis is to develop reliable methods for identifying fine-scale brain networks in large population datasets, which could have important clinical applications. Our preliminary results reveal both successes and challenges of these efforts. Meeting abstract presented at VSS 2015

Enhancing spatial auditory attention decoding with wavelet-based prototype training

Selective attention can be a useful tactic for speech-in-noise (SiN) interpretation as it strengthens cortical responses to attended sensory inputs while suppressing others. This cortical process is referred to as attentional modulation. Our earlier study showed that a neurofeedback training paradigm was effective for improving the attentional modulation of cortical auditory evoked responses. However, it was unclear how such neurofeedback training improved attentional modulation. This paper attempts to unveil what neural mechanisms underlie strengthened auditory selective attention during the neurofeedback training paradigm. Our EEG time–frequency analysis found that, when spatial auditory attention was focused, a fronto-parietal brain network was activated. Additionally, the neurofeedback training increased beta oscillation, which may imply top-down processing was used to anticipate the sound to be attended selectively with prior information. When the subjects were attending to the sound from the right, they exhibited more alpha oscillation in the right parietal cortex during the final session compared to the first, indicating improved spatial inhibitory processing to suppress sounds from the left. After the four-week training period, the temporal cortex exhibited improved attentional modulation of beta oscillation. This suggests strengthened neural activity to predict the target. Moreover, there was an improvement in the strength of attentional modulation on cortical evoked responses to sounds. The Placebo Group, who experienced similar attention training with the exception that feedback was based simply on behavioral accuracy, did not experience these training effects. These findings demonstrate how neurofeedback training effectively improves the neural mechanisms underlying auditory selective attention.

Long-term memory (LTM) has been shown to bias attention to a previously learned visual target location. Here, we examined whether memory-predicted spatial location can facilitate the detection of a faint pure tone target embedded in real world audio clips (e.g., soundtrack of a restaurant). During an initial familiarization task, participants heard audio clips, some of which included a lateralized target (p = 50%). On each trial participants indicated whether the target was presented from the left, right, or was absent. Following a 1 hr retention interval, participants were presented with the same audio clips, which now all included a target. In Experiment 1, participants showed memory-based gains in response time and d'. Experiment 2 showed that temporal expectations modulate attention, with greater memory-guided attention effects on performance when temporal context was reinstated from learning (i.e., when timing of the target within audio clips was not changed from initially learned timing). Experiment 3 showed that while conscious recall of target locations was modulated by exposure to target-context associations during learning (i.e., better recall with higher number of learning blocks), the influence of LTM associations on spatial attention was not reduced (i.e., number of learning blocks did not affect memory-guided attention). Both Experiments 2 and 3 showed gains in performance related to target-context associations, even for associations that were not explicitly remembered. Together, these findings indicate that memory for audio clips is acquired quickly and is surprisingly robust; both implicit and explicit LTM for the location of a faint target tone modulated auditory spatial attention. (PsycINFO Database Record

Behavioral studies support the concept of an auditory spatial attention gradient by demonstrating that attentional benefits progressively diminish as distance increases from an attended location. Damage to the right inferior parietal cortex can induce a rightward attention bias, which implicates this region in the construction of attention gradients. This study used event-related potentials (ERPs) to define attention-related gradients before and after repetitive transcranial magnetic stimulation (rTMS) to the right inferior parietal cortex. Subjects (n = 16) listened to noise bursts at five azimuth locations (left to right: -90°, -45°, 0° midline, +45°, +90°) and responded to stimuli at one target location (-90°, +90°, separate blocks). ERPs as a function of non-target location were examined before (baseline) and after 0.9 Hz rTMS. Results showed that ERP attention gradients were observed in three time windows (frontal 230–340, parietal 400–460, frontal 550–750 ms). Significant transient rTMS effects were seen in the first and third windows. The first window had a voltage decrease at the farthest location when attending to either the left or right side. The third window had on overall increase in positivity, but only when attending to the left side. These findings suggest that rTMS induced a small contraction in spatial attention gradients within the first time window. The asymmetric effect of attended location on gradients in the third time window may relate to neglect of the left hemispace after right parietal injury. Together, these results highlight the role of the right inferior parietal cortex in modulating frontal lobe attention network activity.

Attention control is a core element of cognitive aging, but the specific mechanisms that differ with age are unclear. Here we used a novel auditory spatial attention task to evaluate stimulus processing at the level of early attention capture, later response selection, and thelingering effects of attention capture across trials in young and older adults. We found that the shapes of spatial attention capture gradients were remarkably similar in young and older adults, but only the older group had lingering effects of attention capture on the next trial. Response selection for stimulus-response incompatibilities took longer in older subjects, but primarily when attending to the midline location. The results suggest that the likelihood and spatial tuning of attention capture is comparable among groups, but once attention is captured, older subjects take longer to disengage. Age differences in response selection were supported, but may not be a general feature of cognitive aging.

The effects of auditory spatial attention on event‐related brain potentials (ERPs) were examined in situations that promoted stream segregation. Short and long noise bursts were presented at three azimuth locations and listeners were asked to respond to the longer sounds occurring at either the right‐ or left‐most location. In the baseline condition, the three sound sources were evenly spaced apart. In the distractor clustering conditions, middle and far sounds were clustered. In the attended clustering conditions, middle and attended sounds were clustered. ERP indices of attention, isolated as negative difference (Nd) waves, were greater over the hemisphere contralateral to the attended location. Nd waves were also larger when the middle sounds were moved toward the far distractors, consistent with an object‐based gradient of auditory attention in which higher order information provided by the perceptual context influences selective processing.