The Causal Role of Left and Right Superior Temporal Gyri in Speech Perception in Noise: A Transcranial Magnetic Stimulation Study.

Successful perception of speech in everyday listening conditions requires effective listening strategies to overcome common acoustic distortions, such as background noise. Convergent evidence from neuroimaging and clinical studies identify activation within the temporal lobes as key to successful speech perception. However, current neurobiological models disagree on whether the left temporal lobe is sufficient for successful speech perception or whether bilateral processing is required. We addressed this issue using TMS to selectively disrupt processing in either the left or right superior temporal gyrus (STG) of healthy participants to test whether the left temporal lobe is sufficient or whether both left and right STG are essential. Participants repeated keywords from sentences presented in background noise in a speech reception threshold task while receiving online repetitive TMS separately to the left STG, right STG, or vertex or while receiving no TMS. Results show an equal drop in performance following application of TMS to either left or right STG during the task. A separate group of participants performed a visual discrimination threshold task to control for the confounding side effects of TMS. Results show no effect of TMS on the control task, supporting the notion that the results of Experiment 1 can be attributed to modulation of cortical functioning in STG rather than to side effects associated with online TMS. These results indicate that successful speech perception in everyday listening conditions requires both left and right STG and thus have ramifications for our understanding of the neural organization of spoken language processing.

Cognitive mechanisms underpinning successful perception of different speech distortions.

Few studies thus far have investigated whether perception of distorted speech is consistent across different types of distortion. This study investigated whether participants show a consistent perceptual profile across three speech distortions: time-compressed, noise-vocoded, and speech in noise. Additionally, this study investigated whether/how individual differences in performance on a battery of audiological and cognitive tasks links to perception. Eighty-eight participants completed a speeded sentence-verification task with increases in accuracy and reductions in response times used to indicate performance. Audiological and cognitive task measures include pure tone audiometry, speech recognition threshold, working memory, vocabulary knowledge, attention switching, and pattern analysis. Despite previous studies suggesting that temporal and spectral/environmental perception require different lexical or phonological mechanisms, this study shows significant positive correlations in accuracy and response time performance across all distortions. Results of a principal component analysis and multiple linear regressions suggest that a component based on vocabulary knowledge and working memory predicted performance in the speech in quiet, time-compressed and speech in noise conditions. These results suggest that listeners employ a similar cognitive strategy to perceive different temporal and spectral/environmental speech distortions and that this mechanism is supported by vocabulary knowledge and working memory.

Stimulating Multiple-Demand Cortex Enhances Vocabulary Learning.

It is well established that networks within multiple-demand cortex (MDC) become active when diverse skills and behaviors are being learnt. However, their causal role in learning remains to be established. In the present study, we first performed functional magnetic resonance imaging on healthy female and male human participants to confirm that MDC was most active in the initial stages of learning a novel vocabulary, consisting of pronounceable nonwords (pseudowords), each associated with a picture of a real object. We then examined, in healthy female and male human participants, whether repetitive transcranial magnetic stimulation of a frontal midline node of the cingulo-opercular MDC affected learning rates specifically during the initial stages of learning. We report that stimulation of this node, but not a control brain region, substantially improved both accuracy and response times during the earliest stage of learning pseudoword-object associations. This stimulation had no effect on the processing of established vocabulary, tested by the accuracy and response times when participants decided whether a real word was accurately paired with a picture of an object. These results provide evidence that noninvasive stimulation to MDC nodes can enhance learning rates, thereby demonstrating their causal role in the learning process. We propose that this causal role makes MDC candidate target for experimental therapeutics; for example, in stroke patients with aphasia attempting to reacquire a vocabulary.SIGNIFICANCE STATEMENT Learning a task involves the brain system within which that specific task becomes established. Therefore, successfully learning a new vocabulary establishes the novel words in the language system. However, there is evidence that in the early stages of learning, networks within multiple-demand cortex (MDC), which control higher cognitive functions, such as working memory, attention, and monitoring of performance, become active. This activity declines once the task is learnt. The present study demonstrated that a node within MDC, located in midline frontal cortex, becomes active during the early stage of learning a novel vocabulary. Importantly, noninvasive brain stimulation of this node improved performance during this stage of learning. This observation demonstrated that MDC activity is important for learning.

