Detailed mapping of the complex fiber structure and white matter pathways of the chimpanzee brain.

Long-standing questions about human brain evolution may only be resolved through comparisons with close living evolutionary relatives, such as chimpanzees. This applies in particular to structural white matter (WM) connectivity, which continuously expanded throughout evolution. However, due to legal restrictions on chimpanzee research, neuroscience research currently relies largely on data with limited detail or on comparisons with evolutionarily distant monkeys. Here, we present a detailed magnetic resonance imaging resource to study structural WM connectivity in the chimpanzee. This open-access resource contains (1) WM reconstructions of a postmortem chimpanzee brain, using the highest-quality diffusion magnetic resonance imaging data yet acquired from great apes; (2) an optimized and validated method for high-quality fiber orientation reconstructions; and (3) major fiber tract segmentations for cross-species morphological comparisons. This dataset enabled us to identify phylogenetically relevant details of the chimpanzee connectome, and we anticipate that it will substantially contribute to understanding human brain evolution.

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.

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.

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.

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.

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.

Maturational Indices of the Cognitive Control Network Are Associated with Inhibitory Control in Early Childhood.

Goal-directed behavior crucially relies on our capacity to suppress impulses and predominant behavioral responses. This ability, called inhibitory control, emerges in early childhood with marked improvements between 3 and 4 years. Here, we ask which brain structures are related to the emergence of this critical ability. Using a multimodal approach, we relate the pronounced behavioral improvements in different facets of 3- and 4-year-olds' (N = 37, 20 female) inhibitory control to structural indices of maturation in the developing brain assessed with MRI. Our results show that cortical and subcortical structure of core regions in the adult cognitive control network, including the PFC, thalamus, and the inferior parietal cortices, is associated with early inhibitory functioning in preschool children. Probabilistic tractography revealed an association of frontoparietal (i.e., the superior longitudinal fascicle) and thalamocortical connections with early inhibitory control. Notably, these associations to brain structure were distinct for different facets of early inhibitory control, often referred to as motivational ("hot") and cognitive ("cold") inhibitory control. Our findings thus reveal the structural brain networks and connectivity related to the emergence of this core faculty of human cognition.SIGNIFICANCE STATEMENT The capacity to suppress impulses and behavioral responses is crucial for goal-directed behavior. This ability, called inhibitory control, develops between the ages of 3 and 4 years. The factors behind this developmental milestone have been debated intensely for decades; however, the brain structure that underlies the emergence of inhibitory control in early childhood is largely unknown. Here, we relate the pronounced behavioral improvements in inhibitory control between 3 and 4 years with structural brain markers of gray matter and white matter maturation. Using a multimodal approach that combines analyses of cortical surface structure, subcortical structures, and white matter connectivity, our results reveal the structural brain networks and connectivity related to this core faculty of human cognition.

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.

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.

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.

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.

Two systems for thinking about others' thoughts in the developing brain.

Human social interaction crucially relies on the ability to infer what other people think. Referred to as Theory of Mind (ToM), this ability has long been argued to emerge around 4 y of age when children start passing traditional verbal ToM tasks. This developmental dogma has recently been questioned by nonverbal ToM tasks passed by infants younger than 2 y of age. How do young children solve these tests, and what is their relation to the later-developing verbal ToM reasoning? Are there two different systems for nonverbal and verbal ToM, and when is the developmental onset of mature adult ToM? To address these questions, we related markers of cortical brain structure (i.e., cortical thickness and surface area) of 3- and 4-y-old children to their performance in novel nonverbal and traditional verbal TM tasks. We showed that verbal ToM reasoning was supported by cortical surface area and thickness of the precuneus and temporoparietal junction, classically involved in ToM in adults. Nonverbal ToM reasoning, in contrast, was supported by the cortical structure of a distinct and independent neural network including the supramarginal gyrus also involved in emotional and visual perspective taking, action observation, and social attention or encoding biases. This neural dissociation suggests two systems for reasoning about others' minds-mature verbal ToM that emerges around 4 y of age, whereas nonverbal ToM tasks rely on different earlier-developing possibly social-cognitive processes.

Bridging the Gap Between Neurons and Cognition Through Assemblies of Neurons.

