A double dissociation between anterior and posterior superior temporal gyrus for processing audiovisual speech demonstrated by electrocorticography

Human speech can be comprehended using only auditory information from the talker's voice. However, comprehension is improved if the talker's face is visible, especially if the auditory information is degraded as occurs in noisy environments or with hearing loss. We explored the neural substrates of audiovisual speech perception using electrocorticography, direct recording of neural activity using electrodes implanted on the cortical surface. We observed a double dissociation in the responses to audiovisual speech with clear and noisy auditory component within the superior temporal gyrus (STG), a region long known to be important for speech perception. Anterior STG showed greater neural activity to audiovisual speech with clear auditory component, whereas posterior STG showed similar or greater neural activity to audiovisual speech in which the speech was replaced with speech-like noise. A distinct border between the two response patterns was observed, demarcated by a landmark corresponding to the posterior margin of Heschl's gyrus. To further investigate the computational roles of both regions, we considered Bayesian models of multisensory integration, which predict that combining the independent sources of information available from different modalities should reduce variability in the neural responses. We tested this prediction by measuring the variability of the neural responses to single audiovisual words. Posterior STG showed smaller variability than anterior STG during presentation of audiovisual speech with noisy auditory component. Taken together, these results suggest that posterior STG but not anterior STG is important for multisensory integration of noisy auditory and visual speech

Investigating the Neural Basis of Audiovisual Speech Perception with Intracranial Recordings in Humans

Speech is inherently multisensory, containing auditory information from the voice and visual information from the mouth movements of the talker. Hearing the voice is usually sufficient to understand speech, however in noisy environments or when audition is impaired due to aging or disabilities, seeing mouth movements greatly improves speech perception. Although behavioral studies have well established this perceptual benefit, it is still not clear how the brain processes visual information from mouth movements to improve speech perception. To clarify this issue, I studied the neural activity recorded from the brain surfaces of human subjects using intracranial electrodes, a technique known as electrocorticography (ECoG). First, I studied responses to noisy speech in the auditory cortex, specifically in the superior temporal gyrus (STG). Previous studies identified the anterior parts of the STG as unisensory, responding only to auditory stimulus. On the other hand, posterior parts of the STG are known to be multisensory, responding to both auditory and visual stimuli, which makes it a key region for audiovisual speech perception. I examined how these different parts of the STG respond to clear versus noisy speech. I found that noisy speech decreased the amplitude and increased the across-trial variability of the response in the anterior STG. However, possibly due to its multisensory composition, posterior STG was not as sensitive to auditory noise as the anterior STG and responded similarly to clear and noisy speech. I also found that these two response patterns in the STG were separated by a sharp boundary demarcated by the posterior-most portion of the Heschl’s gyrus. Second, I studied responses to silent speech in the visual cortex. Previous studies demonstrated that visual cortex shows response enhancement when the auditory component of speech is noisy or absent, however it was not clear which regions of the visual cortex specifically show this response enhancement and whether this response enhancement is a result of top-down modulation from a higher region. To test this, I first mapped the receptive fields of different regions in the visual cortex and then measured their responses to visual (silent) and audiovisual speech stimuli. I found that visual regions that have central receptive fields show greater response enhancement to visual speech, possibly because these regions receive more visual information from mouth movements. I found similar response enhancement to visual speech in frontal cortex, specifically in the inferior frontal gyrus, premotor and dorsolateral prefrontal cortices, which have been implicated in speech reading in previous studies. I showed that these frontal regions display strong functional connectivity with visual regions that have central receptive fields during speech perception

Visual speech differentially modulates beta, theta, and high gamma bands in auditory cortex

