Anne-Lise Giraud

Endogenous cortical rhythms determine cerebral specialization for speech perception and production.

Across multiple timescales, acoustic regularities of speech match rhythmic properties of both the auditory and motor systems. Syllabic rate corresponds to natural jaw-associated oscillatory rhythms, and phonemic length could reflect endogenous oscillatory auditory cortical properties. Hemispheric lateralization for speech could result from an asymmetry of cortical tuning, with left and right auditory areas differentially sensitive to spectro-temporal features of speech. Using simultaneous electroencephalographic (EEG) and functional magnetic resonance imaging (fMRI) recordings from humans, we show that spontaneous EEG power variations within the gamma range (phonemic rate) correlate best with left auditory cortical synaptic activity, while fluctuations within the theta range correlate best with that in the right. Power fluctuations in both ranges correlate with activity in the mouth premotor region, indicating coupling between temporal properties of speech perception and production. These data show that endogenous cortical rhythms provide temporal and spatial constraints on the neuronal mechanisms underlying speech perception and production.

Intrinsic Connectivity Networks, Alpha Oscillations, and Tonic Alertness: A Simultaneous Electroencephalography/Functional Magnetic Resonance Imaging Study

Trial-by-trial variability in perceptual performance on identical stimuli has been related to spontaneous fluctuations in ongoing activity of intrinsic functional connectivity networks (ICNs). In a paradigm requiring sustained vigilance for instance, we previously observed that higher prestimulus activity in a cingulo-insular-thalamic network facilitated subsequent perception. Here, we test our proposed interpretation that this network underpins maintenance of tonic alertness. We used simultaneous acquisition of functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) in the absence of any paradigm to test an ensuing hypothesis, namely that spontaneous fluctuations in this ICN′s activity (as measured by fMRI) should show a positive correlation with the electrical signatures of tonic alertness (as recorded by concurrent EEG). We found in human subjects (19 male, 7 female) that activity in a network comprising dorsal anterior cingulate cortex, anterior insula, anterior prefrontal cortex and thalamus is positively correlated with global field power (GFP) of upper alpha band (10–12 Hz) oscillations, the most consistent electrical index of tonic alertness. Conversely, and in line with earlier findings, alpha band power was negatively correlated with activity in another ICN, the so-called dorsal attention network which is most prominently involved in selective spatial attention. We propose that the cingulo-insular-thalamic network serves maintaining tonic alertness through generalized expression of cortical alpha oscillations. Attention is mediated by activity in other systems, e.g., the dorsal attention network for space, selectively disrupts alertness-related suppression and hence manifests as local attenuation of alpha activity.

Implicit multisensory associations influence voice recognition.

Natural objects provide partially redundant information to the brain through different sensory modalities. For example, voices and faces both give information about the speech content, age, and gender of a person. Thanks to this redundancy, multimodal recognition is fast, robust, and automatic. In unimodal perception, however, only part of the information about an object is available. Here, we addressed whether, even under conditions of unimodal sensory input, crossmodal neural circuits that have been shaped by previous associative learning become activated and underpin a performance benefit. We measured brain activity with functional magnetic resonance imaging before, while, and after participants learned to associate either sensory redundant stimuli, i.e. voices and faces, or arbitrary multimodal combinations, i.e. voices and written names, ring tones, and cell phones or brand names of these cell phones. After learning, participants were better at recognizing unimodal auditory voices that had been paired with faces than those paired with written names, and association of voices with faces resulted in an increased functional coupling between voice and face areas. No such effects were observed for ring tones that had been paired with cell phones or names. These findings demonstrate that brief exposure to ecologically valid and sensory redundant stimulus pairs, such as voices and faces, induces specific multisensory associations. Consistent with predictive coding theories, associative representations become thereafter available for unimodal perception and facilitate object recognition. These data suggest that for natural objects effective predictive signals can be generated across sensory systems and proceed by optimization of functional connectivity between specialized cortical sensory modules.

