Lateralization of dorsal fiber tract targeting Broca's area concurs with language skills during development.

Language is bounded to the left hemisphere in the adult brain and the functional lateralization can already be observed early during development. Here we investigate whether this is paralleled by a lateralization of the white matter structural language network. We analyze the strength and microstructural properties of language-related fiber tracts connecting temporal and frontal cortices with a separation of two dorsal tracts, one targeting the posterior Broca's area (BA44) and one targeting the precentral gyrus (BA6). In a large sample of young children (3-6 years), we demonstrate that, in contrast to the BA6-targeting tract, the microstructural asymmetry of the BA44-targeting fiber tract significantly correlates locally with different aspects of development. While the asymmetry in its anterior segment reflects age, the asymmetry in its posterior segment is associated with the children's language skills. These findings demonstrate a fine-grained structure-to-function mapping in the lateralized network and go beyond our current view of language-related human brain maturation.

Distinct neural mechanisms for action access and execution in the human brain: insights from an fMRI study.

Goal-directed actions are fundamental to human behavior, whereby inner goals are achieved through mapping action representations to motor outputs. The left premotor cortex (BA6) and the posterior portion of Broca's area (BA44) are two modulatory poles of the action system. However, how these regions support the representation-output mapping within the system is not yet understood. To address this, we conducted a finger-tapping functional magnetic resonance imaging experiment using action categories ranging from specific to general. Our study found distinct neural behaviors in BA44 and BA6 during action category processing and motor execution. During access of action categories, activity in a posterior portion of BA44 (pBA44) decreased linearly as action categories became less specific. Conversely, during motor execution, activity in BA6 increased linearly with less specific categories. These findings highlight the differential roles of pBA44 and BA6 in action processing. We suggest that pBA44 facilitates access to action categories by utilizing motor information from the behavioral context while the premotor cortex integrates motor information to execute the selected action. This finding enhances our understanding of the interplay between prefrontal cortical regions and premotor cortex in mapping action representation to motor execution and, more in general, of the cortical mechanisms underlying human behavior.

Individual differences in auditory perception predict learning of non-adjacent tone sequences in 3-year-olds.

Auditory processing of speech and non-speech stimuli oftentimes involves the analysis and acquisition of non-adjacent sound patterns. Previous studies using speech material have demonstrated (i) children's early emerging ability to extract non-adjacent dependencies (NADs) and (ii) a relation between basic auditory perception and this ability. Yet, it is currently unclear whether children show similar sensitivities and similar perceptual influences for NADs in the non-linguistic domain. We conducted an event-related potential study with 3-year-old children using a sine-tone-based oddball task, which simultaneously tested for NAD learning and auditory perception by means of varying sound intensity. Standard stimuli were A × B sine-tone sequences, in which specific A elements predicted specific B elements after variable × elements. NAD deviants violated the dependency between A and B and intensity deviants were reduced in amplitude. Both elicited similar frontally distributed positivities, suggesting successful deviant detection. Crucially, there was a predictive relationship between the amplitude of the sound intensity discrimination effect and the amplitude of the NAD learning effect. These results are taken as evidence that NAD learning in the non-linguistic domain is functional in 3-year-olds and that basic auditory processes are related to the learning of higher-order auditory regularities also outside the linguistic domain.

Characterizing directional dynamics of semantic prediction based on inter-regional temporal generalization.

The event-related potential/field component N400(m) has been widely used as a neural index for semantic prediction. It has long been hypothesized that feedback information from inferior frontal areas plays a critical role in generating the N400. However, due to limitations in causal connectivity estimation, direct testing of this hypothesis has remained difficult. Here, magnetoencephalography (MEG) data was obtained during a classic N400 paradigm where the semantic predictability of a fixed target noun was manipulated in simple German sentences. To estimate causality, we implemented a novel approach based on machine learning and temporal generalization to estimate the effect of inferior frontal gyrus (IFG) on temporal areas. In this method, a support vector machine (SVM) classifier is trained on each time point of the neural activity in IFG to classify less predicted (LP) and highly predicted (HP) nouns and then tested on all time points of superior/middle temporal sub-regions activity (and vice versa, to establish spatio-temporal evidence for or against causality). The decoding accuracy was significantly above chance level when the classifier was trained on IFG activity and tested on future activity in superior and middle temporal gyrus (STG/MTG). The results present new evidence for a model predictive speech comprehension where predictive IFG activity is fed back to shape subsequent activity in STG/MTG, implying a feedback mechanism in N400 generation. In combination with the also observed strong feedforward effect from left STG/MTG to IFG, our findings provide evidence of dynamic feedback and feedforward influences between IFG and temporal areas during N400 generation.