Using transcranial magnetic stimulation of the undamaged brain to identify lesion sites that predict language outcome after stroke.

Transcranial magnetic stimulation focused on either the left anterior supramarginal gyrus or opercular part of the left inferior frontal gyrus has been reported to transiently impair the ability to perform phonological more than semantic tasks. Here we tested whether phonological processing abilities were also impaired following lesions to these regions in right-handed, English speaking adults, who were investigated at least 1 year after a left-hemisphere stroke. When our regions of interest were limited to 0.5 cm3 of grey matter centred around sites that had been identified with transcranial magnetic stimulation-based functional localization, phonological impairments were observed in 74% (40/54) of patients with damage to the regions and 21% (21/100) of patients sparing these regions. This classification accuracy was better than that observed when using regions of interest centred on activation sites in previous functional magnetic resonance imaging studies of phonological processing, or transcranial magnetic stimulation sites that did not use functional localization. New regions of interest were generated by redefining the borders of each of the transcranial magnetic stimulation sites to include areas that were consistently damaged in the patients with phonological impairments. This increased the incidence of phonological impairments in the presence of damage to 85% (46/54) and also reduced the incidence of phonological impairments in the absence of damage to 15% (15/100). The difference in phonological processing abilities between those with and without damage to these 'transcranial magnetic stimulation-guided' regions remained highly significant even after controlling for the effect of lesion size. The classification accuracy of the transcranial magnetic stimulation-guided regions was validated in a second sample of 108 patients and found to be better than that for (i) functional magnetic resonance imaging-guided regions; (ii) a region identified from an unguided lesion overlap map; and (iii) a region identified from voxel-based lesion-symptom mapping. Finally, consistent with prior findings from functional imaging and transcranial magnetic stimulation in healthy participants, we show how damage to our transcranial magnetic stimulation-guided regions affected performance on phonologically more than semantically demanding tasks. The observation that phonological processing abilities were impaired years after the stroke, suggests that other brain regions were not able to fully compensate for the contribution that the transcranial magnetic stimulation-guided regions make to language tasks. More generally, our novel transcranial magnetic stimulation-guided lesion-deficit mapping approach shows how non-invasive stimulation of the healthy brain can be used to guide the identification of regions where brain damage is likely to cause persistent behavioural effects.

The effect of speech distortion on the excitability of articulatory motor cortex.

It has become increasingly evident that human motor circuits are active during speech perception. However, the conditions under which the motor system modulates speech perception are not clear. Two prominent accounts make distinct predictions for how listening to speech engages speech motor representations. The first account suggests that the motor system is most strongly activated when observing familiar actions (Pickering and Garrod, 2013). Conversely, Wilson and Knoblich's account asserts that motor excitability is greatest when observing less familiar, ambiguous actions (Wilson and Knoblich, 2005). We investigated these predictions using transcranial magnetic stimulation (TMS). Stimulation of the lip and hand representations in the left primary motor cortex elicited motor evoked potentials (MEPs) indexing the excitability of the underlying motor representation. MEPs for lip, but not for hand, were larger during perception of distorted speech produced using a tongue depressor, relative to naturally produced speech. Additional somatotopic facilitation yielded significantly larger MEPs during perception of lip-articulated distorted speech sounds relative to distorted tongue-articulated sounds. Critically, there was a positive correlation between MEP size and the perception of distorted speech sounds. These findings were consistent with predictions made by Wilson & Knoblich (Wilson and Knoblich, 2005), and provide direct evidence of increased motor excitability when speech perception is difficult.

Inferior parietal lobule contributions to visual word recognition.

This study investigated how the left inferior parietal lobule (IPL) contributes to visual word recognition. We used repetitive TMS to temporarily disrupt neural information processing in two anatomical fields of the IPL, namely, the angular (ANG) and supramarginal (SMG) gyri, and observed the effects on reading tasks that focused attention on either the meaning or sounds of written words. Relative to no TMS, stimulation of the left ANG selectively slowed responses in the meaning, but not sound, task, whereas stimulation of the left SMG affected responses in the sound, but not meaning, task. These results demonstrate that ANG and SMG doubly dissociate in their contributions to visual word recognition. We suggest that this functional division of labor may be understood in terms of the distinct patterns of cortico-cortical connectivity resulting in separable functional circuits.

