Switching off: disruptive TMS reveals distinct contributions of the posterior middle temporal gyrus and angular gyrus to bilingual speech production.

The role of the left temporoparietal cortex in speech production has been extensively studied during native language processing, proving crucial in controlled lexico-semantic retrieval under varying cognitive demands. Yet, its role in bilinguals, fluent in both native and second languages, remains poorly understood. Here, we employed continuous theta burst stimulation to disrupt neural activity in the left posterior middle-temporal gyrus (pMTG) and angular gyrus (AG) while Italian-Friulian bilinguals performed a cued picture-naming task. The task involved between-language (naming objects in Italian or Friulian) and within-language blocks (naming objects ["knife"] or associated actions ["cut"] in a single language) in which participants could either maintain (non-switch) or change (switch) instructions based on cues. During within-language blocks, cTBS over the pMTG entailed faster naming for high-demanding switch trials, while cTBS to the AG elicited slower latencies in low-demanding non-switch trials. No cTBS effects were observed in the between-language block. Our findings suggest a causal involvement of the left pMTG and AG in lexico-semantic processing across languages, with distinct contributions to controlled vs. "automatic" retrieval, respectively. However, they do not support the existence of shared control mechanisms within and between language(s) production. Altogether, these results inform neurobiological models of semantic control in bilinguals.

Multivariate word properties in fluency tasks reveal markers of Alzheimer's dementia.

INTRODUCTION: Verbal fluency tasks are common in Alzheimer's disease (AD) assessments. Yet, standard valid response counts fail to reveal disease-specific semantic memory patterns. Here, we leveraged automated word-property analysis to capture neurocognitive markers of AD vis-à-vis behavioral variant frontotemporal dementia (bvFTD). METHODS: Patients and healthy controls completed two fluency tasks. We counted valid responses and computed each word's frequency, granularity, neighborhood, length, familiarity, and imageability. These features were used for group-level discrimination, patient-level identification, and correlations with executive and neural (magnetic resonanance imaging [MRI], functional MRI [fMRI], electroencephalography [EEG]) patterns. RESULTS: Valid responses revealed deficits in both disorders. Conversely, frequency, granularity, and neighborhood yielded robust group- and subject-level discrimination only in AD, also predicting executive outcomes. Disease-specific cortical thickness patterns were predicted by frequency in both disorders. Default-mode and salience network hypoconnectivity, and EEG beta hypoconnectivity, were predicted by frequency and granularity only in AD. DISCUSSION: Word-property analysis of fluency can boost AD characterization and diagnosis. HIGHLIGHTS: We report novel word-property analyses of verbal fluency in AD and bvFTD. Standard valid response counts captured deficits and brain patterns in both groups. Specific word properties (e.g., frequency, granularity) were altered only in AD. Such properties predicted cognitive and neural (MRI, fMRI, EEG) patterns in AD. Word-property analysis of fluency can boost AD characterization and diagnosis.

Increased top-down semantic processing in natural speech linked to better reading in dyslexia.

Early research proposed that individuals with developmental dyslexia use contextual information to facilitate lexical access and compensate for phonological deficits. Yet at present there is no corroborating neuro-cognitive evidence. We explored this with a novel combination of magnetoencephalography (MEG), neural encoding and grey matter volume analyses. We analysed MEG data from 41 adult native Spanish speakers (14 with dyslexic symptoms) who passively listened to naturalistic sentences. We used multivariate Temporal Response Function analysis to capture online cortical tracking of both auditory (speech envelope) and contextual information. To compute contextual information tracking we used word-level Semantic Surprisal derived using a Transformer Neural Network language model. We related online information tracking to participants' reading scores and grey matter volumes within the reading-linked cortical network. We found that right hemisphere envelope tracking was related to better phonological decoding (pseudoword reading) for both groups, with dyslexic readers performing worse overall at this task. Consistently, grey matter volume in the superior temporal and bilateral inferior frontal areas increased with better envelope tracking abilities. Critically, for dyslexic readers only, stronger Semantic Surprisal tracking in the right hemisphere was related to better word reading. These findings further support the notion of a speech envelope tracking deficit in dyslexia and provide novel evidence for top-down semantic compensatory mechanisms.

Contextual Priors Guide Perception and Motor Responses to Observed Actions.

