The processing of audio-visual speech: empirical and neural bases

In this selective review, I outline a number of ways in which seeing the talker affects auditory perception of speech, including, but not confined to, the McGurk effect. To date, studies suggest that all linguistic levels are susceptible to visual influence, and that two main modes of processing can be described: a complementary mode, whereby vision provides information more efficiently than hearing for some under-specified parts of the speech stream, and a correlated mode, whereby vision partially duplicates information about dynamic articulatory patterning.Cortical correlates of seen speech suggest that at the neurological as well as the perceptual level, auditory processing of speech is affected by vision, so that 'auditory speech regions' are activated by seen speech. The processing of natural speech, whether it is heard, seen or heard and seen, activates the perisylvian language regions (left>right). It is highly probable that activation occurs in a specific order. First, superior temporal, then inferior parietal and finally inferior frontal regions (left>right) are activated. There is some differentiation of the visual input stream to the core perisylvian language system, suggesting that complementary seen speech information makes special use of the visual ventral processing stream, while for correlated visual speech, the dorsal processing stream, which is sensitive to visual movement, may be relatively more involved.     

Cortical dynamics of acoustic and phonological processing in speech perception

In speech perception, a functional hierarchy has been proposed by recent functional neuroimaging studies: core auditory areas on the dorsal plane of superior temporal gyrus (STG) are sensitive to basic acoustic characteristics, whereas downstream regions, specifically the left superior temporal sulcus (STS) and middle temporal gyrus (MTG) ventral to Heschl's gyrus (HG) are responsive to abstract phonological features. What is unclear so far is the relationship between the dorsal and ventral processes, especially with regard to whether low-level acoustic processing is modulated by high-level phonological processing. To address the issue, we assessed sensitivity of core auditory and downstream regions to acoustic and phonological variations by using within- and across-category lexical tonal continua with equal physical intervals. We found that relative to within-category variation, across-category variation elicited stronger activation in the left middle MTG (mMTG), apparently reflecting the abstract phonological representations. At the same time, activation in the core auditory region decreased, resulting from the top-down influences of phonological processing. These results support a hierarchical organization of the ventral acoustic-phonological processing stream, which originates in the right HG/STG and projects to the left mMTG. Furthermore, our study provides direct evidence that low-level acoustic analysis is modulated by high-level phonological representations, revealing the cortical dynamics of acoustic and phonological processing in speech perception. Our findings confirm the existence of reciprocal progression projections in the auditory pathways and the roles of both feed-forward and feedback mechanisms in speech perception.     

Posterior Parietal Cortex Drives Inferotemporal Activations During Three-Dimensional Object Vision

The primate visual system consists of a ventral stream, specialized for object recognition, and a dorsal visual stream, which is crucial for spatial vision and actions. However, little is known about the interactions and information flow between these two streams. We investigated these interactions within the network processing three-dimensional (3D) object information, comprising both the dorsal and ventral stream. Reversible inactivation of the macaque caudal intraparietal area (CIP) during functional magnetic resonance imaging (fMRI) reduced fMRI activations in posterior parietal cortex in the dorsal stream and, surprisingly, also in the inferotemporal cortex (ITC) in the ventral visual stream. Moreover, CIP inactivation caused a perceptual deficit in a depth-structure categorization task. CIP-microstimulation during fMRI further suggests that CIP projects via posterior parietal areas to the ITC in the ventral stream. To our knowledge, these results provide the first causal evidence for the flow of visual 3D information from the dorsal stream to the ventral stream, and identify CIP as a key area for depth-structure processing. Thus, combining reversible inactivation and electrical microstimulation during fMRI provides a detailed view of the functional interactions between the two visual processing streams.     

A new neural framework for visuospatial processing

The division of cortical visual processing into distinct dorsal and ventral streams is a key framework that has guided visual neuroscience. The characterization of the ventral stream as a 'What' pathway is relatively uncontroversial, but the nature of dorsal stream processing is less clear. Originally proposed as mediating spatial perception ('Where'), more recent accounts suggest it primarily serves non-conscious visually guided action ('How'). Here, we identify three pathways emerging from the dorsal stream that consist of projections to the prefrontal and premotor cortices, and a major projection to the medial temporal lobe that courses both directly and indirectly through the posterior cingulate and retrosplenial cortices. These three pathways support both conscious and non-conscious visuospatial processing, including spatial working memory, visually guided action and navigation, respectively.     