Speech perception is a central component of social communication. While principally an auditory process, accurate speech perception in everyday settings is supported by meaningful information extracted from visual cues (e.g., speech content, timing, and speaker identity). Previous research has shown that visual speech modulates activity in cortical areas subserving auditory speech perception, including the superior temporal gyrus (STG), potentially through feedback connections from the multisensory posterior superior temporal sulcus (pSTS). However, it is unknown whether visual modulation of auditory processing in the STG is a unitary phenomenon or, rather, consists of multiple temporally, spatially, or functionally distinct processes. To explore these questions, we examined neural responses to audiovisual speech measured from intracranially implanted electrodes within the temporal cortex of 21 patients undergoing clinical monitoring for epilepsy. We found that visual speech modulates auditory processes in the STG in multiple ways, eliciting temporally and spatially distinct patterns of activity that differ across theta, beta, and high-gamma frequency bands. Before speech onset, visual information increased high-gamma power in the posterior STG and suppressed beta power in mid-STG regions, suggesting crossmodal prediction of speech signals in these areas. After sound onset, visual speech decreased theta power in the middle and posterior STG, potentially reflecting a decrease in sustained feedforward auditory activity. These results are consistent with models that posit multiple distinct mechanisms supporting audiovisual speech perception and provide a crucial map for subsequent studies to identify the types of visual features that are encoded by these separate mechanisms.This study was supported by NIH Grant R00 DC013828 A. Beltz was supported by the Jacobs Foundation.http://deepblue.lib.umich.edu/bitstream/2027.42/167729/1/OriginalManuscript.pdfDescription of OriginalManuscript.pdf : Preprint of the article "Multiple auditory responses to visual speech"SEL

A speech envelope landmark for syllable encoding in human superior temporal gyrus.

The most salient acoustic features in speech are the modulations in its intensity, captured by the amplitude envelope. Perceptually, the envelope is necessary for speech comprehension. Yet, the neural computations that represent the envelope and their linguistic implications are heavily debated. We used high-density intracranial recordings, while participants listened to speech, to determine how the envelope is represented in human speech cortical areas on the superior temporal gyrus (STG). We found that a well-defined zone in middle STG detects acoustic onset edges (local maxima in the envelope rate of change). Acoustic analyses demonstrated that timing of acoustic onset edges cues syllabic nucleus onsets, while their slope cues syllabic stress. Synthesized amplitude-modulated tone stimuli showed that steeper slopes elicited greater responses, confirming cortical encoding of amplitude change, not absolute amplitude. Overall, STG encoding of the timing and magnitude of acoustic onset edges underlies the perception of speech temporal structure

How Learning to Read Changes the Listening Brain

Reading acquisition reorganizes existing brain networks for speech and visual processing to form novel audio-visual language representations. This requires substantial cortical plasticity that is reflected in changes in brain activation and functional as well as structural connectivity between brain areas. The extent to which a child’s brain can accommodate these changes may underlie the high variability in reading outcome in both typical and dyslexic readers. In this review, we focus on reading-induced functional changes of the dorsal speech network in particular and discuss how its reciprocal interactions with the ventral reading network contributes to reading outcome. We discuss how the dynamic and intertwined development of both reading networks may be best captured by approaching reading from a skill learning perspective, using audio-visual learning paradigms and longitudinal designs to follow neuro-behavioral changes while children’s reading skills unfold

Semantic radical consistency and character transparency effects in Chinese: an ERP study

BACKGROUND: This event-related potential (ERP) study aims to investigate the representation and temporal dynamics of Chinese orthography-to-semantics mappings by simultaneously manipulating character transparency and semantic radical consistency. Character components, referred to as radicals, make up the building blocks used dur...postprin

Sensorimotor Modulations by Cognitive Processes During Accurate Speech Discrimination: An EEG Investigation of Dorsal Stream Processing

