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-Dependent Recruitment of Modality-Specific and Multimodal Regions during Conceptual Processing.

Conceptual knowledge is central to cognitive abilities such as word comprehension. Previous neuroimaging evidence indicates that concepts are at least partly composed of perceptual and motor features that are represented in the same modality-specific brain regions involved in actual perception and action. However, it is unclear to what extent the retrieval of perceptual-motor features and the resulting engagement of modality-specific regions depend on the concurrent task. To address this issue, we measured brain activity in 40 young and healthy participants using functional magnetic resonance imaging, while they performed three different tasks-lexical decision, sound judgment, and action judgment-on words that independently varied in their association with sounds and actions. We found neural activation for sound and action features of concepts selectively when they were task-relevant in brain regions also activated during auditory and motor tasks, respectively, as well as in higher-level, multimodal regions which were recruited during both sound and action feature retrieval. For the first time, we show that not only modality-specific perceptual-motor areas but also multimodal regions are engaged in conceptual processing in a flexible, task-dependent fashion, responding selectively to task-relevant conceptual features.

Left posterior inferior parietal cortex causally supports the retrieval of action knowledge.

Conceptual knowledge is central to human cognition. The left posterior inferior parietal lobe (pIPL) is implicated by neuroimaging studies as a multimodal hub representing conceptual knowledge related to various perceptual-motor modalities. However, the causal role of left pIPL in conceptual processing remains unclear. Here, we transiently disrupted left pIPL function with transcranial magnetic stimulation (TMS) to probe its causal relevance for the retrieval of action and sound knowledge. We compared effective TMS over left pIPL with sham TMS, while healthy participants performed three different tasks-lexical decision, action judgment, and sound judgment-on words with a high or low association to actions and sounds. We found that pIPL-TMS selectively impaired action judgments on low sound-low action words. For the first time, we directly related computational simulations of the TMS-induced electrical field to behavioral performance, which revealed that stronger stimulation of left pIPL is associated with worse performance for action but not sound judgments. These results indicate that left pIPL causally supports conceptual processing when action knowledge is task-relevant and cannot be compensated by sound knowledge. Our findings suggest that left pIPL is specialized for the retrieval of action knowledge, challenging the view of left pIPL as a multimodal conceptual hub.

Transcranial direct current stimulation (tDCS) facilitates verb learning by altering effective connectivity in the healthy brain.

Recent studies have shown that the left inferior frontal gyrus (IFG) plays a key role in language learning. Facilitatory stimulation over this region by means of anodal transcranial direct current stimulation (tDCS) can modulate linguistic abilities in healthy individuals and improve language performance in patients with post-stroke aphasia. Neuroimaging studies in healthy participants have suggested that anodal tDCS decreases task-related activity at the stimulated site when applied during different language tasks, and changes resting-state connectivity in a larger network of areas associated with language processing. However, to date, the neural correlates of the potential beneficial effects of tDCS on verb learning remain unclear. The current study investigated how anodal tDCS during verb learning modulates task-related activity and effective connectivity in the healthy language network. To this end, we combined a verb learning paradigm during functional neuroimaging with simultaneous tDCS over the left IFG in healthy human volunteers. We found that, relative to sham stimulation, anodal tDCS significantly decreased task-related activity at the stimulated left IFG and in the right homologue. Effective connectivity analysis showed that anodal tDCS significantly decreased task-related functional coupling between the left IFG and the right insula. Importantly, the individual decrease in connectivity was significantly correlated with the individual behavioural improvement during anodal tDCS. These results demonstrate, for the first time, that the behavioural improvements induced by anodal tDCS might be related to an overall decrease in processing effort both with respect to task-related activity and effective connectivity within a large language network.

Perturbation of left posterior prefrontal cortex modulates top-down processing in sentence comprehension.

