Specificity of Motor Contributions to Auditory Statistical Learning.

Statistical learning is the ability to extract patterned information from continuous sensory signals. Recent evidence suggests that auditory-motor mechanisms play an important role in auditory statistical learning from speech signals. The question remains whether auditory-motor mechanisms support such learning generally or in a domain-specific manner. In Experiment 1, we tested the specificity of motor processes contributing to learning patterns from speech sequences. Participants either whispered or clapped their hands while listening to structured speech. In Experiment 2, we focused on auditory specificity, testing whether whispering equally affects learning patterns from speech and non-speech sequences. Finally, in Experiment 3, we examined whether learning patterns from speech and non-speech sequences are correlated. Whispering had a stronger effect than clapping on learning patterns from speech sequences in Experiment 1. Moreover, whispering impaired statistical learning more strongly from speech than non-speech sequences in Experiment 2. Interestingly, while participants in the non-speech tasks spontaneously synchronized their motor movements with the auditory stream more than participants in the speech tasks, the effect of the motor movements on learning was stronger in the speech domain. Finally, no correlation between speech and non-speech learning was observed. Overall, our findings support the idea that learning statistical patterns from speech versus non-speech relies on segregated mechanisms, and that the speech motor system contributes to auditory statistical learning in a highly specific manner.

Cognitive Development as a Piece of the Language Learning Puzzle.

Why do children learn language more easily than adults do? This puzzle has fascinated cognitive and language scientists for decades. In the present letter, we approach the language learning puzzle from a cognitive perspective that is inspired by evidence from the perceptual and motor learning literature. Neuroscientific studies show that two memory systems in the brain are involved in human learning: an early implicit procedural memory system and a late-developing cognitive or declarative memory system. We argue that higher cognitive development constrains implicit statistical learning processes that are essential for learning patterns and regularities in languages, that is, the adult cognitive architecture has a cost. This is supported by experimental evidence showing that acquisition of implicit linguistic knowledge is enhanced under cognitive depletion in adults. More research is needed to test the cognitive cost hypothesis as it could partly solve the language learning puzzle.

Unlocking adults' implicit statistical learning by cognitive depletion.

Human learning is supported by multiple neural mechanisms that maturate at different rates and interact in mostly cooperative but also sometimes competitive ways. We tested the hypothesis that mature cognitive mechanisms constrain implicit statistical learning mechanisms that contribute to early language acquisition. Specifically, we tested the prediction that depleting cognitive control mechanisms in adults enhances their implicit, auditory word-segmentation abilities. Young adults were exposed to continuous streams of syllables that repeated into hidden novel words while watching a silent film. Afterward, learning was measured in a forced-choice test that contrasted hidden words with nonwords. The participants also had to indicate whether they explicitly recalled the word or not in order to dissociate explicit versus implicit knowledge. We additionally measured electroencephalography during exposure to measure neural entrainment to the repeating words. Engagement of the cognitive mechanisms was manipulated by using two methods. In experiment 1 (n = 36), inhibitory theta-burst stimulation (TBS) was applied to the left dorsolateral prefrontal cortex or to a control region. In experiment 2 (n = 60), participants performed a dual working-memory task that induced high or low levels of cognitive fatigue. In both experiments, cognitive depletion enhanced word recognition, especially when participants reported low confidence in remembering the words (i.e., when their knowledge was implicit). TBS additionally modulated neural entrainment to the words and syllables. These findings suggest that cognitive depletion improves the acquisition of linguistic knowledge in adults by unlocking implicit statistical learning mechanisms and support the hypothesis that adult language learning is antagonized by higher cognitive mechanisms.

Asymmetry of Auditory-Motor Speech Processing is Determined by Language Experience.