In everyday-life scenarios, prior expectations provided by the context in which actions are embedded support action prediction. However, it is still unclear how newly learned action-context associations can drive our perception and motor responses. To fill this gap, we measured behavioral (Experiment 1) and motor responses (Experiment 2) during two tasks requiring the prediction of occluded actions or geometrical shapes. Each task consisted of an implicit probabilistic learning and a test phase. During learning, we exposed participants to videos showing specific associations between a contextual cue and a particular action or shape. During the test phase, videos were earlier occluded to reduce the amount of sensorial information and induce participants to use the implicitly learned action/shape-context associations for disambiguation. Results showed that reliable contextual cues made participants more accurate in identifying the unfolding action or shape. Importantly, motor responses were modulated by contextual probability during action, but not shape prediction. Particularly, in conditions of perceptual uncertainty the motor system coded for the most probable action based on contextual informativeness, regardless of action kinematics. These findings suggest that contextual priors can shape motor responses to action observation beyond mere kinematics mapping.

Spatial frequency tuning of motor responses reveals differential contribution of dorsal and ventral systems to action comprehension.

Understanding object-directed actions performed by others is central to everyday life. This ability is thought to rely on the interaction between the dorsal action observation network (AON) and a ventral object recognition pathway. On this view, the AON would encode action kinematics, and the ventral pathway, the most likely intention afforded by the objects. However, experimental evidence supporting this model is still scarce. Here, we aimed to disentangle the contribution of dorsal vs. ventral pathways to action comprehension by exploiting their differential tuning to low-spatial frequencies (LSFs) and high-spatial frequencies (HSFs). We filtered naturalistic action images to contain only LSF or HSF and measured behavioral performance and corticospinal excitability (CSE) using transcranial magnetic stimulation (TMS). Actions were embedded in congruent or incongruent scenarios as defined by the compatibility between grips and intentions afforded by the contextual objects. Behaviorally, participants were better at discriminating congruent actions in intact than LSF images. This effect was reversed for incongruent actions, with better performance for LSF than intact and HSF. These modulations were mirrored at the neurophysiological level, with greater CSE facilitation for congruent than incongruent actions for HSF and the opposite pattern for LSF images. Finally, only for LSF did we observe CSE modulations according to grip kinematics. While results point to differential dorsal (LSF) and ventral (HSF) contributions to action comprehension for grip and context encoding, respectively, the negative congruency effect for LSF images suggests that object processing may influence action perception not only through ventral-to-dorsal connections, but also through a dorsal-to-dorsal route involved in predictive processing.

A novel cognitive neurosurgery approach for supramaximal resection of non-dominant precuneal gliomas: a case report.

Despite mounting evidence pointing to the contrary, classical neurosurgery presumes many cerebral regions are non-eloquent, and therefore, their excision is possible and safe. This is the case of the precuneus and posterior cingulate, two interacting hubs engaged during various cognitive functions, including reflective self-awareness; visuospatial and sensorimotor processing; and processing social cues. This inseparable duo ensures the cortico-subcortical connectivity that underlies these processes. An adult presenting a right precuneal low-grade glioma invading the posterior cingulum underwent awake craniotomy with direct electrical stimulation (DES). A supramaximal resection was achieved after locating the superior longitudinal fasciculus II. During surgery, we found sites of positive stimulation for line bisection and mentalizing tests that enabled the identification of surgical corridors and boundaries for lesion resection. When post-processing the intraoperative recordings, we further identified areas that positively responded to DES during the trail-making and mentalizing tests. In addition, a clear worsening of the patient's self-assessment ability was observed throughout the surgery. An awake cognitive neurosurgery approach allowed supramaximal resection by reaching the cortico-subcortical functional limits. The mapping of complex functions such as social cognition and self-awareness is key to preserving patients' postoperative cognitive health by maximizing the ability to resect the lesion and surrounding areas.

Decoding motor expertise from fine-tuned oscillatory network organization.