The Role of Parieto-Occipital Junction in the Interaction between Dorsal and Ventral Streams in Disparity-Defined Near and Far Space Processing

Neuropsychological and functional MRI data suggest that two functionally and anatomically dissociable streams of visual processing exist: a ventral perception-related stream and a dorsal action-related stream. However, relatively little is known about how the two streams interact in the intact brain during the production of adaptive behavior. Using functional MRI and a virtual three-dimensional paradigm, we aimed at examining whether the parieto-occipital junction (POJ) acts as an interface for the integration and processing of information between the dorsal and ventral streams in the near and far space processing. Virtual reality three-dimensional near and far space was defined by manipulating binocular disparity, with -68.76 arcmin crossed disparity for near space and +68.76 arcmin uncrossed disparity for near space. Our results showed that the POJ and bilateral superior occipital gyrus (SOG) showed relative increased activity when responded to targets presented in the near space than in the far space, which was independent of the retinotopic and perceived sizes of target. Furthermore, the POJ showed the enhanced functional connectivity with both the dorsal and ventral streams during the far space processing irrespective of target sizes, supporting that the POJ acts as an interface between the dorsal and ventral streams in disparity-defined near and far space processing. In contrast, the bilateral SOG showed the enhanced functional connectivity only with the ventral stream if retinotopic sizes of targets in the near and far spaces were matched, which suggested there was a functional dissociation between the POJ and bilateral SOG.     

Occipital Alpha Activity during Stimulus Processing Gates the Information Flow to Object-Selective Cortex

Given the limited processing capabilities of the sensory system, it is essential that attended information is gated to downstream areas, whereas unattended information is blocked. While it has been proposed that alpha band (8–13 Hz) activity serves to route information to downstream regions by inhibiting neuronal processing in task-irrelevant regions, this hypothesis remains untested. Here we investigate how neuronal oscillations detected by electroencephalography in visual areas during working memory encoding serve to gate information reflected in the simultaneously recorded blood-oxygenation-level-dependent (BOLD) signals recorded by functional magnetic resonance imaging in downstream ventral regions. We used a paradigm in which 16 participants were presented with faces and landscapes in the right and left hemifields; one hemifield was attended and the other unattended. We observed that decreased alpha power contralateral to the attended object predicted the BOLD signal representing the attended object in ventral object-selective regions. Furthermore, increased alpha power ipsilateral to the attended object predicted a decrease in the BOLD signal representing the unattended object. We also found that the BOLD signal in the dorsal attention network inversely correlated with visual alpha power. This is the first demonstration, to our knowledge, that oscillations in the alpha band are implicated in the gating of information from the visual cortex to the ventral stream, as reflected in the representationally specific BOLD signal. This link of sensory alpha to downstream activity provides a neurophysiological substrate for the mechanism of selective attention during stimulus processing, which not only boosts the attended information but also suppresses distraction. Although previous studies have shown a relation between the BOLD signal from the dorsal attention network and the alpha band at rest, we demonstrate such a relation during a visuospatial task, indicating that the dorsal attention network exercises top-down control of visual alpha activity.     

Form and motion coherence activate independent, but not dorsal/ventral segregated, networks in the human brain

There is much evidence in primates' visual processing for distinct mechanisms involved in object recognition and encoding object position and motion, which have been identified with 'ventral' and 'dorsal' streams, respectively, of the extra-striate visual areas [1] [2] [3]. This distinction may yield insights into normal human perception, its development and pathology. Motion coherence sensitivity has been taken as a test of global processing in the dorsal stream [4] [5]. We have proposed an analogous 'form coherence' measure of global processing in the ventral stream [6]. In a functional magnetic resonance imaging (fMRI) experiment, we found that the cortical regions activated by form coherence did not overlap with those activated by motion coherence in the same individuals. Areas differentially activated by form coherence included regions in the middle occipital gyrus, the ventral occipital surface, the intraparietal sulcus, and the temporal lobe. Motion coherence activated areas consistent with those previously identified as V5 and V3a, the ventral occipital surface, the intraparietal sulcus, and temporal structures. Neither form nor motion coherence activated area V1 differentially. Form and motion foci in occipital, parietal, and temporal areas were nearby but showed almost no overlap. These results support the idea that form and motion coherence test distinct functional brain systems, but that these do not necessarily correspond to a gross anatomical separation of dorsal and ventral processing streams.     

