Visual Stimuli Modulate Local Field Potentials But Drive No High-Frequency Activity in Human Auditory Cortex.

Neuroimaging studies suggest cross-sensory visual influences in human auditory cortices (ACs). Whether these influences reflect active visual processing in human ACs, which drives neuronal firing and concurrent broadband high-frequency activity (BHFA; >70 Hz), or whether they merely modulate sound processing is still debatable. Here, we presented auditory, visual, and audiovisual stimuli to 16 participants (7 women, 9 men) with stereo-EEG depth electrodes implanted near ACs for presurgical monitoring. Anatomically normalized group analyses were facilitated by inverse modeling of intracranial source currents. Analyses of intracranial event-related potentials (iERPs) suggested cross-sensory responses to visual stimuli in ACs, which lagged the earliest auditory responses by several tens of milliseconds. Visual stimuli also modulated the phase of intrinsic low-frequency oscillations and triggered 15-30 Hz event-related desynchronization in ACs. However, BHFA, a putative correlate of neuronal firing, was not significantly increased in ACs after visual stimuli, not even when they coincided with auditory stimuli. Intracranial recordings demonstrate cross-sensory modulations, but no indication of active visual processing in human ACs.

Cortical depth profiles of auditory and visual 7 T functional MRI responses in human superior temporal areas.

Invasive neurophysiological studies in nonhuman primates have shown different laminar activation profiles to auditory vs. visual stimuli in auditory cortices and adjacent polymodal areas. Means to examine the underlying feedforward vs. feedback type influences noninvasively have been limited in humans. Here, using 1-mm isotropic resolution 3D echo-planar imaging at 7 T, we studied the intracortical depth profiles of functional magnetic resonance imaging (fMRI) blood oxygenation level dependent (BOLD) signals to brief auditory (noise bursts) and visual (checkerboard) stimuli. BOLD percent-signal-changes were estimated at 11 equally spaced intracortical depths, within regions-of-interest encompassing auditory (Heschl's gyrus, Heschl's sulcus, planum temporale, and posterior superior temporal gyrus) and polymodal (middle and posterior superior temporal sulcus) areas. Effects of differing BOLD signal strengths for auditory and visual stimuli were controlled via normalization and statistical modeling. The BOLD depth profile shapes, modeled with quadratic regression, were significantly different for auditory vs. visual stimuli in auditory cortices, but not in polymodal areas. The different depth profiles could reflect sensory-specific feedforward versus cross-sensory feedback influences, previously shown in laminar recordings in nonhuman primates. The results suggest that intracortical BOLD profiles can help distinguish between feedforward and feedback type influences in the human brain. Further experimental studies are still needed to clarify how underlying signal strength influences BOLD depth profiles under different stimulus conditions.

Distinct Regional Oscillatory Connectivity Patterns During Auditory Target and Novelty Processing.

Auditory attention allows us to focus on relevant target sounds in the acoustic environment while maintaining the capability to orient to unpredictable (novel) sound changes. An open question is whether orienting to expected vs. unexpected auditory events are governed by anatomically distinct attention pathways, respectively, or by differing communication patterns within a common system. To address this question, we applied a recently developed PeSCAR analysis method to evaluate spectrotemporal functional connectivity patterns across subregions of broader cortical regions of interest (ROIs) to analyze magnetoencephalography data obtained during a cued auditory attention task. Subjects were instructed to detect a predictable harmonic target sound embedded among standard tones in one ear and to ignore the standard tones and occasional unpredictable novel sounds presented in the opposite ear. Phase coherence of estimated source activity was calculated between subregions of superior temporal, frontal, inferior parietal, and superior parietal cortex ROIs. Functional connectivity was stronger in response to target than novel stimuli between left superior temporal and left parietal ROIs and between left frontal and right parietal ROIs, with the largest effects observed in the beta band (15-35 Hz). In contrast, functional connectivity was stronger in response to novel than target stimuli in inter-hemispheric connections between left and right frontal ROIs, observed in early time windows in the alpha band (8-12 Hz). Our findings suggest that auditory processing of expected target vs. unexpected novel sounds involves different spatially, temporally, and spectrally distributed oscillatory connectivity patterns across temporal, parietal, and frontal areas.

Interacting parallel pathways associate sounds with visual identity in auditory cortices.

Spatial and non-spatial information of sound events is presumably processed in parallel auditory cortex (AC) "what" and "where" streams, which are modulated by inputs from the respective visual-cortex subsystems. How these parallel processes are integrated to perceptual objects that remain stable across time and the source agent's movements is unknown. We recorded magneto- and electroencephalography (MEG/EEG) data while subjects viewed animated video clips featuring two audiovisual objects, a black cat and a gray cat. Adaptor-probe events were either linked to the same object (the black cat meowed twice in a row in the same location) or included a visually conveyed identity change (the black and then the gray cat meowed with identical voices in the same location). In addition to effects in visual (including fusiform, middle temporal or MT areas) and frontoparietal association areas, the visually conveyed object-identity change was associated with a release from adaptation of early (50-150ms) activity in posterior ACs, spreading to left anterior ACs at 250-450ms in our combined MEG/EEG source estimates. Repetition of events belonging to the same object resulted in increased theta-band (4-8Hz) synchronization within the "what" and "where" pathways (e.g., between anterior AC and fusiform areas). In contrast, the visually conveyed identity changes resulted in distributed synchronization at higher frequencies (alpha and beta bands, 8-32Hz) across different auditory, visual, and association areas. The results suggest that sound events become initially linked to perceptual objects in posterior AC, followed by modulations of representations in anterior AC. Hierarchical what and where pathways seem to operate in parallel after repeating audiovisual associations, whereas the resetting of such associations engages a distributed network across auditory, visual, and multisensory areas.