Speech processing relies on interactions between auditory and motor systems and is asymmetrically organized in the human brain. The left auditory system is specialized for processing of phonemes, whereas the right is specialized for processing of pitch changes in speech affecting prosody. In speakers of tonal languages, however, processing of pitch (i.e., tone) changes that alter word meaning is left-lateralized indicating that linguistic function and language experience shape speech processing asymmetries. Here, we investigated the asymmetry of motor contributions to auditory speech processing in male and female speakers of tonal and non-tonal languages. We temporarily disrupted the right or left speech motor cortex using transcranial magnetic stimulation (TMS) and measured the impact of these disruptions on auditory discrimination (mismatch negativity; MMN) responses to phoneme and tone changes in sequences of syllables using electroencephalography (EEG). We found that the effect of motor disruptions on processing of tone changes differed between language groups: disruption of the right speech motor cortex suppressed responses to tone changes in non-tonal language speakers, whereas disruption of the left speech motor cortex suppressed responses to tone changes in tonal language speakers. In non-tonal language speakers, the effects of disruption of left speech motor cortex on responses to tone changes were inconclusive. For phoneme changes, disruption of left but not right speech motor cortex suppressed responses in both language groups. We conclude that the contributions of the right and left speech motor cortex to auditory speech processing are determined by the functional roles of acoustic cues in the listener's native language.SIGNIFICANCE STATEMENT The principles underlying hemispheric asymmetries of auditory speech processing remain debated. The asymmetry of processing of speech sounds is affected by low-level acoustic cues, but also by their linguistic function. By combining transcranial magnetic stimulation (TMS) and electroencephalography (EEG), we investigated the asymmetry of motor contributions to auditory speech processing in tonal and non-tonal language speakers. We provide causal evidence that the functional role of the acoustic cues in the listener's native language affects the asymmetry of motor influences on auditory speech discrimination ability [indexed by mismatch negativity (MMN) responses]. Lateralized top-down motor influences can affect asymmetry of speech processing in the auditory system.

Decline of auditory-motor speech processing in older adults with hearing loss.

Older adults often experience difficulties in understanding speech, partly because of age-related hearing loss (HL). In young adults, activity of the left articulatory motor cortex is enhanced and it interacts with the auditory cortex via the left-hemispheric dorsal stream during speech processing. Little is known about the effect of aging and age-related HL on this auditory-motor interaction and speech processing in the articulatory motor cortex. It has been proposed that upregulation of the motor system during speech processing could compensate for HL and auditory processing deficits in older adults. Alternatively, age-related auditory deficits could reduce and distort the input from the auditory cortex to the articulatory motor cortex, suppressing recruitment of the motor system during listening to speech. The aim of the present study was to investigate the effects of aging and age-related HL on the excitability of the tongue motor cortex during listening to spoken sentences using transcranial magnetic stimulation and electromyography. Our results show that the excitability of the tongue motor cortex was facilitated during listening to speech in young and older adults with normal hearing. This facilitation was significantly reduced in older adults with HL. These findings suggest a decline of auditory-motor processing of speech in adults with age-related HL.

Facilitation of motor excitability during listening to spoken sentences is not modulated by noise or semantic coherence.

Comprehending speech can be particularly challenging in a noisy environment and in the absence of semantic context. It has been proposed that the articulatory motor system would be recruited especially in difficult listening conditions. However, it remains unknown how signal-to-noise ratio (SNR) and semantic context affect the recruitment of the articulatory motor system when listening to continuous speech. The aim of the present study was to address the hypothesis that involvement of the articulatory motor cortex increases when the intelligibility and clarity of the spoken sentences decreases, because of noise and the lack of semantic context. We applied Transcranial Magnetic Stimulation (TMS) to the lip and hand representations in the primary motor cortex and measured motor evoked potentials from the lip and hand muscles, respectively, to evaluate motor excitability when young adults listened to sentences. In Experiment 1, we found that the excitability of the lip motor cortex was facilitated during listening to both semantically anomalous and coherent sentences in noise relative to non-speech baselines, but neither SNR nor semantic context modulated the facilitation. In Experiment 2, we replicated these findings and found no difference in the excitability of the lip motor cortex between sentences in noise and clear sentences without noise. Thus, our results show that the articulatory motor cortex is involved in speech processing even in optimal and ecologically valid listening conditions and that its involvement is not modulated by the intelligibility and clarity of speech.