The Brain’s Dorsal Route for Speech Represents Word Meaning: Evidence from Gesture

The dual-route model of speech processing includes a dorsal stream that maps auditory to motor features at the sublexical level rather than at the lexico-semantic level. However, the literature on gesture is an invitation to revise this model because it suggests that the premotor cortex of the dorsal route is a major site of lexico-semantic interaction. Here we investigated lexico-semantic mapping using word-gesture pairs that were either congruent or incongruent. Using fMRI-adaptation in 28 subjects, we found that temporo-parietal and premotor activity during auditory processing of single action words was modulated by the prior audiovisual context in which the words had been repeated. The BOLD signal was suppressed following repetition of the auditory word alone, and further suppressed following repetition of the word accompanied by a congruent gesture (e.g. [“grasp” + grasping gesture]). Conversely, repetition suppression was not observed when the same action word was accompanied by an incongruent gesture (e.g. [“grasp” + sprinkle]). We propose a simple model to explain these results: auditory and visual information converge onto premotor cortex where it is represented in a comparable format to determine (in)congruence between speech and gesture. This ability of the dorsal route to detect audiovisual semantic (in)congruence suggests that its function is not restricted to the sublexical level.     

Action-related properties shape object representations in the ventral stream

The principles driving the organization of the ventral object-processing stream remain unknown. Here, we show that stimulus-specific repetition suppression (RS) in one region of the ventral stream is biased according to motor-relevant properties of objects. Quantitative analysis confirmed that this result was not confounded with similarity in visual shape. A similar pattern of biases in RS according to motor-relevant properties of objects was observed in dorsal stream regions in the left hemisphere. These findings suggest that neural specificity for "tools" in the ventral stream is driven by similarity metrics computed over motor-relevant information represented in dorsal structures. Support for this view is provided by converging results from functional connectivity analyses of the fMRI data and a separate neuropsychological study. More generally, these data suggest that a basic organizing principle giving rise to "category specificity" in the ventral stream may involve similarity metrics computed over information represented elsewhere in the brain.     

Top-down modulations from dorsal stream in lexical recognition: an effective connectivity FMRI study

Both the ventral and dorsal visual streams in the human brain are known to be involved in reading. However, the interaction of these two pathways and their responses to different cognitive demands remains unclear. In this study, activation of neural pathways during Chinese character reading was acquired by using a functional magnetic resonance imaging (fMRI) technique. Visual-spatial analysis (mediated by the dorsal pathway) was disassociated from lexical recognition (mediated by the ventral pathway) via a spatial-based lexical decision task and effective connectivity analysis. Connectivity results revealed that, during spatial processing, the left superior parietal lobule (SPL) positively modulated the left fusiform gyrus (FG), while during lexical processing, the left SPL received positive modulatory input from the left inferior frontal gyrus (IFG) and sent negative modulatory output to the left FG. These findings suggest that the dorsal stream is highly involved in lexical recognition and acts as a top-down modulator for lexical processing.     

形状和空间位置知觉两条通路的功能磁共振研究

利用功能磁共振成像（ｆＭＲＩ） 技术,研究在处理形状知觉、位置知觉和特定形状图形的空间位置知觉的情况下,人类视皮层背侧（Ｄｏｒｓａｌ ｓｔｒｅａｍ） 和腹侧（Ｖｅｎｔｒａｌ ｓｔｒｅａｍ） 两条通路是怎样反应的。结果发现：形状知觉仅引起腹侧通路的兴奋;空间位置的知觉引起背侧通路的兴奋;特定形状的空间位置知觉引起腹侧通路和背侧通路的共同兴奋。这一结果丰富了对人类视觉皮层的两条通路在功能上定位的认识。     

Is Attention Based on Spatial Contextual Memory Preferentially Guided by Low Spatial Frequency Signals?

A popular model of visual perception states that coarse information (carried by low spatial frequencies) along the dorsal stream is rapidly transmitted to prefrontal and medial temporal areas, activating contextual information from memory, which can in turn constrain detailed input carried by high spatial frequencies arriving at a slower rate along the ventral visual stream, thus facilitating the processing of ambiguous visual stimuli. We were interested in testing whether this model contributes to memory-guided orienting of attention. In particular, we asked whether global, low-spatial frequency (LSF) inputs play a dominant role in triggering contextual memories in order to facilitate the processing of the upcoming target stimulus. We explored this question over four experiments. The first experiment replicated the LSF advantage reported in perceptual discrimination tasks by showing that participants were faster and more accurate at matching a low spatial frequency version of a scene, compared to a high spatial frequency version, to its original counterpart in a forced-choice task. The subsequent three experiments tested the relative contributions of low versus high spatial frequencies during memory-guided covert spatial attention orienting tasks. Replicating the effects of memory-guided attention, pre-exposure to scenes associated with specific spatial memories for target locations (memory cues) led to higher perceptual discrimination and faster response times to identify targets embedded in the scenes. However, either high or low spatial frequency cues were equally effective; LSF signals did not selectively or preferentially contribute to the memory-driven attention benefits to performance. Our results challenge a generalized model that LSFs activate contextual memories, which in turn bias attention and facilitate perception.     