How Early Does the Brain Distinguish between Regular Words, Irregular Words, and Pseudowords during the Reading Process? Evidence from Neurochronometric TMS.

Cognitive theories on reading propose that the characteristics of written stimuli determine how they are processed in the brain. However, whether the brain distinguishes between regular words, irregular words, and pseudowords already at an early stage of the reading process is still subject to debate. Here we used chronometric TMS to address this issue. During the first 140 msec of regular word, irregular word, and pseudoword reading, TMS was used to disrupt the function of the ventral occipitotemporal, posterior middle temporal, and supramarginal gyri, which are key areas involved in orthographic, semantic, and phonological processing, respectively. Early TMS stimulation delivered on posterior middle temporal and supramarginal gyri affected regular and irregular word, but not pseudoword, reading. In contrast, ventral occipitotemporal disruption affected both word and pseudoword reading. We thus found evidence for an early distinction between word and pseudoword processing in the semantic and phonological systems, but not in the orthographic system.

An anatomical signature for literacy.

Language is a uniquely human ability that evolved at some point in the roughly 6,000,000 years since human and chimpanzee lines diverged. Even in the most linguistically impoverished environments, children naturally develop sophisticated language systems. In contrast, reading is a learnt skill that does not develop without intensive tuition and practice. Learning to read is likely to involve ontogenic structural brain changes, but these are nearly impossible to isolate in children owing to concurrent biological, environmental and social maturational changes. In Colombia, guerrillas are re-integrating into mainstream society and learning to read for the first time as adults. This presents a unique opportunity to investigate how literacy changes the brain, without the maturational complications present in children. Here we compare structural brain scans from those who learnt to read as adults (late-literates) with those from a carefully matched set of illiterates. Late-literates had more white matter in the splenium of the corpus callosum and more grey matter in bilateral angular, dorsal occipital, middle temporal, left supramarginal and superior temporal gyri. The importance of these brain regions for skilled reading was investigated in early literates, who learnt to read as children. We found anatomical connections linking the left and right angular and dorsal occipital gyri through the area of the corpus callosum where white matter was higher in late-literates than in illiterates; that reading, relative to object naming, increased the interhemispheric functional connectivity between the left and right angular gyri; and that activation in the left angular gyrus exerts top-down modulation on information flow from the left dorsal occipital gyrus to the left supramarginal gyrus. These findings demonstrate how the regions identified in late-literates interact during reading, relative to object naming, in early literates.

Inter- and intrahemispheric connectivity differences when reading Japanese Kanji and Hiragana.

Unlike most languages that are written using a single script, Japanese uses multiple scripts including morphographic Kanji and syllabographic Hiragana and Katakana. Here, we used functional magnetic resonance imaging with dynamic causal modeling to investigate competing theories regarding the neural processing of Kanji and Hiragana during a visual lexical decision task. First, a bilateral model investigated interhemispheric connectivity between ventral occipito-temporal (vOT) cortex and Broca's area ("pars opercularis"). We found that Kanji significantly increased the connection strength from right-to-left vOT. This is interpreted in terms of increased right vOT activity for visually complex Kanji being integrated into the left (i.e. language dominant) hemisphere. Secondly, we used a unilateral left hemisphere model to test whether Kanji and Hiragana rely preferentially on ventral and dorsal paths, respectively, that is, they have different intrahemispheric functional connectivity profiles. Consistent with this hypothesis, we found that Kanji increased connectivity within the ventral path (V1 ↔ vOT ↔ Broca's area), and that Hiragana increased connectivity within the dorsal path (V1 ↔ supramarginal gyrus ↔ Broca's area). Overall, the results illustrate how the differential processing demands of Kanji and Hiragana influence both inter- and intrahemispheric interactions.

The neural representation of abstract words: the role of emotion.