Communication is an inferential process. In particular, language comprehension constantly requires top-down efforts, as often multiple interpretations are compatible with a given sentence. To assess top-down processing in the language domain, our experiment employed ambiguous sentences that allow for multiple interpretations (e.g., The client sued the murderer with the corrupt lawyer., where the corrupt lawyer could either belong to The client or the murderer). Interpretation thus depended on whether participants chunk the words of the sentence into short or long syntactic phrases. In principle, bottom-up acoustic information (i.e., the presence or absence of an intonational phrase boundary at the offset of the murderer) indicates one of the two possible interpretations. Yet, acoustic information often indicates interpretations that require words to be chunked into overly long phrases that would overburden working memory. Processing is biased against these demands, reflected in a top-down preference to chunk words into short rather than long phrases. It is often proposed, but also hotly debated, that the ability to chunk words into short phrases is subserved by the left inferior frontal gyrus (IFG). Here, we employed focal repetitive transcranial magnetic stimulation to perturb the left IFG, which resulted in a further decrease of the aptitude to tolerate long phrases, indicating the inability of the left IFG to assist the chunking of words into phrases. In contrast, the processing of auditory information was not affected. Our findings support a causal top-down role of the left inferior frontal gyrus in the chunking of words into phrases.

Left posterior inferior frontal gyrus is causally involved in reordering during sentence processing.

Storage and reordering of incoming information are two core processes required for successful sentence comprehension. Storage is necessary whenever the verb and its arguments (i.e., subject and object) are separated over a long distance, while reordering is necessary whenever the argument order is atypical (e.g., object-first order in German, where subject-first order is typical). Previous neuroimaging work has associated storage with the left planum temporale (PT), and reordering with the left posterior inferior frontal gyrus (pIFG). Here, we tested the causal role of the PT and pIFG in storage and reordering using repetitive transcranial magnetic stimulation (rTMS). We applied either effective rTMS over PT or pIFG, or sham rTMS, while subjects listened to sentences that independently varied storage demands (short vs. long argument-verb distance) and reordering demands (subject- vs. object-first argument order). We found that rTMS over pIFG, but not PT, selectively affected reordering during the processing of sentences with a long argument-verb distance. Specifically, relative to sham rTMS, rTMS over pIFG significantly increased the performance difference between object- and subject-first long-distance sentences. These results demonstrate a causal involvement of left pIFG in reordering during sentence comprehension and thus contribute to a better understanding of the role of the pIFG in language processing.

Conceptual representations in the default, control and attention networks are task-dependent and cross-modal.

Conceptual knowledge is central to human cognition. Neuroimaging studies suggest that conceptual processing involves modality-specific and multimodal brain regions in a task-dependent fashion. However, it remains unclear (1) to what extent conceptual feature representations are also modulated by the task, (2) whether conceptual representations in multimodal regions are indeed cross-modal, and (3) how the conceptual system relates to the large-scale functional brain networks. To address these issues, we conducted multivariate pattern analyses on fMRI data. 40 participants performed three tasks-lexical decision, sound judgment, and action judgment-on written words. We found that (1) conceptual feature representations are strongly modulated by the task, (2) conceptual representations in several multimodal regions are cross-modal, and (3) conceptual feature retrieval involves the default, frontoparietal control, and dorsal attention networks. Conceptual representations in these large-scale networks are task-dependent and cross-modal. Our findings support theories that assume conceptual processing to rely on a flexible, multi-level architecture.

Disrupted network interactions serve as a neural marker of dyslexia.

Dyslexia, a frequent learning disorder, is characterized by severe impairments in reading and writing and hypoactivation in reading regions in the left hemisphere. Despite decades of research, it remains unclear to date if observed behavioural deficits are caused by aberrant network interactions during reading and whether differences in functional activation and connectivity are directly related to reading performance. Here we provide a comprehensive characterization of reading-related brain connectivity in adults with and without dyslexia. We find disrupted functional coupling between hypoactive reading regions, especially between the left temporo-parietal and occipito-temporal cortices, and an extensive functional disruption of the right cerebellum in adults with dyslexia. Network analyses suggest that individuals with dyslexia process written stimuli via a dorsal decoding route and show stronger reading-related interaction with the right cerebellum. Moreover, increased connectivity within networks is linked to worse reading performance in dyslexia. Collectively, our results provide strong evidence for aberrant task-related connectivity as a neural marker for dyslexia that directly impacts behavioural performance. The observed differences in activation and connectivity suggest that one effective way to alleviate reading problems in dyslexia is through modulating interactions within the reading network with neurostimulation methods.