A stimulus-driven approach to object identity and location processing in the human brain

The primate visual system is considered to be segregated into ventral and dorsal streams specialized for processing object identity and location, respectively. We reexamined the dorsal/ventral model using a stimulus-driven approach to object identity and location processing. While looking at repeated presentations of a standard object at a standard location, subjects monitored for any infrequent "oddball" changes in object identity, location, or identity and location (conjunction). While the identity and location oddballs preferentially activated ventral and dorsal brain regions respectively, each oddball type activated both pathways. Furthermore, all oddball types recruited the lateral temporal cortex and the temporo-parietal junction. These findings suggest that a strict dorsal/ventral dual-stream model does not fully account for the perception of novel objects in space.     

Stereoscopic Vision in the Absence of the Lateral Occipital Cortex

Both dorsal and ventral cortical visual streams contain neurons sensitive to binocular disparities, but the two streams may underlie different aspects of stereoscopic vision. Here we investigate stereopsis in the neurological patient D.F., whose ventral stream, specifically lateral occipital cortex, has been damaged bilaterally, causing profound visual form agnosia. Despite her severe damage to cortical visual areas, we report that DF''s stereo vision is strikingly unimpaired. She is better than many control observers at using binocular disparity to judge whether an isolated object appears near or far, and to resolve ambiguous structure-from-motion. DF is, however, poor at using relative disparity between features at different locations across the visual field. This may stem from a difficulty in identifying the surface boundaries where relative disparity is available. We suggest that the ventral processing stream may play a critical role in enabling healthy observers to extract fine depth information from relative disparities within one surface or between surfaces located in different parts of the visual field.     

Is visual processing in the dorsal stream accessible to consciousness?

There are two highly interconnected clusters of visually responsive areas in the primate cortex. These two clusters have relatively few interconnections with each other, though those interconnections are undoubtedly important. One of the two main clusters (the dorsal stream) links the primary visual cortex (V1) to superior regions of the occipito-parietal cortex, while the other (the ventral stream) links V1 to inferior regions of the occipito-temporal cortex. According to our current understanding of the functional anatomy of these two systems, the dorsal stream's principal role is to provide real-time 'bottom-up' visual guidance of our movements online. In contrast, the ventral stream, in conjunction with top-down information from visual and semantic memory, provides perceptual representations that can serve recognition, visual thought, planning and memory offline. In recent years, this interpretation, initially based chiefly on studies of non-human primates and human neurological patients, has been well supported by functional MRI studies in humans. This perspective presents empirical evidence for the contention that the dorsal stream governs the visual control of movement without the intervention of visual awareness.     

Temporal and spatial effects of Sonic hedgehog signaling in chick eye morphogenesis

Proper dorsal--ventral pattern formation of the optic cup is essential for vertebrate eye morphogenesis and retinotectal topographic mapping. Previous studies have suggested that midline tissue-derived Sonic hedgehog (Shh) molecules play critical roles in establishing the bilateral eye fields and in determining the proximal--distal axis of the eye primordium. Here, we have examined the temporal requirements for Shh during the optic vesicle to optic cup transition and after early optic cup formation in chick embryos. Both misexpressing Shh by virus and blocking Shh activity by antibodies resulted in disruption of ventral ocular tissues. Decreasing endogenous Shh signals unexpectedly revealed a sharp morphological boundary subdividing dorsal and ventral portions of the optic cup. In addition, Shh signals differentially influenced expression patterns of genes involved in ocular tissue specification (Pax6, Pax2, and Otx2) and dorsal--ventral patterning (cVax) within the ventral but not dorsal optic cup. Ectopic Shh suppressed expression of Bone Morphogenetic Protein 4 (BMP4) in the dorsal retina, whereas reducing endogenous Sonic hedgehog activity resulted in a ventral expansion of BMP4 territory. These results demonstrate that temporal requirements for Shh signals persist after the formation of the optic cup and suggest that the early vertebrate optic primordium may be subdivided into dorsal and ventral compartments. We propose a model in which ventrally derived Shh signals and dorsally restricted BMP4 signals act antagonistically to regulate the growth and specification of the optic primordium.     