Transcranial direct current stimulation over left inferior frontal cortex improves speech fluency in adults who stutter.

See Crinion (doi:10.1093/brain/awy075) for a scientific commentary on this article.Stuttering is a neurodevelopmental condition affecting 5% of children, and persisting in 1% of adults. Promoting lasting fluency improvement in adults who stutter is a particular challenge. Novel interventions to improve outcomes are of value, therefore. Previous work in patients with acquired motor and language disorders reported enhanced benefits of behavioural therapies when paired with transcranial direct current stimulation. Here, we report the results of the first trial investigating whether transcranial direct current stimulation can improve speech fluency in adults who stutter. We predicted that applying anodal stimulation to the left inferior frontal cortex during speech production with temporary fluency inducers would result in longer-lasting fluency improvements. Thirty male adults who stutter completed a randomized, double-blind, controlled trial of anodal transcranial direct current stimulation over left inferior frontal cortex. Fifteen participants received 20 min of 1-mA stimulation on five consecutive days while speech fluency was temporarily induced using choral and metronome-timed speech. The other 15 participants received the same speech fluency intervention with sham stimulation. Speech fluency during reading and conversation was assessed at baseline, before and after the stimulation on each day of the 5-day intervention, and at 1 and 6 weeks after the end of the intervention. Anodal stimulation combined with speech fluency training significantly reduced the percentage of disfluent speech measured 1 week after the intervention compared with fluency intervention alone. At 6 weeks after the intervention, this improvement was maintained during reading but not during conversation. Outcome scores at both post-intervention time points on a clinical assessment tool (the Stuttering Severity Instrument, version 4) also showed significant improvement in the group receiving transcranial direct current stimulation compared with the sham group, in whom fluency was unchanged from baseline. We conclude that transcranial direct current stimulation combined with behavioural fluency intervention can improve fluency in adults who stutter. Transcranial direct current stimulation thereby offers a potentially useful adjunct to future speech therapy interventions for this population, for whom fluency therapy outcomes are currently limited.

An interactive model of auditory-motor speech perception.

Mounting evidence indicates a role in perceptual decoding of speech for the dorsal auditory stream connecting between temporal auditory and frontal-parietal articulatory areas. The activation time course in auditory, somatosensory and motor regions during speech processing is seldom taken into account in models of speech perception. We critically review the literature with a focus on temporal information, and contrast between three alternative models of auditory-motor speech processing: parallel, hierarchical, and interactive. We argue that electrophysiological and transcranial magnetic stimulation studies support the interactive model. The findings reveal that auditory and somatomotor areas are engaged almost simultaneously, before 100 ms. There is also evidence of early interactions between auditory and motor areas. We propose a new interactive model of auditory-motor speech perception in which auditory and articulatory somatomotor areas are connected from early stages of speech processing. We also discuss how attention and other factors can affect the timing and strength of auditory-motor interactions and propose directions for future research.

Supernatural Belief Is Not Modulated by Intuitive Thinking Style or Cognitive Inhibition.

According to the Intuitive Belief Hypothesis, supernatural belief relies heavily on intuitive thinking-and decreases when analytic thinking is engaged. After pointing out various limitations in prior attempts to support this Intuitive Belief Hypothesis, we test it across three new studies using a variety of paradigms, ranging from a pilgrimage field study to a neurostimulation experiment. In all three studies, we found no relationship between intuitive or analytical thinking and supernatural belief. We conclude that it is premature to explain belief in gods as 'intuitive', and that other factors, such as socio-cultural upbringing, are likely to play a greater role in the emergence and maintenance of supernatural belief than cognitive style.