Can motor expertise be robustly predicted by the organization of frequency-specific oscillatory brain networks? To answer this question, we recorded high-density electroencephalography (EEG) in expert Tango dancers and naïves while viewing and judging the correctness of Tango-specific movements and during resting. We calculated task-related and resting-state connectivity at different frequency-bands capturing task performance (delta [δ], 1.5-4 Hz), error monitoring (theta [θ], 4-8 Hz), and sensorimotor experience (mu [µ], 8-13 Hz), and derived topographical features using graph analysis. These features, together with canonical expertise measures (i.e., performance in action discrimination, time spent dancing Tango), were fed into a data-driven computational learning analysis to test whether behavioral and brain signatures robustly classified individuals depending on their expertise level. Unsurprisingly, behavioral measures showed optimal classification (100%) between dancers and naïves. When considering brain models, the task-based classification performed well (~73%), with maximal discrimination afforded by theta-band connectivity, a hallmark signature of error processing. Interestingly, mu connectivity during rest outperformed (100%) the task-based approach, matching the optimal classification of behavioral measures and thus emerging as a potential trait-like marker of sensorimotor network tuning by intense training. Overall, our findings underscore the power of fine-tuned oscillatory network signatures for capturing expertise-related differences and their potential value in the neuroprognosis of learning outcomes.

Oscillatory and structural signatures of language plasticity in brain tumor patients: A longitudinal study.

Recent evidence suggests that damage to the language network triggers its functional reorganization. Yet, the spectro-temporal fingerprints of this plastic rearrangement and its relation to anatomical changes is less well understood. Here, we combined magnetoencephalographic recordings with a proxy measure of white matter to investigate oscillatory activity supporting language plasticity and its relation to structural reshaping. First, cortical dynamics were acquired in a group of healthy controls during object and action naming. Results showed segregated beta (13-28 Hz) power decreases in left ventral and dorsal pathways, in a time-window associated to lexico-semantic processing (~250-500 ms). Six patients with left tumors invading either ventral or dorsal regions performed the same naming task before and 3 months after surgery for tumor resection. When longitudinally comparing patients' responses we found beta compensation mimicking the category-based segregation showed by controls, with ventral and dorsal damage leading to selective compensation for object and action naming, respectively. At the structural level, all patients showed preoperative changes in white matter tracts possibly linked to plasticity triggered by tumor growth. Furthermore, in some patients, structural changes were also evident after surgery and showed associations with longitudinal changes in beta power lateralization toward the contralesional hemisphere. Overall, our findings support the existence of anatomo-functional dependencies in language reorganization and highlight the potential role of oscillatory markers in tracking longitudinal plasticity in brain tumor patients. By doing so, they provide valuable information for mapping preoperative and postoperative neural reshaping and plan surgical strategies to preserve language function and patient's quality of life.

MULTIMAP: Multilingual picture naming test for mapping eloquent areas during awake surgeries.

Picture naming tasks are currently the gold standard for identifying and preserving language-related areas during awake brain surgery. With multilingual populations increasing worldwide, patients frequently need to be tested in more than one language. There is still no reliable testing instrument, as the available batteries have been developed for specific languages. Heterogeneity in the selection criteria for stimuli leads to differences, for example, in the size, color, image quality, and even names associated with pictures, making direct cross-linguistic comparisons difficult. Here we present MULTIMAP, a new multilingual picture naming test for mapping eloquent areas during awake brain surgery. Recognizing that the distinction between nouns and verbs is necessary for detailed and precise language mapping, MULTIMAP consists of a database of 218 standardized color pictures representing both objects and actions. These images have been tested for name agreement with speakers of Spanish, Basque, Catalan, Italian, French, English, German, Mandarin Chinese, and Arabic, and have been controlled for relevant linguistic features in cross-language combinations. The MULTIMAP test for objects and verbs represents an alternative to the Oral Denomination 80 (DO 80) monolingual pictorial set currently used in language mapping, providing an open-source, standardized set of up-to-date pictures, where relevant linguistic variables across several languages have been taken into account in picture creation and selection.

Contextual priors do not modulate action prediction in children with autism.