It is generally assumed that abstract concepts are linguistically coded, in line with imaging evidence of greater engagement of the left perisylvian language network for abstract than concrete words (Binder JR, Desai RH, Graves WW, Conant LL. 2009. Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cerebral Cortex. 19:2767-2796; Wang J, Conder JA, Blitzer DN, Shinkareva SV. 2010. Neural representation of abstract and concrete concepts: A meta-analysis of neuroimaging studies. Hum Brain Map. 31:1459-1468). Recent behavioral work, which used tighter matching of items than previous studies, however, suggests that abstract concepts also entail affective processing to a greater extent than concrete concepts (Kousta S-T, Vigliocco G, Vinson DP, Andrews M, Del Campo E. The representation of abstract words: Why emotion matters. J Exp Psychol Gen. 140:14-34). Here we report a functional magnetic resonance imaging experiment that shows greater engagement of the rostral anterior cingulate cortex, an area associated with emotion processing (e.g., Etkin A, Egner T, Peraza DM, Kandel ER, Hirsch J. 2006. Resolving emotional conflict: A role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron. 52:871), in abstract processing. For abstract words, activation in this area was modulated by the hedonic valence (degree of positive or negative affective association) of our items. A correlation analysis of more than 1,400 English words further showed that abstract words, in general, receive higher ratings for affective associations (both valence and arousal) than concrete words, supporting the view that engagement of emotional processing is generally required for processing abstract words. We argue that these results support embodiment views of semantic representation, according to which, whereas concrete concepts are grounded in our sensory-motor experience, affective experience is crucial in the grounding of abstract concepts.

Can extreme experiences enhance creativity? The case of the underwater nightclub.

Creativity is a valuable commodity. Research has revealed some identifying characteristics of creative people and some of the emotional states that can bring out the most creativity in all of us. It has also been shown that the long-term experience of different cultures and lifestyles that is the result of travel and immigration can also enhance creativity. However, the role of one-off, extreme, or unusual experiences on creativity has not been directly observed before. In part, that may be because, by their very nature, such experiences are very difficult to bring into the laboratory. Here, we brought the tools and empirical methods of the laboratory into the wild, measuring the psychological effects of a unique multisensory experience: an underwater nightclub. We showed - with fully randomized and experimentally controlled conditions - that such an experience boosted measures of divergent thinking in participants. This demonstrates that one element of creativity can be directly enhanced by unusual situations, and that experimental tools of psychology can be used to investigate a range of consumer experiences.

Speech motor facilitation is not affected by ageing but is modulated by task demands during speech perception.

Motor areas for speech production activate during speech perception. Such activation may assist speech perception in challenging listening conditions. It is not known how ageing affects the recruitment of articulatory motor cortex during active speech perception. This study aimed to determine the effect of ageing on recruitment of speech motor cortex during speech perception. Single-pulse Transcranial Magnetic Stimulation (TMS) was applied to the lip area of left primary motor cortex (M1) to elicit lip Motor Evoked Potentials (MEPs). The M1 hand area was tested as a control site. TMS was applied whilst participants perceived syllables presented with noise (-10, 0, +10 dB SNRs) and without noise (clear). Participants detected and counted syllables throughout MEP recording. Twenty younger adult subjects (aged 18-25) and twenty older adult subjects (aged 65-78) participated in this study. Results indicated a significant interaction between age and noise condition in the syllable task. Specifically, older adults significantly misidentified syllables in the 0 dB SNR condition, and missed the syllables in the -10 dB SNR condition, relative to the clear condition. There were no differences between conditions for younger adults. There was a significant main effect of noise level on lip MEPs. Lip MEPs were unexpectedly inhibited in the 0 dB SNR condition relative to clear condition. There was no interaction between age group and noise condition. There was no main effect of noise or age group on control hand MEPs. These data suggest that speech-induced facilitation in articulatory motor cortex is abolished when performing a challenging secondary task, irrespective of age.

Hunt-Vitell's General Theory of Marketing Ethics Predicts "Attitude-Behaviour" Gap in Pro-environmental Domain.

The inconsistency between pro-environmental attitudes and behaviours, known as the "attitude-behaviour" gap, is exceptionally pronounced in scenarios associated with "green" choice. The current literature offers numerous explanations for the reasons behind the "attitude-behaviour" gap, however, the generalisability of these explanations is complex. In addition, the answer to the question of whether the gap occurs between attitudes and intentions, or intentions and behaviours is also unknown. In this study, we propose the moral dimension as a generalisable driver of the "attitude-behaviour" gap and investigate its effectiveness in predicting attitudes, pro-environmental intentions and subsequent behaviours. We do so by using Hunt-Vitell's moral philosophy-based framework of ethical decision-making, which conceptualises morality as the central decision-making parameter. The results from 557 US MTurk participants revealed that the manipulation of moral dimensions, specifically deontology and teleology, impacted ethical evaluation of presented dilemmas, however, failed to translate into subsequent intentions and behaviours. This finding suggests (i) that the moral dimension has an effect in shaping attitudes toward environmental issues, and (ii) that gap occurs between attitudes and intentions rather than intentions and behaviours. Further investigation of what strengthens and/or overrides the effects of the moral dimension would help understand the reasons why moral attitudes do not always translate into subsequent intentions and behaviours in the pro-environmental domain.