Transitions in neural oscillations reflect prediction errors generated in audiovisual speech

According to the predictive coding theory, top-down predictions are conveyed by backward connections and prediction errors are propagated forward across the cortical hierarchy. Using MEG in humans, we show that violating multisensory predictions causes a fundamental and qualitative change in both the frequency and spatial distribution of cortical activity. When visual speech input correctly predicted auditory speech signals, a slow delta regime (3–4 Hz) developed in higher-order speech areas. In contrast, when auditory signals invalidated predictions inferred from vision, a low-beta (14–15 Hz) / high-gamma (60–80 Hz) coupling regime appeared locally in a multisensory area (area STS). This frequency shift in oscillatory responses scaled with the degree of audio-visual congruence and was accompanied by increased gamma activity in lower sensory regions. These findings are consistent with the notion that bottom-up prediction errors are communicated in predominantly high (gamma) frequency ranges, whereas top-down predictions are mediated by slower (beta) frequencies.

Dual Neural Routing of Visual Facilitation in Speech Processing

Viewing our interlocutor facilitates speech perception, unlike for instance when we telephone. Several neural routes and mechanisms could account for this phenomenon. Using magnetoencephalography, we show that when seeing the interlocutor, latencies of auditory responses (M100) are the shorter the more predictable speech is from visual input, whether the auditory signal was congruent or not. Incongruence of auditory and visual input affected auditory responses ∼20 ms after latency shortening was detected, indicating that initial content-dependent auditory facilitation by vision is followed by a feedback signal that reflects the error between expected and received auditory input (prediction error). We then used functional magnetic resonance imaging and confirmed that distinct routes of visual information to auditory processing underlie these two functional mechanisms. Functional connectivity between visual motion and auditory areas depended on the degree of visual predictability, whereas connectivity between the superior temporal sulcus and both auditory and visual motion areas was driven by audiovisual (AV) incongruence. These results establish two distinct mechanisms by which the brain uses potentially predictive visual information to improve auditory perception. A fast direct corticocortical pathway conveys visual motion parameters to auditory cortex, and a slower and indirect feedback pathway signals the error between visual prediction and auditory input.

How the brain repairs stuttering

Stuttering is a neurodevelopmental disorder associated with left inferior frontal structural anomalies. While children often recover, stuttering may also spontaneously disappear much later after years of dysfluency. These rare cases of unassisted recovery in adulthood provide a model of optimal brain repair outside the classical windows of developmental plasticity. Here we explore what distinguishes this type of recovery from less optimal repair modes, i.e. therapy-induced assisted recovery and attempted compensation in subjects who are still affected. We show that persistent stuttering is associated with mobilization of brain regions contralateral to the structural anomalies for compensation attempt. In contrast, the only neural landmark of optimal repair is activation of the left BA 47/12 in the orbitofrontal cortex, adjacent to a region where a white matter anomaly is observed in persistent stutterers, but normalized in recovered subjects. These findings show that late repair of neurodevelopmental stuttering follows the principles of contralateral and perianomalous reorganization.

Severity of dysfluency correlates with basal ganglia activity in persistent developmental stuttering

Previous studies suggest that anatomical anomalies [Foundas, A. L., Bollich, A. M., Corey, D. M., Hurley, M., & Heilman, K. M. (2001). Anomalous anatomy of speech-language areas in adults with persistent developmental stuttering. Neurology, 57, 207-215; Foundas, A. L., Corey, D. M., Angeles, V., Bollich, A. M., Crabtree-Hartman, E., & Heilman, K. M. (2003). Atypical cerebral laterality in adults with persistent developmental stuttering. Neurology, 61, 1378-1385; Foundas, A. L., Bollich, A. M., Feldman, J., Corey, D. M., Hurley, M., & Lemen, L. C. et al., (2004). Aberrant auditory processing and atypical planum temporale in developmental stuttering. Neurology, 63, 1640-1646; Jancke, L., Hanggi, J., & Steinmetz, H. (2004). Morphological brain differences between adult stutterers and non-stutterers. BMC Neurology, 4, 23], in particular a reduction of the white matter anisotropy underlying the left sensorimotor cortex [Sommer, M., Koch, M. A., Paulus, W., Weiller, C., & Buchel, C. (2002). Disconnection of speech-relevant brain areas in persistent developmental stuttering. Lancet, 360, 380-383] could be at the origin of persistent developmental stuttering (PDS). Because neural connections between the motor cortex and basal ganglia are implicated in speech motor functions, PDS could also be associated with a dysfunction in basal ganglia activity [Alm, P. (2004). Stuttering and the basal ganglia circuits: a critical review of possible relations. Journal of Communication Disorders, 37, 325-369]. This fMRI study reports a correlation between severity of stuttering and activity in the basal ganglia and shows that this activity is modified by fluency shaping therapy through long-term therapy effects that reflect speech production improvement. A model of dysfunction in stuttering and possible repair modes is proposed that accommodates the data presented here and observations previously made by us and by others.