White matter plasticity during second language learning within and across hemispheres.

Adult second language (L2) learning is a challenging enterprise inducing neuroplastic changes in the human brain. However, it remains unclear how the structural language connectome and its subnetworks change during adult L2 learning. The current study investigated longitudinal changes in white matter (WM) language networks in each hemisphere, as well as their interconnection, in a large group of Arabic-speaking adults who learned German intensively for 6 mo. We found a significant increase in WM-connectivity within bilateral temporal-parietal semantic and phonological subnetworks and right temporal-frontal pathways mainly in the second half of the learning period. At the same time, WM-connectivity between the two hemispheres decreased significantly. Crucially, these changes in WM-connectivity are correlated with L2 performance. The observed changes in subnetworks of the two hemispheres suggest a network reconfiguration due to lexical learning. The reduced interhemispheric connectivity may indicate a key role of the corpus callosum in L2 learning by reducing the inhibition of the language-dominant left hemisphere. Our study highlights the dynamic changes within and across hemispheres in adult language-related networks driven by L2 learning.

Cognitive and sensory expectations independently shape musical expectancy and pleasure.

Expectation is crucial for our enjoyment of music, yet the underlying generative mechanisms remain unclear. While sensory models derive predictions based on local acoustic information in the auditory signal, cognitive models assume abstract knowledge of music structure acquired over the long term. To evaluate these two contrasting mechanisms, we compared simulations from four computational models of musical expectancy against subjective expectancy and pleasantness ratings of over 1000 chords sampled from 739 US Billboard pop songs. Bayesian model comparison revealed that listeners' expectancy and pleasantness ratings were predicted by the independent, non-overlapping, contributions of cognitive and sensory expectations. Furthermore, cognitive expectations explained over twice the variance in listeners' perceived surprise compared to sensory expectations, suggesting a larger relative importance of long-term representations of music structure over short-term sensory-acoustic information in musical expectancy. Our results thus emphasize the distinct, albeit complementary, roles of cognitive and sensory expectations in shaping musical pleasure, and suggest that this expectancy-driven mechanism depends on musical information represented at different levels of abstraction along the neural hierarchy. This article is part of the theme issue 'Art, aesthetics and predictive processing: theoretical and empirical perspectives'.

Causal evidence for a coordinated temporal interplay within the language network.

Recent neurobiological models on language suggest that auditory sentence comprehension is supported by a coordinated temporal interplay within a left-dominant brain network, including the posterior inferior frontal gyrus (pIFG), posterior superior temporal gyrus and sulcus (pSTG/STS), and angular gyrus (AG). Here, we probed the timing and causal relevance of the interplay between these regions by means of concurrent transcranial magnetic stimulation and electroencephalography (TMS-EEG). Our TMS-EEG experiments reveal region- and time-specific causal evidence for a bidirectional information flow from left pSTG/STS to left pIFG and back during auditory sentence processing. Adapting a condition-and-perturb approach, our findings further suggest that the left pSTG/STS can be supported by the left AG in a state-dependent manner.

Chimpanzees show the capacity to communicate about concomitant daily life events.

One universal feature of human language is its versatility in communicating about juxtapositions of everyday events. Versatile combinatorial systems of communication can be selected for if (a) several vocal units are flexibly combined into numerous and long vocal sequences and (b) vocal sequences relate to numerous daily life events. We propose (b) is more likely during simultaneous or serial (concomitant) events than single events. We analyzed 9,391 vocal utterances across the repertoire of wild chimpanzees and their events of production. Chimpanzees used vocal sequences across a range of daily life events and twice as often during concomitant than single events. Also, utterance diversity correlated positively with event diversity. Our results show the potential of chimpanzee vocal sequences to convey combined information about numerous daily life events, a step from which generalized combinatoriality could have evolved.

Electrophysiological correlates of basic semantic composition in people with aphasia.