How does learning to read affect speech perception?

Behavioral studies have demonstrated that learning to read and write affects the processing of spoken language. The present study investigates the neural mechanism underlying the emergence of such orthographic effects during speech processing. Transcranial magnetic stimulation (TMS) was used to tease apart two competing hypotheses that consider this orthographic influence to be either a consequence of a change in the nature of the phonological representations during literacy acquisition or a consequence of online coactivation of the orthographic and phonological representations during speech processing. Participants performed an auditory lexical decision task in which the orthographic consistency of spoken words was manipulated and repetitive TMS was used to interfere with either phonological or orthographic processing by stimulating left supramarginal gyrus (SMG) or left ventral occipitotemporal cortex (vOTC), respectively. The advantage for consistently spelled words was removed only when the stimulation was delivered to SMG and not to vOTC, providing strong evidence that this effect arises at a phonological, rather than an orthographic, level. We propose a possible mechanistic explanation for the role of SMG in phonological processing and how this is affected by learning to read.

Improving the reliability of functional localizers.

A critical assumption underlying the practice of functional localization is that the voxels identified by functional localization are essentially the same as those activated in the main experiment for a particular anatomical area. Violations of this assumption bias the resulting analyses and can dramatically increase the likelihood of both Type I and Type II errors. Here we investigated how the amount of data affects the reliability of a set of common functionally-defined regions-of-interest (fROIs). Four participants were scanned ten times each to functionally localize extrastriate regions sensitive to visually presented words, objects and faces. A within-subject random-effects analysis was used as the "gold standard" for identifying the fROIs and the results were compared to within-subject, fixed-effect analyses typically used for functional localization. By varying the quantity of data included in the analyses, we empirically assessed the amount needed to ensure reliable identification of the fROIs. The results demonstrated that the most consistent fROIs were based on either stringent statistical thresholding (Z>5.0) of large quantities of data or on lenient thresholding (Z>2.3) of a modest amount of data, with both methods yielding 70-80% overlap between the functional localization results and the "gold standard." Stringent statistical thresholds on typical quantities of localizer data led to the poorest reliability (<20% overlap). These findings suggest that the most reliable and cost-efficient method for functional localization involves collecting a relatively small amount of data (~10 min) and using a lenient statistical threshold to identify all voxels in a given region that are sensitive to the process-of-interest.

Top-down modulation of ventral occipito-temporal responses during visual word recognition.

Although interactivity is considered a fundamental principle of cognitive (and computational) models of reading, it has received far less attention in neural models of reading that instead focus on serial stages of feed-forward processing from visual input to orthographic processing to accessing the corresponding phonological and semantic information. In particular, the left ventral occipito-temporal (vOT) cortex is proposed to be the first stage where visual word recognition occurs prior to accessing nonvisual information such as semantics and phonology. We used functional magnetic resonance imaging (fMRI) to investigate whether there is evidence that activation in vOT is influenced top-down by the interaction of visual and nonvisual properties of the stimuli during visual word recognition tasks. Participants performed two different types of lexical decision tasks that focused on either visual or nonvisual properties of the word or word-like stimuli. The design allowed us to investigate how vOT activation during visual word recognition was influenced by a task change to the same stimuli and by a stimulus change during the same task. We found both stimulus- and task-driven modulation of vOT activation that can only be explained by top-down processing of nonvisual aspects of the task and stimuli. Our results are consistent with the hypothesis that vOT acts as an interface linking visual form with nonvisual processing in both bottom up and top down directions. Such interactive processing at the neural level is in agreement with cognitive and computational models of reading but challenges some of the assumptions made by current neuro-anatomical models of reading.

Expertise with artificial nonspeech sounds recruits speech-sensitive cortical regions.