A Color Hierarchy for Automatic Target Selection

Visual processing of color starts at the cones in the retina and continues through ventral stream visual areas, called the parvocellular pathway. Motion processing also starts in the retina but continues through dorsal stream visual areas, called the magnocellular system. Color and motion processing are functionally and anatomically discrete. Previously, motion processing areas MT and MST have been shown to have no color selectivity to a moving stimulus; the neurons were colorblind whenever color was presented along with motion. This occurs when the stimuli are luminance-defined versus the background and is considered achromatic motion processing. Is motion processing independent of color processing? We find that motion processing is intrinsically modulated by color. Color modulated smooth pursuit eye movements produced upon saccading to an aperture containing a surface of coherently moving dots upon a black background. Furthermore, when two surfaces that differed in color were present, one surface was automatically selected based upon a color hierarchy. The strength of that selection depended upon the distance between the two colors in color space. A quantifiable color hierarchy for automatic target selection has wide-ranging implications from sports to advertising to human-computer interfaces.     

The Natural Statistics of Audiovisual Speech

Humans, like other animals, are exposed to a continuous stream of signals, which are dynamic, multimodal, extended, and time varying in nature. This complex input space must be transduced and sampled by our sensory systems and transmitted to the brain where it can guide the selection of appropriate actions. To simplify this process, it''s been suggested that the brain exploits statistical regularities in the stimulus space. Tests of this idea have largely been confined to unimodal signals and natural scenes. One important class of multisensory signals for which a quantitative input space characterization is unavailable is human speech. We do not understand what signals our brain has to actively piece together from an audiovisual speech stream to arrive at a percept versus what is already embedded in the signal structure of the stream itself. In essence, we do not have a clear understanding of the natural statistics of audiovisual speech. In the present study, we identified the following major statistical features of audiovisual speech. First, we observed robust correlations and close temporal correspondence between the area of the mouth opening and the acoustic envelope. Second, we found the strongest correlation between the area of the mouth opening and vocal tract resonances. Third, we observed that both area of the mouth opening and the voice envelope are temporally modulated in the 2–7 Hz frequency range. Finally, we show that the timing of mouth movements relative to the onset of the voice is consistently between 100 and 300 ms. We interpret these data in the context of recent neural theories of speech which suggest that speech communication is a reciprocally coupled, multisensory event, whereby the outputs of the signaler are matched to the neural processes of the receiver.     

Differential effects of viewpoint on object-driven activation in dorsal and ventral streams

Using fMRI, we showed that an area in the ventral temporo-occipital cortex (area vTO), which is part of the human homolog of the ventral stream of visual processing, exhibited priming for both identical and depth-rotated images of objects. This pattern of activation in area vTO corresponded to performance in a behavioral matching task. An area in the caudal part of the intraparietal sulcus (area cIPS) also showed priming, but only with identical images of objects. This dorsal-stream area treated rotated images as new objects. The difference in the pattern of priming-related activation in the two areas may reflect the respective roles of the ventral and dorsal streams in object recognition and object-directed action.     

A cortical network processes auditory error signals during human speech production to maintain fluency

Hearing one’s own voice is critical for fluent speech production as it allows for the detection and correction of vocalization errors in real time. This behavior known as the auditory feedback control of speech is impaired in various neurological disorders ranging from stuttering to aphasia; however, the underlying neural mechanisms are still poorly understood. Computational models of speech motor control suggest that, during speech production, the brain uses an efference copy of the motor command to generate an internal estimate of the speech output. When actual feedback differs from this internal estimate, an error signal is generated to correct the internal estimate and update necessary motor commands to produce intended speech. We were able to localize the auditory error signal using electrocorticographic recordings from neurosurgical participants during a delayed auditory feedback (DAF) paradigm. In this task, participants hear their voice with a time delay as they produced words and sentences (similar to an echo on a conference call), which is well known to disrupt fluency by causing slow and stutter-like speech in humans. We observed a significant response enhancement in auditory cortex that scaled with the duration of feedback delay, indicating an auditory speech error signal. Immediately following auditory cortex, dorsal precentral gyrus (dPreCG), a region that has not been implicated in auditory feedback processing before, exhibited a markedly similar response enhancement, suggesting a tight coupling between the 2 regions. Critically, response enhancement in dPreCG occurred only during articulation of long utterances due to a continuous mismatch between produced speech and reafferent feedback. These results suggest that dPreCG plays an essential role in processing auditory error signals during speech production to maintain fluency.

Hearing one’s own voice is critical for fluent speech production, allowing detection and correction of vocalization errors in real-time. This study shows that the dorsal precentral gyrus is a critical component of a cortical network that monitors auditory feedback to produce fluent speech; this region is engaged specifically when speech production is effortful during articulation of long utterances.