The contribution of frequency-specific activity to hierarchical information processing in the human auditory cortex

The fact that feed-forward and top-down propagation of sensory information use distinct frequency bands is an appealing assumption for which evidence remains scarce. Here we obtain human depth recordings from two auditory cortical regions in both hemispheres, while subjects listen to sentences, and show that information travels in each direction using separate frequency channels. Bottom-up and top-down propagation dominates in γ- and δ–β (<40 Hz) bands, respectively. The predominance of low frequencies for top-down information transfer is confirmed by cross-regional frequency coupling, which indicates that the power of γ-activity in A1 is modulated by the phase of δ–β activity sampled from association auditory cortex (AAC). This cross-regional coupling effect is absent in the opposite direction. Finally, we show that information transfer does not proceed continuously but by time windows where bottom-up or top-down processing alternatively dominates. These findings suggest that the brain uses both frequency- and time-division multiplexing to optimize directional information transfer.

Simulation of talking faces in the human brain improves auditory speech recognition.

Human face-to-face communication is essentially audiovisual. Typically, people talk to us face-to-face, providing concurrent auditory and visual input. Understanding someone is easier when there is visual input, because visual cues like mouth and tongue movements provide complementary information about speech content. Here, we hypothesized that, even in the absence of visual input, the brain optimizes both auditory-only speech and speaker recognition by harvesting speaker-specific predictions and constraints from distinct visual face-processing areas. To test this hypothesis, we performed behavioral and neuroimaging experiments in two groups: subjects with a face recognition deficit (prosopagnosia) and matched controls. The results show that observing a specific person talking for 2 min improves subsequent auditory-only speech and speaker recognition for this person. In both prosopagnosics and controls, behavioral improvement in auditory-only speech recognition was based on an area typically involved in face-movement processing. Improvement in speaker recognition was only present in controls and was based on an area involved in face-identity processing. These findings challenge current unisensory models of speech processing, because they show that, in auditory-only speech, the brain exploits previously encoded audiovisual correlations to optimize communication. We suggest that this optimization is based on speaker-specific audiovisual internal models, which are used to simulate a talking face.

Alpha-Band Phase Synchrony Is Related to Activity in the Fronto-Parietal Adaptive Control Network

Neural oscillations in the alpha band (8–12 Hz) are increasingly viewed as an active inhibitory mechanism that gates and controls sensory information processing as a function of cognitive relevance. Extending this view, phase synchronization of alpha oscillations across distant cortical regions could regulate integration of information. Here, we investigated whether such long-range cross-region coupling in the alpha band is intrinsically and selectively linked to activity in a distinct functionally specialized brain network. If so, this would provide new insight into the functional role of alpha band phase synchrony. We adapted the phase-locking value to assess fluctuations in synchrony that occur over time in ongoing activity. Concurrent EEG and functional magnetic resonance imaging (fMRI) were recorded during resting wakefulness in 26 human subjects. Fluctuations in global synchrony in the upper alpha band correlated positively with activity in several prefrontal and parietal regions (as measured by fMRI). fMRI intrinsic connectivity analysis confirmed that these regions correspond to the well known fronto-parietal (FP) network. Spectral correlations with this networks activity confirmed that no other frequency band showed equivalent results. This selective association supports an intrinsic relation between large-scale alpha phase synchrony and cognitive functions associated with the FP network. This network has been suggested to implement phasic aspects of top-down modulation such as initiation and change in moment-to-moment control. Mechanistically, long-range upper alpha band synchrony is well suited to support these functions. Complementing our previous findings that related alpha oscillation power to neural structures serving tonic control, the current findings link alpha phase synchrony to neural structures underpinning phasic control of alertness and task requirements.