Language learning in the adult brain: disrupting the dorsolateral prefrontal cortex facilitates word-form learning.

Adults do not learn languages as easily as children do. It has been hypothesized that the late-developing prefrontal cortex that supports executive functions competes with procedural learning mechanisms that are important for language learning. To address this hypothesis, we tested whether a temporary neural disruption of the left Dorsolateral Prefrontal Cortex (DLPFC) can improve implicit, procedural learning of word-forms in adults. Young adults were presented with repeating audio-visual sequences of syllables for immediate serial recall in a Hebb repetition learning task that simulates word-form learning. Inhibitory theta-burst Transcranial Magnetic Stimulation was applied to the left DLPFC or to the control site before the Hebb task. The DLPFC-disrupted group showed enhanced learning of the novel phonological sequences relative to the control group. Moreover, learning was negatively correlated with executive functions that rely on the DLPFC in the control group, but not in the DLPFC-disrupted group. The results support the hypothesis that a mature prefrontal cortex competes with implicit learning of word-forms. The findings provide new insight into the competition between brain mechanisms that contribute to language learning in the adult brain.

Investigating the feasibility of using transcranial direct current stimulation to enhance fluency in people who stutter.

Developmental stuttering is a disorder of speech fluency affecting 1% of the adult population. Long-term reductions in stuttering are difficult for adults to achieve with behavioural therapies. We investigated whether a single session of transcranial direct current stimulation (TDCS) could improve fluency in people who stutter (PWS). In separate sessions, either anodal TDCS (1mA for 20min) or sham stimulation was applied over the left inferior frontal cortex while PWS read sentences aloud. Fluency was induced during the stimulation period by using choral speech, that is, participants read in unison with another speaker. Stuttering frequency during sentence reading, paragraph reading and conversation was measured at baseline and at two outcome time points: immediately after the stimulation period and 1h later. Stuttering was reduced significantly at both outcome time points for the sentence-reading task, presumably due to practice, but not during the paragraph reading or conversation tasks. None of the outcome measures were significantly modulated by anodal TDCS. Although the results of this single-session study showed no significant TDCS-induced improvements in fluency, there were some indications that further research is warranted. We discuss factors that we believe may have obscured the expected positive effects of TDCS on fluency, such as heterogeneity in stuttering severity for the sample and variations across sessions. Consideration of such factors may inform future studies aimed at determining the potential of TDCS in the treatment of developmental stuttering.

Neural basis of understanding communicative actions: Changes associated with knowing the actor's intention and the meanings of the actions.

People can communicate by using hand actions, e.g., signs. Understanding communicative actions requires that the observer knows that the actor has an intention to communicate and the meanings of the actions. Here, we investigated how this prior knowledge affects processing of observed actions. We used functional MRI to determine changes in action processing when non-signers were told that the observed actions are communicative (i.e., signs) and learned the meanings of half of the actions. Processing of hand actions activated the left and right inferior frontal gyrus (IFG, BA 44 and 45) when the communicative intention of the actor was known, even when the meanings of the actions remained unknown. These regions were not active when the observers did not know about the communicative nature of the hand actions. These findings suggest that the left and right IFG play a role in understanding the intention of the actor, but do not process visuospatial features of the communicative actions. Knowing the meanings of the hand actions further enhanced activity in the anterior part of the IFG (BA 45), the inferior parietal lobule and posterior inferior and middle temporal gyri in the left hemisphere. These left-hemisphere language regions could provide a link between meanings and observed actions. In sum, the findings provide evidence for the segregation of the networks involved in the neural processing of visuospatial features of communicative hand actions and those involved in understanding the actor's intention and the meanings of the actions.

The effects of delayed auditory and visual feedback on speech production.