The neuroanatomical correlates of basic semantic composition have been investigated in previous neuroimaging and lesion studies, but research on the electrophysiology of the involved processes is scarce. A large literature on sentence-level event-related potentials (ERPs) during semantic processing has identified at least two relevant components - the N400 and the P600. Other studies demonstrated that these components are reduced and/or delayed in people with aphasia (PWA). However, it remains to be shown if these findings generalize beyond the sentence level. Specifically, it is an open question if an alteration in ERP responses in PWA can also be observed during basic semantic composition, providing a potential future diagnostic tool. The present study aimed to elucidate the electrophysiological dynamics of basic semantic composition in a group of post-stroke PWA. We included 20 PWA and 20 age-matched controls (mean age 58 years) and measured ERP responses while they performed a plausibility judgment task on two-word phrases that were either meaningful ("anxious horse"), anomalous ("anxious wood") or had the noun replaced by a pseudoword ("anxious gufel"). The N400 effect for anomalous versus meaningful phrases was similar in both groups. In contrast, unlike the control group, PWA did not show an N400 effect between pseudoword and meaningful phrases. Moreover, both groups exhibited a parietal P600 effect towards pseudoword phrases, while PWA showed an additional P600 over frontal electrodes. Finally, PWA showed an inverse correlation between the magnitude of the N400 and P600 effects: PWA exhibiting no or even reversed N400 effects towards anomalous and pseudoword phrases showed a stronger P600 effect. These results may reflect a compensatory mechanism which allows PWA to arrive at the correct interpretation of the phrase. When compositional processing capacities are impaired in the early N400 time-window, PWA may make use of a more elaborate re-analysis process reflected in the P600.

Cleaning up the Brickyard: How Theory and Methodology Shape Experiments in Cognitive Neuroscience of Language.

The capacity for language is a defining property of our species, yet despite decades of research, evidence on its neural basis is still mixed and a generalized consensus is difficult to achieve. We suggest that this is partly caused by researchers defining "language" in different ways, with focus on a wide range of phenomena, properties, and levels of investigation. Accordingly, there is very little agreement among cognitive neuroscientists of language on the operationalization of fundamental concepts to be investigated in neuroscientific experiments. Here, we review chains of derivation in the cognitive neuroscience of language, focusing on how the hypothesis under consideration is defined by a combination of theoretical and methodological assumptions. We first attempt to disentangle the complex relationship between linguistics, psychology, and neuroscience in the field. Next, we focus on how conclusions that can be drawn from any experiment are inherently constrained by auxiliary assumptions, both theoretical and methodological, on which the validity of conclusions drawn rests. These issues are discussed in the context of classical experimental manipulations as well as study designs that employ novel approaches such as naturalistic stimuli and computational modeling. We conclude by proposing that a highly interdisciplinary field such as the cognitive neuroscience of language requires researchers to form explicit statements concerning the theoretical definitions, methodological choices, and other constraining factors involved in their work.

Morphological evolution of language-relevant brain areas.

Human language is supported by a cortical network involving Broca's area, which comprises Brodmann Areas 44 and 45 (BA44 and BA45). While cytoarchitectonic homolog areas have been identified in nonhuman primates, it remains unknown how these regions evolved to support human language. Here, we use histological data and advanced cortical registration methods to precisely compare the morphology of BA44 and BA45 in humans and chimpanzees. We found a general expansion of Broca's areas in humans, with the left BA44 enlarging the most, growing anteriorly into a region known to process syntax. Together with recent functional and receptorarchitectural studies, our findings support the conclusion that BA44 evolved from an action-related region to a bipartite system, with a posterior portion supporting action and an anterior portion supporting syntactic processes. Our findings add novel insights to the longstanding debate on the relationship between language and action, and the evolution of Broca's area.

Evolutionary neuroanatomical expansion of Broca's region serving a human-specific function.

The question concerning the evolution of language is directly linked to the debate on whether language and action are dependent or not and to what extent Broca's region serves as a common neural basis. The debate resulted in two opposing views, one arguing for and one against the dependence of language and action mainly based on neuroscientific data. This article presents an evolutionary neuroanatomical framework which may offer a solution to this dispute. It is proposed that in humans, Broca's region houses language and action independently in spatially separated subregions. This became possible due to an evolutionary expansion of Broca's region in the human brain, which was not paralleled by a similar expansion in the chimpanzee's brain, providing additional space needed for the neural representation of language in humans.

Exploring the neurobiology of Merge at a basic level: insights from a novel artificial grammar paradigm.