Bayesian accounts of autism suggest that this disorder may be rooted in an impaired ability to estimate the probability of future events, possibly owing to reduced priors. Here, we tested this hypothesis within the action domain in children with and without autism using a behavioural paradigm comprising a familiarization and a testing phase. During familiarization, children observed videos depicting a child model performing actions in diverse contexts. Crucially, within this phase, we implicitly biased action-context associations in terms of their probability of co-occurrence. During testing, children observed the same videos but drastically shortened (i.e. reduced amount of kinematics information) and were asked to infer action unfolding. Since during the testing phase movement kinematics became ambiguous, we expected children's responses to be biased to contextual priors, thus compensating for perceptual uncertainty. While this probabilistic effect was present in controls, no such modulation was observed in autistic children, overall suggesting an impairment in using contextual priors when predicting other peoples' actions in uncertain environments.

Dissociated Representations of Deceptive Intentions and Kinematic Adaptations in the Observer's Motor System.

Previous studies showed that observing deceptive actions modulates the activity of the observer's motor system. However, it is unclear whether this modulation reflects the coding of deceptive intentions or the mapping of the kinematic adaptations required to attain deceptive actions. Here, we used single-pulse transcranial magnetic stimulation to measure cortico-spinal excitability (CSE) from hand and forearm muscles while participants predicted the weight of cubes lifted by actors who received truthful information on the object weight and provided 1) truthful (truthful actions) or 2) deceptive (deceptive actions) cues to the observers or 3) who received fooling information and were asked to provide truthful cues (deceived actions). This way, we independently manipulated actor's intentions and kinematic adaptations. We found that, as compared to truthful action observation, CSE increased during observation of deceptive actions, but decreased during observation of deceived actions. Importantly, while the CSE enhancement in response to deceptive intentions lacked muscle specificity, perceiving kinematic alterations in the deceived condition affected CSE only for the hand muscle involved in kinematic adaptations to unexpected object weight. This suggests that actor's intentions and movement kinematics may be coded by the observer's motor system at different hierarchical levels of action representation.

Contextualizing action observation in the predictive brain: Causal contributions of prefrontal and middle temporal areas.

Context facilitates the recognition of forthcoming actions by pointing to which intention is likely to drive them. This intention is thought to be estimated in a ventral pathway linking MTG with frontal regions and to further impact on the implementation of sensory predictions within the action observation network (AON). Additionally, when conflicting intentions are estimated from context, the DLPFC may bias action selection. However, direct evidence for the contribution of these areas to context-embedded action representations in the AON is still lacking. Here, we used a perturb-and-measure TMS-approach to disrupt neural activity, separately in MTG and DLPFC and subsequently measure cortico-spinal excitability while observing actions embedded in congruent, incongruent or ambiguous contexts. Context congruency was manipulated in terms of compatibility between observed kinematics and the action goal suggested by the ensemble of objects depicted in the environment. In the control session (vertex), we found an early facilitation and later inhibition for kinematics embedded in congruent and incongruent contexts, respectively. MTG stimulation altered the differential modulation of M1 response to congruent vs. incongruent contexts, suggesting this area specifies prior representations about appropriate object graspability. Interestingly, all effects were abolished after DLPFC stimulation highlighting its critical role in broader contextual modulation of the AON activity.

Tracking the Time Course of Top-Down Contextual Effects on Motor Responses during Action Comprehension.

Context plays a key role in coding high-level components of others' behavior, including the goal and the intention of an observed action. However, little is known about its possible role in shaping lower levels of action processing, such as simulating action kinematics and muscular activity. Furthermore, there is no evidence regarding the time course and the neural mechanisms subserving this modulation. To address these issues, we combined single-pulse transcranial magnetic stimulation and motor-evoked potentials while healthy humans watched videos of everyday actions embedded in congruent, incongruent, or ambiguous contexts. Video endings were occluded from view and participants had to predict action unfolding. Transcranial magnetic stimulation was delivered at 80, 240, and 400 ms after action onset. An earlier selective facilitation of motor resonance occurring at 240 ms was observed for actions embedded in congruent contexts, compared with those occurring in incongruent and ambiguous ones. Later on, at 400 ms, a selective inhibition of motor resonance was found for actions embedded in incongruent contexts, compared with those taking place in congruent and ambiguous ones. No modulations were observed at 80 ms. Together, these findings indicate that motor resonance can be modulated by contextual information with different timings, depending on the (in)congruency between the different levels of action representation. Furthermore, the different time course of these effects suggests that they stem from partially independent mechanisms, with the early facilitation directly involving M1, and the later inhibition recruiting high-level structures outside the motor system. SIGNIFICANCE STATEMENT: Previous studies indicate that, when we observe other people's actions, the context in which actions take place influences intention understanding. However, little is known about the precise mechanisms involved in the contextual modulation of action representation (i.e., inhibition vs facilitation) and how they unfold in time. The present study sheds light on these aspects. Specifically, we show an early top-down facilitation (at ∼240 ms) and a later inhibition (at ∼400 ms) of motor resonance in response to actions observed in congruent and incongruent contexts, respectively.