Monitoring the sensory consequences of articulatory movements supports speaking. For example, delaying auditory feedback of a speaker's voice disrupts speech production. Also, there is evidence that this disruption may be decreased by immediate visual feedback, i.e., seeing one's own articulatory movements. It is, however, unknown whether delayed visual feedback affects speech production in fluent speakers. Here, the effects of delayed auditory and visual feedback on speech fluency (i.e., speech rate and errors), vocal control (i.e., intensity and pitch), and speech rhythm were investigated. Participants received delayed (by 200 ms) or immediate auditory feedback, while repeating sentences. Moreover, they received either no visual feedback, immediate visual feedback, or delayed visual feedback (by 200, 400, and 600 ms). Delayed auditory feedback affected fluency, vocal control, and rhythm. Immediate visual feedback had no effect on any of the speech measures when it was combined with delayed auditory feedback. Delayed visual feedback did, however, affect speech fluency when it was combined with delayed auditory feedback. In sum, the findings show that delayed auditory feedback disrupts fluency, vocal control, and rhythm and that delayed visual feedback can strengthen the disruptive effect of delayed auditory feedback on fluency.

Dissociating Contributions of the Motor Cortex to Speech Perception and Response Bias by Using Transcranial Magnetic Stimulation.

Recent studies using repetitive transcranial magnetic stimulation (TMS) have demonstrated that disruptions of the articulatory motor cortex impair performance in demanding speech perception tasks. These findings have been interpreted as support for the idea that the motor cortex is critically involved in speech perception. However, the validity of this interpretation has been called into question, because it is unknown whether the TMS-induced disruptions in the motor cortex affect speech perception or rather response bias. In the present TMS study, we addressed this question by using signal detection theory to calculate sensitivity (i.e., d') and response bias (i.e., criterion c). We used repetitive TMS to temporarily disrupt the lip or hand representation in the left motor cortex. Participants discriminated pairs of sounds from a "ba"-"da" continuum before TMS, immediately after TMS (i.e., during the period of motor disruption), and after a 30-min break. We found that the sensitivity for between-category pairs was reduced during the disruption of the lip representation. In contrast, disruption of the hand representation temporarily reduced response bias. This double dissociation indicates that the hand motor cortex contributes to response bias during demanding discrimination tasks, whereas the articulatory motor cortex contributes to perception of speech sounds.

Effect of attentional load on audiovisual speech perception: evidence from ERPs.

Seeing articulatory movements influences perception of auditory speech. This is often reflected in a shortened latency of auditory event-related potentials (ERPs) generated in the auditory cortex. The present study addressed whether this early neural correlate of audiovisual interaction is modulated by attention. We recorded ERPs in 15 subjects while they were presented with auditory, visual, and audiovisual spoken syllables. Audiovisual stimuli consisted of incongruent auditory and visual components known to elicit a McGurk effect, i.e., a visually driven alteration in the auditory speech percept. In a Dual task condition, participants were asked to identify spoken syllables whilst monitoring a rapid visual stream of pictures for targets, i.e., they had to divide their attention. In a Single task condition, participants identified the syllables without any other tasks, i.e., they were asked to ignore the pictures and focus their attention fully on the spoken syllables. The McGurk effect was weaker in the Dual task than in the Single task condition, indicating an effect of attentional load on audiovisual speech perception. Early auditory ERP components, N1 and P2, peaked earlier to audiovisual stimuli than to auditory stimuli when attention was fully focused on syllables, indicating neurophysiological audiovisual interaction. This latency decrement was reduced when attention was loaded, suggesting that attention influences early neural processing of audiovisual speech. We conclude that reduced attention weakens the interaction between vision and audition in speech.

Discrimination of speech and non-speech sounds following theta-burst stimulation of the motor cortex.