Mapping the signal-to-noise-ratios of cortical sources in magnetoencephalography and electroencephalography.

Although magnetoencephalography (MEG) and electroencephalography (EEG) have been available for decades, their relative merits are still debated. We examined regional differences in signal-to-noise-ratios (SNRs) of cortical sources in MEG and EEG. Data from four subjects were used to simulate focal and extended sources located on the cortical surface reconstructed from high-resolution magnetic resonance images. The SNR maps for MEG and EEG were found to be complementary. The SNR of deep sources was larger in EEG than in MEG, whereas the opposite was typically the case for superficial sources. Overall, the SNR maps were more uniform for EEG than for MEG. When using a noise model based on uniformly distributed random sources on the cortex, the SNR in MEG was found to be underestimated, compared with the maps obtained with noise estimated from actual recorded MEG and EEG data. With extended sources, the total area of cortex in which the SNR was higher in EEG than in MEG was larger than with focal sources. Clinically, SNR maps in a patient explained differential sensitivity of MEG and EEG in detecting epileptic activity. Our results emphasize the benefits of recording MEG and EEG simultaneously.

Objective phonological and subjective perceptual characteristics of syllables modulate spatiotemporal patterns of superior temporal gyrus activity.

Natural consonant-vowel syllables are reliably classified by most listeners as voiced or voiceless. However, our previous research [Liederman, J., Frye, R., Fisher, J.M., Greenwood, K., Alexander, R., 2005. A temporally dynamic context effect that disrupts voice onset time discrimination of rapidly successive stimuli. Psychon Bull Rev. 12, 380-386] suggests that among synthetic stimuli varying systematically in voice onset time (VOT), syllables that are classified reliably as voiceless are nonetheless perceived differently within and between listeners. This perceptual ambiguity was measured by variation in the accuracy of matching two identical stimuli presented in rapid succession. In the current experiment, we used magnetoencephalography (MEG) to examine the differential contribution of objective (i.e., VOT) and subjective (i.e., perceptual ambiguity) acoustic features on speech processing. Distributed source models estimated cortical activation within two regions of interest in the superior temporal gyrus (STG) and one in the inferior frontal gyrus. These regions were differentially modulated by VOT and perceptual ambiguity. Ambiguity strongly influenced lateralization of activation; however, the influence on lateralization was different in the anterior and middle/posterior portions of the STG. The influence of ambiguity on the relative amplitude of activity in the right and left anterior STG activity depended on VOT, whereas that of middle/posterior portions of the STG did not. These data support the idea that early cortical responses are bilaterally distributed whereas late processes are lateralized to the dominant hemisphere and support a "how/what" dual-stream auditory model. This study helps to clarify the role of the anterior STG, especially in the right hemisphere, in syllable perception. Moreover, our results demonstrate that both objective phonological and subjective perceptual characteristics of syllables independently modulate spatiotemporal patterns of cortical activation.

Effects of phonological contrast on auditory word discrimination in children with and without reading disability: a magnetoencephalography (MEG) study.

Poor readers perform worse than their normal reading peers on a variety of speech perception tasks, which may be linked to their phonological processing abilities. The purpose of the study was to compare the brain activation patterns of normal and impaired readers on speech perception to better understand the phonological basis in reading disability. Whole-head magnetoencephalography (MEG) was recorded as good and poor readers, 7-13 years of age, performed an auditory word discrimination task. We used an auditory oddball paradigm in which the 'deviant' stimuli (/bat/, /kat/, /rat/) differed in the degree of phonological contrast (one versus three features) from a repeated standard word (/pat/). Both good and poor readers responded more slowly to deviants that were phonologically similar compared to deviants that were phonologically dissimilar to the standard word. Source analysis of the MEG data using minimum norm estimation (MNE) showed that compared to good readers, poor readers had reduced left-hemisphere activation to the most demanding phonological condition reflecting their difficulties with phonological processing. Furthermore, unlike good readers, poor readers did not show differences in activation as a function of the degree of phonological contrast. These results are consistent with a phonological account of reading disability.

Biasing the brain's attentional set: I. cue driven deployments of intersensory selective attention.

Brain activity associated with directing attention to one of two possible sensory modalities was examined using high-density mapping of human event-related potentials. The deployment of selective attention was based on visually presented symbolic cue-words instructing subjects on a trial-by-trial basis, which sensory modality to attend. We measured the spatio-temporal pattern of activation in the approximately 1 second period between the cue-instruction and a subsequent compound auditory-visual imperative stimulus. This allowed us to assess the flow of processing across brain regions involved in deploying and sustaining inter-sensory selective attention, prior to the actual selective processing of the compound audio-visual target stimulus. Activity over frontal and parietal areas showed sensory specific increases in activation during the early part of the anticipatory period (~230 ms), probably representing the activation of fronto-parietal attentional deployment systems for top-down control of attention. In the later period preceding the arrival of the "to-be-attended" stimulus, sustained differential activity was seen over fronto-central regions and parieto-occipital regions, suggesting the maintenance of sensory-specific biased attentional states that would allow for subsequent selective processing. Although there was clear sensory biasing in this late sustained period, it was also clear that both sensory systems were being prepared during the cue-target period. These late sensory-specific biasing effects were also accompanied by sustained activations over frontal cortices that also showed both common and sensory specific activation patterns, suggesting that maintenance of the biased state includes top-down inputs from generators in frontal cortices, some of which are sensory-specific regions. These data support extensive interactions between sensory, parietal and frontal regions during processing of cue information, deployment of attention, and maintenance of the focus of attention in anticipation of impending attentionally relevant input.