Variability in functional brain networks predicts expertise during action observation.

Observing an action performed by another individual activates, in the observer, similar circuits as those involved in the actual execution of that action. This activation is modulated by prior experience; indeed, sustained training in a particular motor domain leads to structural and functional changes in critical brain areas. Here, we capitalized on a novel graph-theory approach to electroencephalographic data (Fraiman et al., 2016) to test whether variability in functional brain networks implicated in Tango observation can discriminate between groups differing in their level of expertise. We found that experts and beginners significantly differed in the functional organization of task-relevant networks. Specifically, networks in expert Tango dancers exhibited less variability and a more robust functional architecture. Notably, these expertise-dependent effects were captured within networks derived from electrophysiological brain activity recorded in a very short time window (2s). In brief, variability in the organization of task-related networks seems to be a highly sensitive indicator of long-lasting training effects. This finding opens new methodological and theoretical windows to explore the impact of domain-specific expertise on brain plasticity, while highlighting variability as a fruitful measure in neuroimaging research.

Contextual modulation of motor resonance during the observation of everyday actions.

Neuroimaging studies on action observation suggest that context plays a key role in coding high-level components of motor behavior, including the short-term and the end-goal of an action. However, little is known about the possible role of context in shaping lower-levels of action processing such as reading action kinematics and simulating muscular activity. Here, we combined single-pulse TMS and motor-evoked potentials (MEPs) recording to explore whether top-down contextual information is capable of modulating low-level motor representations. We recorded MEPs from FDI and FCR muscles while participants watched videos about everyday actions embedded in congruent, incongruent or ambiguous contexts. Videos were interrupted before action ending, and participants were requested to predict the course of the observed action. A contextual modulation of corticospinal excitability was observed only for the FDI muscle, which is specifically involved in the execution of reaching-to-grasping movements, and whose corticospinal pathway is influenced by the observation of the very same movements. This modulation was reflected in a selective decrease of corticospinal excitability during the observation of actions embedded in incongruent as compared to congruent and ambiguous contexts. These findings indicate that motor resonance is not an entirely automatic process, but it can be modulated by high-level contextual representations.

Familiarity modulates motor activation while other species' actions are observed: a magnetic stimulation study.

Observing other people's actions facilitates the observer's motor system as compared with observing the same individuals at rest. This motor activation is thought to result from mirror-like activity in fronto-parietal areas, which enhances the excitability of the primary motor cortex via cortico-cortical pathways. Although covert motor activation in response to observed actions has been widely investigated between conspecifics, how humans cope with other species' actions has received less attention. For example, it remains unclear whether the human motor system is activated by observing other species' actions, and whether prior familiarity with the non-conspecific agent modulates this activation. Here, we combined single-pulse transcranial magnetic stimulation and motor-evoked potential recording to explore the impact of familiarity on motor activation during the observation of non-conspecific actions. Videos displaying actions performed either by a conspecific (human) or by a non-conspecific (dog) were shown to individuals who had prior familiarity or no familiarity at all with the non-conspecific agent. We found that, whereas individuals with long-lasting familiarity showed similar levels of motor activation for human and canine actions, individuals who had no familiarity showed higher motor activation for human than for canine actions. These findings suggest that the human motor system is flexible enough to resonate with other species, and that familiarity plays a key role in tuning this ability.

Time to Tango: expertise and contextual anticipation during action observation.