Perceiving speech engages parts of the motor system involved in speech production. The role of the motor cortex in speech perception has been demonstrated using low-frequency repetitive transcranial magnetic stimulation (rTMS) to suppress motor excitability in the lip representation and disrupt discrimination of lip-articulated speech sounds (Möttönen and Watkins, 2009). Another form of rTMS, continuous theta-burst stimulation (cTBS), can produce longer-lasting disruptive effects following a brief train of stimulation. We investigated the effects of cTBS on motor excitability and discrimination of speech and non-speech sounds. cTBS was applied for 40 s over either the hand or the lip representation of motor cortex. Motor-evoked potentials recorded from the lip and hand muscles in response to single pulses of TMS revealed no measurable change in motor excitability due to cTBS. This failure to replicate previous findings may reflect the unreliability of measurements of motor excitability related to inter-individual variability. We also measured the effects of cTBS on a listener's ability to discriminate: (1) lip-articulated speech sounds from sounds not articulated by the lips ("ba" vs. "da"); (2) two speech sounds not articulated by the lips ("ga" vs. "da"); and (3) non-speech sounds produced by the hands ("claps" vs. "clicks"). Discrimination of lip-articulated speech sounds was impaired between 20 and 35 min after cTBS over the lip motor representation. Specifically, discrimination of across-category ba-da sounds presented with an 800-ms inter-stimulus interval was reduced to chance level performance. This effect was absent for speech sounds that do not require the lips for articulation and non-speech sounds. Stimulation over the hand motor representation did not affect discrimination of speech or non-speech sounds. These findings show that stimulation of the lip motor representation disrupts discrimination of speech sounds in an articulatory feature-specific way.

Stimulating the lip motor cortex with transcranial magnetic stimulation.

Transcranial magnetic stimulation (TMS) has proven to be a useful tool in investigating the role of the articulatory motor cortex in speech perception. Researchers have used single-pulse and repetitive TMS to stimulate the lip representation in the motor cortex. The excitability of the lip motor representation can be investigated by applying single TMS pulses over this cortical area and recording TMS-induced motor evoked potentials (MEPs) via electrodes attached to the lip muscles (electromyography; EMG). Larger MEPs reflect increased cortical excitability. Studies have shown that excitability increases during listening to speech as well as during viewing speech-related movements. TMS can be used also to disrupt the lip motor representation. A 15-min train of low-frequency sub-threshold repetitive stimulation has been shown to suppress motor excitability for a further 15-20 min. This TMS-induced disruption of the motor lip representation impairs subsequent performance in demanding speech perception tasks and modulates auditory-cortex responses to speech sounds. These findings are consistent with the suggestion that the motor cortex contributes to speech perception. This article describes how to localize the lip representation in the motor cortex and how to define the appropriate stimulation intensity for carrying out both single-pulse and repetitive TMS experiments.

Attention fine-tunes auditory-motor processing of speech sounds.

The earliest stages of cortical processing of speech sounds take place in the auditory cortex. Transcranial magnetic stimulation (TMS) studies have provided evidence that the human articulatory motor cortex contributes also to speech processing. For example, stimulation of the motor lip representation influences specifically discrimination of lip-articulated speech sounds. However, the timing of the neural mechanisms underlying these articulator-specific motor contributions to speech processing is unknown. Furthermore, it is unclear whether they depend on attention. Here, we used magnetoencephalography and TMS to investigate the effect of attention on specificity and timing of interactions between the auditory and motor cortex during processing of speech sounds. We found that TMS-induced disruption of the motor lip representation modulated specifically the early auditory-cortex responses to lip-articulated speech sounds when they were attended. These articulator-specific modulations were left-lateralized and remarkably early, occurring 60-100 ms after sound onset. When speech sounds were ignored, the effect of this motor disruption on auditory-cortex responses was nonspecific and bilateral, and it started later, 170 ms after sound onset. The findings indicate that articulatory motor cortex can contribute to auditory processing of speech sounds even in the absence of behavioral tasks and when the sounds are not in the focus of attention. Importantly, the findings also show that attention can selectively facilitate the interaction of the auditory cortex with specific articulator representations during speech processing.