Introduction: Human language allows us to generate an infinite number of linguistic expressions. It's proposed that this competence is based on a binary syntactic operation, Merge, combining two elements to form a new constituent. An increasing number of recent studies have shifted from complex syntactic structures to two-word constructions to investigate the neural representation of this operation at the most basic level. Methods: This fMRI study aimed to develop a highly flexible artificial grammar paradigm for testing the neurobiology of human syntax at a basic level. During scanning, participants had to apply abstract syntactic rules to assess whether a given two-word artificial phrase could be further merged with a third word. To control for lower-level template-matching and working memory strategies, an additional non-mergeable word-list task was set up. Results: Behavioral data indicated that participants complied with the experiment. Whole brain and region of interest (ROI) analyses were performed under the contrast of "structure > word-list." Whole brain analysis confirmed significant involvement of the posterior inferior frontal gyrus [pIFG, corresponding to Brodmann area (BA) 44]. Furthermore, both the signal intensity in Broca's area and the behavioral performance showed significant correlations with natural language performance in the same participants. ROI analysis within the language atlas and anatomically defined Broca's area revealed that only the pIFG was reliably activated. Discussion: Taken together, these results support the notion that Broca's area, particularly BA 44, works as a combinatorial engine where words are merged together according to syntactic information. Furthermore, this study suggests that the present artificial grammar may serve as promising material for investigating the neurobiological basis of syntax, fostering future cross-species studies.

Uncovering the Morphological Evolution of Language-Relevant Brain Areas.

Human language is supported by a cortical network involving Broca's area which comprises Brodmann Areas 44 and 45 (BA44, BA45). While cytoarchitectonic homolog areas have been identified in nonhuman primates, it remains unknown how these regions evolved to support human language. Here, we use histological data and advanced cortical registration methods to precisely compare the morphology of BA44 and 45 between humans and chimpanzees. We found a general expansion of Broca's areas in humans, with the left BA44 enlarging the most, growing anteriorly into a region known to process syntax. Together with recent functional studies, our findings show that BA44 evolved from a purely action-related region to a more expanded region in humans, with a posterior portion supporting action and an anterior portion supporting syntactic processes. Furthermore, our findings provide a solution for the longstanding debate concerning the structural and functional evolution of Broca's area and its role in action and language.

Native language differences in the structural connectome of the human brain.

Is the neuroanatomy of the language structural connectome modulated by the life-long experience of speaking a specific language? The current study compared the brain white matter connections of the language and speech production network in a large cohort of 94 native speakers of two very different languages: an Indo-European morphosyntactically complex language (German) and a Semitic root-based language (Arabic). Using high-resolution diffusion-weighted MRI and tractography-based network statistics of the language connectome, we demonstrated that German native speakers exhibited stronger connectivity in an intra-hemispheric frontal to parietal/temporal dorsal language network, known to be associated with complex syntax processing. In comparison, Arabic native speakers showed stronger connectivity in the connections between semantic language regions, including the left temporo-parietal network, and stronger inter-hemispheric connections via the posterior corpus callosum connecting bilateral superior temporal and inferior parietal regions. The current study suggests that the structural language connectome develops and is modulated by environmental factors such as the characteristic processing demands of the native language.

Maturation of consonant perception, but not vowel perception, predicts lexical skills at 12 months.

Consonants and vowels differentially contribute to lexical acquisition. From 8 months on, infants' preferential reliance on consonants has been shown to predict their lexical outcome. Here, the predictive value of German-learning infants' (n = 58, 29 girls, 29 boys) trajectories of consonant and vowel perception, indicated by the electrophysiological mismatch response, across 2, 6, and 10 months for later lexical acquisition was studied. The consonant-perception trajectory from 2 to 6 months (ß = -2.95) and 6 to 10 months (ß = -.91), but not the vowel-perception trajectory, significantly predicted receptive vocabulary at 12 months. These results reveal an earlier predictive value of consonant perception for word learning than previously found, and a particular role of the longitudinal maturation of this skill in lexical acquisition.

White matter brain structure predicts language performance and learning success.

Individual differences in the ability to process language have long been discussed. Much of the neural basis of these, however, is yet unknown. Here we investigated the relationship between long-range white matter connectivity of the brain, as revealed by diffusion tractography, and the ability to process syntactically complex sentences in the participants' native language as well as the improvement thereof by multiday training. We identified specific network motifs by singular value decomposition that indeed related white matter structural connectivity to individual language processing performance. First, for two such motifs, one in the left and one in the right hemisphere, their individual prevalence significantly predicted the individual language performance, suggesting an anatomical predisposition for the individual ability to process syntactically complex sentences. Both motifs comprise a number of cortical regions, but seem to be dominated by areas known for the involvement in working memory rather than the classical language network itself. Second, we identified another left hemispheric network motif, whose change of prevalence over the training period significantly correlated with the individual change in performance, thus reflecting training induced white matter plasticity. This motif comprises diverse cortical areas including regions known for their involvement in language processing, working memory and motor functions. The present findings suggest that individual differences in language processing and learning can be explained, in part, by individual differences in the brain's white matter structure. Brain structure may be a crucial factor to be considered when discussing variations in human cognitive performance, more generally.