Internal models mediate the transmission of information between anterior and posterior regions of the dorsal stream in support of speech perception, though it remains unclear how this mechanism responds to cognitive processes in service of task demands. The purpose of the current study was to identify the influences of attention and working memory on sensorimotor activity across the dorsal stream during speech discrimination, with set size and signal clarity employed to modulate stimulus predictability and the time course of increased task demands, respectively. Independent Component Analysis of 64–channel EEG data identified bilateral sensorimotor mu and auditory alpha components from a cohort of 42 participants, indexing activity from anterior (mu) and posterior (auditory) aspects of the dorsal stream. Time frequency (ERSP) analysis evaluated task-related changes in focal activation patterns with phase coherence measures employed to track patterns of information flow across the dorsal stream. ERSP decomposition of mu clusters revealed event-related desynchronization (ERD) in beta and alpha bands, which were interpreted as evidence of forward (beta) and inverse (alpha) internal modeling across the time course of perception events. Stronger pre-stimulus mu alpha ERD in small set discrimination tasks was interpreted as more efficient attentional allocation due to the reduced sensory search space enabled by predictable stimuli. Mu-alpha and mu-beta ERD in peri- and post-stimulus periods were interpreted within the framework of Analysis by Synthesis as evidence of working memory activity for stimulus processing and maintenance, with weaker activity in degraded conditions suggesting that covert rehearsal mechanisms are sensitive to the quality of the stimulus being retained in working memory. Similar ERSP patterns across conditions despite the differences in stimulus predictability and clarity, suggest that subjects may have adapted to tasks. In light of this, future studies of sensorimotor processing should consider the ecological validity of the tasks employed, as well as the larger cognitive environment in which tasks are performed. The absence of interpretable patterns of mu-auditory coherence modulation across the time course of speech discrimination highlights the need for more sensitive analyses to probe dorsal stream connectivity

Evidence for causal top-down frontal contributions to predictive processes in speech perception

Perception relies on the integration of sensory information and prior expectations. Here we show that selective neurodegeneration of human frontal speech regions results in delayed reconciliation of predictions in temporal cortex. These temporal regions were not atrophic, displayed normal evoked magnetic and electrical power, and preserved neural sensitivity to manipulations of sensory detail. Frontal neurodegeneration does not prevent the perceptual effects of contextual information; instead, prior expectations are applied inflexibly. The precision of predictions correlates with beta power, in line with theoretical models of the neural instantiation of predictive coding. Fronto-temporal interactions are enhanced while participants reconcile prior predictions with degraded sensory signals. Excessively precise predictions can explain several challenging phenomena in frontal aphasias, including agrammatism and subjective difficulties with speech perception. This work demonstrates that higher-level frontal mechanisms for cognitive and behavioural flexibility make a causal functional contribution to the hierarchical generative models underlying speech perception.This study was supported by the National Institute for Health Research, the Association of British Neurologists and Patrick Berthoud Charitable Trust (TEC fellowship); the Wellcome Trust (JBR Senior Fellowship, 103838); the Evelyn Trust; and the Medical Research Council Cognition and Brain Sciences unit (MC-A060-5PQ30, MC-A060-5PQ80)

The hearing hippocampus

The hippocampus has a well-established role in spatial and episodic memory but a broader function has been proposed including aspects of perception and relational processing. Neural bases of sound analysis have been described in the pathway to auditory cortex, but wider networks supporting auditory cognition are still being established. We review what is known about the role of the hippocampus in processing auditory information, and how the hippocampus itself is shaped by sound. In examining imaging, recording, and lesion studies in species from rodents to humans, we uncover a hierarchy of hippocampal responses to sound including during passive exposure, active listening, and the learning of associations between sounds and other stimuli. We describe how the hippocampus' connectivity and computational architecture allow it to track and manipulate auditory information – whether in the form of speech, music, or environmental, emotional, or phantom sounds. Functional and structural correlates of auditory experience are also identified. The extent of auditory-hippocampal interactions is consistent with the view that the hippocampus makes broad contributions to perception and cognition, beyond spatial and episodic memory. More deeply understanding these interactions may unlock applications including entraining hippocampal rhythms to support cognition, and intervening in links between hearing loss and dementia