During recent decades, our understanding of the brain has advanced dramatically at both the cellular and molecular levels and at the cognitive neurofunctional level; however, a huge gap remains between the microlevel of physiology and the macrolevel of cognition. We propose that computational models based on assemblies of neurons can serve as a blueprint for bridging these two scales. We discuss recently developed computational models of assemblies that have been demonstrated to mediate higher cognitive functions such as the processing of simple sentences, to be realistically realizable by neural activity, and to possess general computational power.

Associated functional network development and language abilities in children.

During childhood, the brain is gradually converging to the efficient functional architecture observed in adults. How the brain's functional architecture evolves with age, particularly in young children, is however, not well understood. We examined the functional connectivity of the core language regions, in association with cortical growth and language abilities, in 175 young children in the age range of 4 to 9 years. We analyzed the brain's developmental changes using resting-state functional and T1-weighted structural magnetic resonance imaging data. The results showed increased functional connectivity strength with age between the pars triangularis of the left inferior frontal gyrus and left temporoparietal regions (cohen's d = 0.54, CI: 0.24 - 0.84), associated with children's language abilities. Stronger functional connectivity between bilateral prefrontal and temporoparietal regions was associated with better language abilities regardless of age. In addition, the stronger functional connectivity between the left inferior frontal and temporoparietal regions was associated with larger surface area and thinner cortical thickness in these regions, which in turn was associated with superior language abilities. Thus, using functional and structural brain indices, coupled with behavioral measures, we elucidate the association of functional language network development, language ability, and cortical growth, thereby adding to our understanding of the neural basis of language acquisition in young children.

Hierarchical syntactic processing is beyond mere associating: Functional magnetic resonance imaging evidence from a novel artificial grammar.

Grammar is central to any natural language. In the past decades, the artificial grammar of the An Bn type in which a pair of associated elements can be nested in the other pair was considered as a desirable model to mimic human language syntax without semantic interference. However, such a grammar relies on mere associating mechanisms, thus insufficient to reflect the hierarchical nature of human syntax. Here, we test how the brain imposes syntactic hierarchies according to the category relations on linearized sequences by designing a novel artificial "Hierarchical syntactic structure-building Grammar" (HG), and compare this to the An Bn grammar as a "Nested associating Grammar" (NG) based on multilevel associations. Thirty-six healthy German native speakers were randomly assigned to one of the two grammars. Both groups performed a grammaticality judgment task on auditorily presented word sequences generated by the corresponding grammar in the scanner after a successful explicit behavioral learning session. Compared to the NG group, we found that the HG group showed a (a) significantly higher involvement of Brodmann area (BA) 44 in Broca's area and the posterior superior temporal gyrus (pSTG); and (b) qualitatively distinct connectivity between the two regions. Thus, the present study demonstrates that the build-up process of syntactic hierarchies on the basis of category relations critically relies on a distinctive left-hemispheric syntactic network involving BA 44 and pSTG. This indicates that our novel artificial grammar can constitute a suitable experimental tool to investigate syntax-specific processes in the human brain.

Intonation processing increases task-specific fronto-temporal connectivity in tonal language speakers.

Language comprehension depends on tight functional interactions between distributed brain regions. While these interactions are established for semantic and syntactic processes, the functional network of speech intonation - the linguistic variation of pitch - has been scarcely defined. Particularly little is known about intonation in tonal languages, in which pitch not only serves intonation but also expresses meaning via lexical tones. The present study used psychophysiological interaction analyses of functional magnetic resonance imaging data to characterise the neural networks underlying intonation and tone processing in native Mandarin Chinese speakers. Participants categorised either intonation or tone of monosyllabic Mandarin words that gradually varied between statement and question and between Tone 2 and Tone 4. Intonation processing induced bilateral fronto-temporal activity and increased functional connectivity between left inferior frontal gyrus and bilateral temporal regions, likely linking auditory perception and labelling of intonation categories in a phonological network. Tone processing induced bilateral temporal activity, associated with the auditory representation of tonal (phonemic) categories. Together, the present data demonstrate the breadth of the functional intonation network in a tonal language including higher-level phonological processes in addition to auditory representations common to both intonation and tone.