Regions of the human temporal lobe show greater activation for speech than for other sounds. These differences may reflect intrinsically specialized domain-specific adaptations for processing speech, or they may be driven by the significant expertise we have in listening to the speech signal. To test the expertise hypothesis, we used a video-game-based paradigm that tacitly trained listeners to categorize acoustically complex, artificial nonlinguistic sounds. Before and after training, we used functional MRI to measure how expertise with these sounds modulated temporal lobe activation. Participants' ability to explicitly categorize the nonspeech sounds predicted the change in pretraining to posttraining activation in speech-sensitive regions of the left posterior superior temporal sulcus, suggesting that emergent auditory expertise may help drive this functional regionalization. Thus, seemingly domain-specific patterns of neural activation in higher cortical regions may be driven in part by experience-based restructuring of high-dimensional perceptual space.

Investigating occipito-temporal contributions to reading with TMS.

The debate regarding the role of ventral occipito-temporal cortex (vOTC) in visual word recognition arises, in part, from difficulty delineating the functional contributions of vOTC as separate from other areas of the reading network. Here, we investigated the feasibility of using TMS to interfere with vOTC processing in order to explore its specific contributions to visual word recognition. Three visual lexical decision experiments were conducted using neuronavigated TMS. The first demonstrated that repetitive stimulation of vOTC successfully slowed word, but not nonword, responses. The second confirmed and extended these findings by demonstrating the effect was specific to vOTC and not present in the adjacent lateral occipital complex. The final experiment used paired-pulse TMS to investigate the time course of vOTC processing for words and revealed activation starting as early as 80-120 msec poststimulus onset-significantly earlier than that expected based on electrophysiological and magnetoencephalography studies. Taken together, these results clearly indicate that TMS can be successfully used to stimulate parts of vOTC previously believed to be inaccessible and provide a new tool for systematically investigating the information processing characteristics of vOTC. In addition, the findings provide strong evidence that lexical status and frequency significantly affect vOTC processing, findings difficult to reconcile with prelexical accounts of vOTC function.

The role of the left head of caudate in suppressing irrelevant words.

Suppressing irrelevant words is essential to successful speech production and is expected to involve general control mechanisms that reduce interference from task-unrelated processing. To investigate the neural mechanisms that suppress visual word interference, we used fMRI and a Stroop task, using a block design with an event-related analysis. Participants indicated with a finger press whether a visual stimulus was colored pink or blue. The stimulus was either the written word "BLUE," the written word "PINK," or a string of four Xs, with word interference introduced when the meaning of the word and its color were "incongruent" (e.g., BLUE in pink hue) relative to congruent (e.g., BLUE in blue) or neutral (e.g., XXXX in pink). The participants also made color decisions in the presence of spatial interference rather than word interference (i.e., the Simon task). By blocking incongruent, congruent, and neutral trials, we identified activation related to the mechanisms that suppress interference as that which was greater at the end relative to the start of incongruency. This highlighted the role of the left head of caudate in the control of word interference but not spatial interference. The response in the left head of caudate contrasted to bilateral inferior frontal activation that was greater at the start than at the end of incongruency, and to the dorsal anterior cingulate gyrus which responded to a change in the motor response. Our study therefore provides novel insights into the role of the left head of caudate in the mechanisms that suppress word interference.

On-line plasticity in spoken sentence comprehension: Adapting to time-compressed speech.

Listeners show remarkable flexibility in processing variation in speech signal. One striking example is the ease with which they adapt to novel speech distortions such as listening to someone with a foreign accent. Behavioural studies suggest that significant improvements in comprehension occur rapidly--often within 10-20 sentences. In the present experiment, we investigate the neural changes underlying on-line adaptation to distorted speech using time-compressed speech. Listeners performed a sentence verification task on normal-speed and time-compressed sentences while their neural responses were recorded using fMRI. The results showed that rapid learning of the time-compressed speech occurred during presentation of the first block of 16 sentences and was associated with increased activation in left and right auditory association cortices and in left ventral premotor cortex. These findings suggest that the ability to adapt to a distorted speech signal may, in part, rely on mapping novel acoustic patterns onto existing articulatory motor plans, consistent with the idea that speech perception involves integrating multi-modal information including auditory and motoric cues.