Exploring the neurobiology of reading through non-invasive brain stimulation: A review

Non-invasive brain stimulation (NIBS) has gained increasing popularity as a modulatory tool for drawing causal inferences and exploring task-specific network interactions. Yet, a comprehensive synthesis of reading-related NIBS studies is still missing. We fill this gap by synthesizing the results of 78 NIBS studies investigating the causal involvement of brain regions for reading processing, and then link these results to a neurobiological model of reading. The included studies provide evidence for a functional-anatomical double dissociation for phonology versus semantics during reading-related processes within left inferior frontal and parietal areas. Additionally, the posterior parietal cortex and the anterior temporal lobe are identified as critical regions for reading-related processes. Overall, the findings provide some evidence for a dual-stream neurobiological model of reading, in which a dorsal stream (left temporo-parietal and inferior frontal areas) processes unfamiliar words and pseudowords, and a ventral stream (left occipito-temporal and inferior frontal areas, with assistance from the angular gyrus and the anterior temporal lobe) processes known words. However, individual differences in reading abilities and strategies, as well as differences in stimulation parameters, may impact the neuromodulatory effects induced by NIBS. We emphasize the need to investigate task-specific network interactions in future studies by combining NIBS with neuroimaging

Syntactic and semantic contributions of pitch accents during sentence comprehension

Syntactic, semantic, and prosodic cues all establish expectations that guide sentence comprehension. In the prosodic domain, pitch accents can assign contrastive focus and resolve a syntactically ambiguous phrase. However, can prosodic focus marking (by pitch accenting) influence the interpretation of a sentence in the presence of syntactic and semantic cues? Our auditory experiment revolved around the sentence (in German) “Yesterday the policeman arrested the thief, not the murderer”. A pitch accent on either POLICEMAN or THIEF placed one of those arguments in contrastive focus with the ellipsis structure ("the murderer”). The two contrasted arguments could contain violations: in the syntax condition, the grammatical case of the article in the ellipsis structure mismatched the focused constituent in the main clause (nominative vs. accusative). In the semantic condition, the thematic roles of the contrasted words were incongruent (typical agent vs. patient roles of “arrest”). Visual comprehension questions probed the agent/patient role of the arguments in the sentence (subject or object), followed by a button-press response. Reaction times showed that if the pitch accent marked syntactic information that mismatched the syntactic information in the ellipsis structure, responses were delayed. The direction of the semantic effect depended on the focused noun. The response patterns showed that participants were led by the syntactic information to make their syntactic judgements, despite a conflicting expectation established by prosody. The experiment shows that pitch accents establish a syntactic expectation during sentence comprehension. However, these expectations are overwritten by incoming syntactic information to yield an interpretation of the sentence

Functional specialization within the inferior parietal lobes across cognitive domains

The inferior parietal lobe (IPL) is a key neural substrate underlying diverse mental processes, from basic attention to language and social cognition, that define human interactions. Its putative domain-global role appears to tie into poorly understood differences between cognitive domains in both hemispheres. Across attentional, semantic, and social cognitive tasks, our study explored functional specialization within the IPL. The task specificity of IPL subregion activity was substantiated by distinct predictive signatures identified by multivariate pattern-learning algorithms. Moreover, the left and right IPL exerted domain-specific modulation of effective connectivity among their subregions. Task-evoked functional interactions of the anterior and posterior IPL subregions involved recruitment of distributed cortical partners. While anterior IPL subregions were engaged in strongly lateralized coupling links, both posterior subregions showed more symmetric coupling patterns across hemispheres. Our collective results shed light on how under-appreciated hemispheric specialization in the IPL supports some of the most distinctive human mental capacities

Task-dependent functional and effective connectivity during conceptual processing