Meta-analytic evidence for a novel hierarchical model of conceptual processing.

Conceptual knowledge plays a pivotal role in human cognition. Grounded cognition theories propose that concepts consist of perceptual-motor features represented in modality-specific perceptual-motor cortices. However, it is unclear whether conceptual processing consistently engages modality-specific areas. Here, we performed an activation likelihood estimation (ALE) meta-analysis across 212 neuroimaging experiments on conceptual processing related to 7 perceptual-motor modalities (action, sound, visual shape, motion, color, olfaction-gustation, and emotion). We found that conceptual processing consistently engages brain regions also activated during real perceptual-motor experience of the same modalities. In addition, we identified multimodal convergence zones that are recruited for multiple modalities. In particular, the left inferior parietal lobe (IPL) and posterior middle temporal gyrus (pMTG) are engaged for three modalities: action, motion, and sound. These "trimodal" regions are surrounded by "bimodal" regions engaged for two modalities. Our findings support a novel model of the conceptual system, according to which conceptual processing relies on a hierarchical neural architecture from modality-specific to multimodal areas up to an amodal hub.

Cortical, subcortical, and cerebellar contributions to language processing: A meta-analytic review of 403 neuroimaging experiments.

Language is a key human faculty for communication and interaction that provides invaluable insight into the human mind. Previous work has dissected different linguistic operations, but the large-scale brain networks involved in language processing are still not fully uncovered. Particularly, little is known about the subdomain-specific engagement of brain areas during semantic, syntactic, phonological, and prosodic processing and the role of subcortical and cerebellar areas. Here, we present the largest coordinate-based meta-analysis of language processing including 403 experiments. Overall, language processing primarily engaged bilateral fronto-temporal cortices, with the highest activation likelihood in the left posterior inferior frontal gyrus (IFG). Whereas we could not detect any syntax-specific regions, semantics specifically engaged left posterior temporal areas (left fusiform and occipitotemporal cortex) and the left frontal pole. Phonology showed highest subdomain-specificity in bilateral auditory and left postcentral regions, whereas prosody engaged specifically the right amygdala and the right IFG. Across all subdomains and modalities, we found strong bilateral subcortical and cerebellar contributions. Especially the right cerebellum was engaged during various processes, including speech production, visual, and phonological tasks. Collectively, our results emphasize consistent recruitment and high functional modularity for general language processing in bilateral domain-specific (temporo-frontal) and domain-general (medial frontal/anterior cingulate cortex) regions but also a high specialization of different subareas for different linguistic subdomains. Our findings refine current neurobiological models of language by adding novel insight into the general sensitivity of the language network and subdomain-specific functions of different brain areas and highlighting the role of subcortical and cerebellar regions for different language operations. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

The role of the angular gyrus in semantic cognition: a synthesis of five functional neuroimaging studies.

Semantic knowledge is central to human cognition. The angular gyrus (AG) is widely considered a key brain region for semantic cognition. However, the role of the AG in semantic processing is controversial. Key controversies concern response polarity (activation vs. deactivation) and its relation to task difficulty, lateralization (left vs. right AG), and functional-anatomical subdivision (PGa vs. PGp subregions). Here, we combined the fMRI data of five studies on semantic processing (n = 172) and analyzed the response profiles from the same anatomical regions-of-interest for left and right PGa and PGp. We found that the AG was consistently deactivated during non-semantic conditions, whereas response polarity during semantic conditions was inconsistent. However, the AG consistently showed relative response differences between semantic and non-semantic conditions, and between different semantic conditions. A combined analysis across all studies revealed that AG responses could be best explained by separable effects of task difficulty and semantic processing demand. Task difficulty effects were stronger in PGa than PGp, regardless of hemisphere. Semantic effects were stronger in left than right AG, regardless of subregion. These results suggest that the AG is engaged in both domain-general task-difficulty-related processes and domain-specific semantic processes. In semantic processing, we propose that left AG acts as a "multimodal convergence zone" that binds different semantic features associated with the same concept, enabling efficient access to task-relevant features.