Functional neuroanatomy of language without speech: An ALE meta-analysis of sign language.

Sign language (SL) conveys linguistic information using gestures instead of sounds. Here, we apply a meta-analytic estimation approach to neuroimaging studies (N = 23; subjects = 316) and ask whether SL comprehension in deaf signers relies on the same primarily left-hemispheric cortical network implicated in spoken and written language (SWL) comprehension in hearing speakers. We show that: (a) SL recruits bilateral fronto-temporo-occipital regions with strong left-lateralization in the posterior inferior frontal gyrus known as Broca's area, mirroring functional asymmetries observed for SWL. (b) Within this SL network, Broca's area constitutes a hub which attributes abstract linguistic information to gestures. (c) SL-specific voxels in Broca's area are also crucially involved in SWL, as confirmed by meta-analytic connectivity modeling using an independent large-scale neuroimaging database. This strongly suggests that the human brain evolved a lateralized language network with a supramodal hub in Broca's area which computes linguistic information independent of speech.

Functional brain plasticity during L1 training on complex sentences: Changes in gamma-band oscillatory activity.

The adult human brain remains plastic even after puberty. However, whether first language (L1) training in adults can alter the language network is yet largely unknown. Thus, we conducted a longitudinal training experiment on syntactically complex German sentence comprehension. Sentence complexity was varied by the depth of the center embedded relative clauses (i.e., single or double embedded). Comprehension was tested after each sentence with a question on the thematic role assignment. Thirty adult, native German speakers were recruited for 4 days of training. Magnetoencephalography (MEG) data were recorded and subjected to spectral power analysis covering the classical frequency bands (i.e., theta, alpha, beta, low gamma, and gamma). Normalized spectral power, time-locked to the final closure of the relative clause, was subjected to a two-factor analysis ("sentence complexity" and "training days"). Results showed that for the more complex sentences, the interaction of sentence complexity and training days was observed in Brodmann area 44 (BA 44) as a decrease of gamma power with training. Moreover, in the gamma band (55-95 Hz) functional connectivity between BA 44 and other brain regions such as the inferior frontal sulcus and the inferior parietal cortex were correlated with behavioral performance increase due to training. These results show that even for native speakers, complex L1 sentence training improves language performance and alters neural activities of the left hemispheric language network. Training strengthens the use of the dorsal processing stream with working-memory-related brain regions for syntactically complex sentences, thereby demonstrating the brain's functional plasticity for L1 training.

The ontogeny of the cortical language network.

Language-processing functions follow heterogeneous developmental trajectories. The human embryo can already distinguish vowels in utero, but grammatical complexity is usually not fully mastered until at least 7 years of age. Examining the current literature, we propose that the ontogeny of the cortical language network can be roughly subdivided into two main developmental stages. In the first stage extending over the first 3 years of life, the infant rapidly acquires bottom-up processing capacities, which are primarily implemented bilaterally in the temporal cortices. In the second stage continuing into adolescence, top-down processes emerge gradually with the increasing functional selectivity and structural connectivity of the left inferior frontal cortex.

Language and action in Broca's area: Computational differentiation and cortical segregation.

Actions have been proposed to follow hierarchical principles similar to those hypothesized for language syntax. These structural similarities are claimed to be reflected in the common involvement of certain neural populations of Broca's area, in the Inferior Frontal Gyrus (IFG). In this position paper, we follow an influential hypothesis in linguistic theory to introduce the syntactic operation Merge and the corresponding motor/conceptual interfaces. We argue that actions hierarchies do not follow the same principles ruling language syntax. We propose that hierarchy in the action domain lies in predictive processing mechanisms mapping sensory inputs and statistical regularities of action-goal relationships. At the cortical level, distinct Broca's subregions appear to support different types of computations across the two domains. We argue that anterior BA44 is a major hub for the implementation of the syntactic operation Merge. On the other hand, posterior BA44 is recruited in selecting premotor mental representations based on the information provided by contextual signals. This functional distinction is corroborated by a recent meta-analysis (Papitto, Friederici, & Zaccarella, 2020). We conclude by suggesting that action and language can meet only where the interfaces transfer abstract computations either to the external world or to the internal mental world.