Conceptual knowledge is central to cognition. Previous neuroimaging research indicates that conceptual processing involves both modality-specific perceptual-motor areas and multimodal convergence zones. For example, our previous functional magnetic resonance imaging (fMRI) study revealed that both modality-specific and multimodal regions respond to sound and action features of concepts in a task-dependent fashion (Kuhnke P, Kiefer M, Hartwigsen G. 2020b. Task-dependent recruitment of modality-specific and multimodal regions during conceptual processing. Cereb Cortex. 30:3938-3959.). However, it remains unknown whether and how modality-specific and multimodal areas interact during conceptual tasks. Here, we asked 1) whether multimodal and modality-specific areas are functionally coupled during conceptual processing, 2) whether their coupling depends on the task, 3) whether information flows top-down, bottom-up or both, and 4) whether their coupling is behaviorally relevant. We combined psychophysiological interaction analyses with dynamic causal modeling on the fMRI data of our previous study. We found that functional coupling between multimodal and modality-specific areas strongly depended on the task, involved both top-down and bottom-up information flow, and predicted conceptually guided behavior. Notably, we also found coupling between different modality-specific areas and between different multimodal areas. These results suggest that functional coupling in the conceptual system is extensive, reciprocal, task-dependent, and behaviorally relevant. We propose a new model of the conceptual system that incorporates task-dependent functional interactions between modality-specific and multimodal areas

Task-specific network interactions across key cognitive domains

Human cognition is organized in distributed networks in the brain. Although distinct specialized networks have been identified for different cognitive functions, previous work also emphasizes the overlap of key cognitive domains in higher level association areas. The majority of previous studies focused on network overlap and dissociation during resting states whereas task-related network interactions across cognitive domains remain largely unexplored. A better understanding of network overlap and dissociation during different cognitive tasks may elucidate flexible (re-)distribution of resources during human cognition. The present study addresses this issue by providing a broad characterization of large-scale network dynamics in three key cognitive domains. Combining prototypical tasks of the larger domains of attention, language, and social cognition with whole-brain multivariate activity and connectivity approaches, we provide a spatiotemporal characterization of multiple large-scale, overlapping networks that differentially interact across cognitive domains. We show that network activity and interactions increase with increased cognitive complexity across domains. Interaction patterns reveal a common core structure across domains as well as dissociable domain-specific network activity. The observed patterns of activation and deactivation of overlapping and strongly coupled networks provide insight beyond region-specific activity within a particular cognitive domain toward a network perspective approach across diverse key cognitive functions

Age-dependent contribution of domain-general networks to semantic cognition

Aging is characterized by a decline of cognitive control. In semantic cognition, this leads to the paradox that older adults usually show poorer task performance than young adults despite their greater semantic knowledge. So far, the underlying neural changes of these behavioral differences are poorly understood. In the current neuroimaging study, we investigated the interaction of domain-specific and domain-general networks during verbal semantic fluency in young and older adults. Across age groups, task processing was characterized by a strong positive integration within the multiple-demand as well as between the multiple-demand and the default mode network during semantic fluency. However, the behavioral relevance of strengthened connectivity differed between groups: While within-network functional connectivity in both networks predicted greater efficiency in semantic fluency in young adults, it was associated with slower performance in older adults. Moreover, only young adults profited from connectivity between networks for their semantic memory performance. Our results suggest that the functional coupling of usually anticorrelated networks is critical for successful task processing, independent of age, when access to semantic memory is required. Furthermore, our findings lend novel support to the notion of reduced efficiency in the aging brain due to neural dedifferentiation in semantic cognition

Differential contributions of left-hemispheric language regions to basic semantic composition

Semantic composition, the ability to combine single words to form complex meanings, is a core feature of human language. Despite growing interest in the basis of semantic composition, the neural correlates and the interaction of regions within this network remain a matter of debate. We designed a well-controlled two-word fMRI paradigm in which phrases only differed along the semantic dimension while keeping syntactic information alike. Healthy participants listened to meaningful (“fresh apple”), anomalous (“awake apple”) and pseudoword phrases (“awake gufel”) while performing an implicit and an explicit semantic task. We identified neural signatures for distinct processes during basic semantic composition. When lexical information is kept constant across conditions and the evaluation of phrasal plausibility is examined (meaningful vs. anomalous phrases), a small set of mostly left-hemispheric semantic regions, including the anterior part of the left angular gyrus, is found active. Conversely, when the load of lexical information—independently of phrasal plausibility—is varied (meaningful or anomalous vs. pseudoword phrases), conceptual combination involves a wide-spread left-hemispheric network comprising executive semantic control regions and general conceptual representation regions. Within this network, the functional coupling between the left anterior inferior frontal gyrus, the bilateral pre-supplementary motor area and the posterior angular gyrus specifically increases for meaningful phrases relative to pseudoword phrases. Stronger effects in the explicit task further suggest task-dependent neural recruitment. Overall, we provide a separation between distinct nodes of the semantic network, whose functional contributions depend on the type of compositional process under analysis