Predictive theories of action observation propose that we use our own motor system as a guide for anticipating and understanding other people's actions through the generation of context-based expectations. According to this view, people should be better in predicting and interpreting those actions that are present in their own motor repertoire compared to those that are not. We recorded high-density event-related potentials (ERPs: P300, N400 and Slow Wave, SW) and source estimation in 80 subjects separated by their level of expertise (experts, beginners and naïves) as they observed realistic videos of Tango steps with different degrees of execution correctness. We also performed path analysis to infer causal relationships between ongoing anticipatory brain activity, evoked semantic responses, expertise measures and behavioral performance. We found that anticipatory activity, with sources in a fronto-parieto-occipital network, early discriminated between groups according to their level of expertise. Furthermore, this early activity significantly predicted subsequent semantic integration indexed by semantic responses (N400 and SW, sourced in temporal and motor regions) which also predicted motor expertise. In addition, motor expertise was a good predictor of behavioral performance. Our results show that neural and temporal dynamics underlying contextual action anticipation and comprehension can be interpreted in terms of successive levels of contextual prediction that are significantly modulated by subject's prior experience.

Decoding bilingualism from resting-state oscillatory network organization.

Can lifelong bilingualism be robustly decoded from intrinsic brain connectivity? Can we determine, using a spectrally resolved approach, the oscillatory networks that better predict dual-language experience? We recorded resting-state magnetoencephalographic activity in highly proficient Spanish-Basque bilinguals and Spanish monolinguals, calculated functional connectivity at canonical frequency bands, and derived topological network properties using graph analysis. These features were fed into a machine learning classifier to establish how robustly they discriminated between the groups. The model showed excellent classification (AUC: 0.91 ± 0.12) between individuals in each group. The key drivers of classification were network strength in beta (15-30 Hz) and delta (2-4 Hz) rhythms. Further characterization of these networks revealed the involvement of temporal, cingulate, and fronto-parietal hubs likely underpinning the language and default-mode networks (DMNs). Complementary evidence from a correlation analysis showed that the top-ranked features that better discriminated individuals during rest also explained interindividual variability in second language (L2) proficiency within bilinguals, further supporting the robustness of the machine learning model in capturing trait-like markers of bilingualism. Overall, our results show that long-term experience with an L2 can be "brain-read" at a fine-grained level from resting-state oscillatory network organization, highlighting its pervasive impact, particularly within language and DMN networks.

Electrophysiological alterations during action semantic processing in Parkinson's disease.

Assessments of action semantics consistently reveal markers of Parkinson's disease (PD). However, neurophysiological signatures of the domain remain under-examined in this population, especially under conditions that allow patients to process stimuli without stringent time constraints. Here we assessed event-related potentials and time-frequency modulations in healthy individuals (HPs) and PD patients during a delayed-response semantic judgment task involving related and unrelated action-picture pairs. Both groups had shorter response times for related than for unrelated trials, but they exhibited discrepant electrophysiological patterns. HPs presented significantly greater N400 amplitudes as well as theta enhancement and mu desynchronization for unrelated relative to related trials. Conversely, N400 and theta modulations were abolished in the patients, who further exhibited a contralateralized cluster in the mu range. None of these patterns were associated with the participants' cognitive status. Our results suggest that PD involves multidimensional neurophysiological disruptions during action-concept processing, even under task conditions that elicit canonical behavioral effects. New constraints thus emerge for translational neurocognitive models of the disease.

"Left and right prefrontal routes to action comprehension".

Successful action comprehension requires the integration of motor information and semantic cues about objects in context. Previous evidence suggests that while motor features are dorsally encoded in the fronto-parietal action observation network (AON); semantic features are ventrally processed in temporal structures. Importantly, these dorsal and ventral routes seem to be preferentially tuned to low (LSF) and high (HSF) spatial frequencies, respectively. Recently, we proposed a model of action comprehension where we hypothesized an additional route to action understanding whereby coarse LSF information about objects in context is projected to the dorsal AON via the prefrontal cortex (PFC), providing a prediction signal of the most likely intention afforded by them. Yet, this model awaits for experimental testing. To this end, we used a perturb-and-measure continuous theta burst stimulation (cTBS) approach, selectively disrupting neural activity in the left and right PFC and then evaluating the participant's ability to recognize filtered action stimuli containing only HSF or LSF. We find that stimulation over PFC triggered different spatial-frequency modulations depending on lateralization: left-cTBS and right-cTBS led to poorer performance on HSF and LSF action stimuli, respectively. Our findings suggest that left and right PFC exploit distinct spatial frequencies to support action comprehension, providing evidence for multiple routes to social perception in humans.