The role of left temporo-parietal and inferior frontal cortex in comprehending syntactically complex sentences: A brain stimulation study.

BACKGROUND AND OBJECTIVES: Syntactic competence relies on a left-lateralized network converging on hubs in inferior-frontal and posterior-temporal cortices. We address the question whether anodal transcranial direct current stimulation (a-tDCS) over these hubs can modulate comprehension of sentences, whose syntactic complexity systematically varied along the factors embedding depths and canonicity. Semantic content and length of the sentences were kept identical and forced choice picture matching was required after the full sentence had been presented. METHODS: We used a single-blind, within-subject, sham-controlled design, applying a-tDCS targeting left posterior tempo-parietal (TP) and left inferior frontal cortex (FC). Stimulation sites were determined by individual neuro-navigation. 20 participants were included of whom 19 entered the analysis. Results were analysed using (generalized) mixed models. In a pilot-experiment in another group of 20 participants we validated the manipulation of syntactic complexity by the two factors embedding depth and argument-order. RESULTS: Reaction times increased and accuracy decreased with higher embedding depth and non-canonical argument order in both experiments. Notably a-tDCS over TP enhanced sentence-to-picture matching, while FC-stimulation showed no consistent effect. Moreover, the analysis disclosed a session effect, indicating improvements of task performance especially regarding speed. CONCLUSIONS: We conclude that the posterior 'hub' of the neuronal network affording syntactic analysis represents a 'bottleneck', likely due to working-memory capacity and the challenges of mapping semantic to syntactic information allowing for role assignment. While this does not challenge the role of left inferior-frontal cortex for syntax processing and novel-grammar learning, the application of highly established syntactic rules during sentence comprehension may be considered optimized, thus not augmentable by a-tDCS in the uncompromised network. SIGNIFICANCE STATEMENT: Anodal transcranial direct current stimulation (a-tDCS) over left temporo-parietal cortex enhances comprehension of complex sentences in uncompromised young speakers. Since a-tDCS over left frontal cortex did not elicit any change, the 'bottleneck' for the understanding of complex sentences seems to be the posterior, temporo-parietal rather than the anterior inferior-frontal 'hub' of language processing. Regarding the attested role of inferior-frontal cortex in syntax processing, we suggest that its function is optimized in competent young speakers, preventing further enhancement by (facilitatory) tDCS. Results shed light on the functional anatomy of syntax processing during sentence comprehension; moreover, they open perspectives for research in the lesioned language network of people with syntactic deficits due to aphasia.

Children's syntax is supported by the maturation of BA44 at 4 years, but of the posterior STS at 3 years of age.

Within the first years of life, children learn major aspects of their native language. However, the ability to process complex sentence structures, a core faculty in human language called syntax, emerges only slowly. A milestone in syntax acquisition is reached around the age of 4 years, when children learn a variety of syntactic concepts. Here, we ask which maturational changes in the child's brain underlie the emergence of syntactically complex sentence processing around this critical age. We relate markers of cortical brain maturation to 3- and 4-year-olds' sentence processing in contrast to other language abilities. Our results show that distinct cortical brain areas support sentence processing in the two age groups. Sentence production abilities at 3 years were associated with increased surface area in the most posterior part of the left superior temporal sulcus, whereas 4-year-olds showed an association with cortical thickness in the left posterior part of Broca's area, i.e. BA44. The present findings suggest that sentence processing abilities rely on the maturation of distinct cortical regions in 3- compared to 4-year-olds. The observed shift to more mature regions involved in processing syntactically complex sentences may underlie behavioral milestones in syntax acquisition at around 4 years.

Brain structure and function: a multidisciplinary pipeline to study hominoid brain evolution.

To decipher the evolution of the hominoid brain and its functions, it is essential to conduct comparative studies in primates, including our closest living relatives. However, strong ethical concerns preclude in vivo neuroimaging of great apes. We propose a responsible and multidisciplinary alternative approach that links behavior to brain anatomy in non-human primates from diverse ecological backgrounds. The brains of primates observed in the wild or in captivity are extracted and fixed shortly after natural death, and then studied using advanced MRI neuroimaging and histology to reveal macro- and microstructures. By linking detailed neuroanatomy with observed behavior within and across primate species, our approach provides new perspectives on brain evolution. Combined with endocranial brain imprints extracted from computed tomographic scans of the skulls these data provide a framework for decoding evolutionary changes in hominin fossils. This approach is poised to become a key resource for investigating the evolution and functional differentiation of hominoid brains.