Humans in Love Are Singing Birds: Socially-Mediated Brain Activity in Language Production

Published: August 30 2023This functional magnetic resonance imaging (fMRI) study investigated whether and how the human speech production circuit is mediated by social factors. Participants recited a poem in the MRI scanner while viewing pictures of their lover, unknown persons, or houses to simulate different social contexts. The results showed, as expected, the recruitment of the speech production circuit during recitation. However, for the first time, we demonstrated that this circuit is tightly linked to the network underlying social cognition. The socially relevant contexts (familiar and unfamiliar persons) elicited the recruitment of a widespread bilateral circuit including regions such as the amygdala, anterior cingulate, and orbitofrontal cortex, in contrast to the non-socially relevant context (houses). We also showed a neural gradient generated by the differences in the social relevance of affective and nonaffective contexts. This study opens up a novel line of research into socially mediated speech production, revealing drastic differences in brain activation when performing the same speech production task in different social contexts. Interestingly, the analogous avian anterior neural pathway in the zebra finch is also differentially activated when the bird sings facing a (potential) mate or alone. Thus, this study suggests that despite important phylogenetic differences, speech production in humans is based, as in songbirds, on a complex neural circuitry that is modulated by evolutionarily primordial aspects such as the social relevance of the addressee.Manuel Carreiras, Eusko Jaurlaritza (https://dx.doi.org/10.13039/501100003086), Award ID: BERC 2018 2021. Manuel Carreiras, Agencia Estatal de Investigación (https://dx.doi.org/10 .13039/501100011033), Award ID: CEX2020-001010-S. Manuel Carreiras, Ministerio de Economía y Competitividad (https://dx.doi.org/10.13039/501100003329), Award ID: RTI2018 093547 B I00. Ileana Quiñones, Ministerio de Economía y Competitividad (https:// dx.doi.org/10.13039/501100003329), Award ID: RTI2018 093547 B I00. Clara Martin, Ministerio de Economía y Competitividad (https://dx.doi.org/10.13039/501100003329), Award ID: PID2020-113926GB-I00. Clara Martin, H2020 European Research Council (https://dx.doi.org /10.13039/100010663), Award ID: 819093

Disentangling meaning in the brain: Left temporal involvement in agreement processing

Published online 18 November 2016Sentence comprehension is successfully accomplished by means of a form-to-meaning mapping procedure that relies on the extraction of morphosyntactic information from the input and its mapping to higher-level semantic–discourse representations. In this study, we sought to determine whether neuroanatomically distinct brain regions are involved in the processing of different types of information contained in the propositional meaning of a sentence, namely person and number. While person information indexes the role that an individual has in discourse (i.e., the speaker, the addressee or the entity being talked about by speaker and addressee), number indicates its cardinality (i.e., a single entity vs a multitude of entities). An event-related functional magnetic resonance imaging (fMRI) experiment was run using agreement-Correct and Person- and Number-violated sentences in Spanish, to disentangle the processing mechanisms and neural substrates associated with the building of discourse and cardinality representations. The contrast between Person and Number Violations showed qualitative and quantitative differences. A greater response for person compared to number was found in the left middle temporal gyrus (LMTG). However, critically, a posterior-to-anterior functional gradient emerged within this region. While the posterior portion of the LMTG was sensitive to both Person and Number Violations, the anterior portion of this region showed selective response for Person Violations. These results confirm that the comprehension of the propositional meaning of a sentence results from a composite, feature-sensitive mechanism of form-to-meaning mapping in which the nodes of the language network are differentially involved.BCBL acknowledges funding from Ayuda Centro de Excelencia Severo Ochoa SEV-2015-0490. S.M. acknowledges funding from the Gipuzkoako Foru Aldundia Fellowship Program and from grant PI_2014_38 from the Basque Government. N.M. was funded by grant PSI2012- 32350 and PSI2015-65694-P from the Spanish Ministry of Economy and Competitiveness. M.C was funded by grant PSI2012-31448 from the Spanish Ministry of Science and Innovation and ERC-2011-ADG-295362 from the European Research Council

What Can Glioma Patients Teach Us about Language (Re)Organization in the Bilingual Brain: Evidence from fMRI and MEG

Published: 25 May 2021Recent evidence suggests that the presence of brain tumors (e.g., low-grade gliomas) triggers language reorganization. Neuroplasticity mechanisms called into play can transfer linguistic functions from damaged to healthy areas unaffected by the tumor. This phenomenon has been reported in monolingual patients, but much less is known about the neuroplasticity of language in the bilingual brain. A central question is whether processing a first or second language involves the same or different cortical territories and whether damage results in diverse recovery patterns depending on the language involved. This question becomes critical for preserving language areas in bilingual brain-tumor patients to prevent involuntary pathological symptoms following resection. While most studies have focused on intraoperative mapping, here, we go further, reporting clinical cases for five bilingual patients tested before and after tumor resection, using a novel multimethod approach merging neuroimaging information from fMRI and MEG to map the longitudinal reshaping of the language system. Here, we present four main findings. First, all patients preserved linguistic function in both languages after surgery, suggesting that the surgical intervention with intraoperative language mapping was successful in preserving cortical and subcortical structures necessary for brain plasticity at the functional level. Second, we found reorganization of the language network after tumor resection in both languages, mainly reflected by a shift of activity to right hemisphere nodes and the recruitment of ipsilesional left nodes. Third, we found that this reorganization varied according to the language involved, indicating that L1 and L2 follow different reshaping patterns after surgery. Fourth, oscillatory longitudinal effects were correlated with BOLD laterality changes in superior parietal and middle frontal areas. These findings may reflect that neuroplasticity impacts on the compensatory involvement of executive control regions, supporting the allocation of cognitive resources as a consequence of increased attentional demands. Furthermore, these results hint at the complementary role of this neuroimaging approach in language mapping, with fMRI offering excellent spatial localization and MEG providing optimal spectrotemporal resolutionThis research was supported by the Ikerbasque Foundation; by the Basque Government through the BERC 2018 2021 program; by the Spanish State Research Agency through BCBL Severo Ochoa excellence accreditation SEV 2015 0490; by the Fundación Científica AECC (FCAECC) through the project PROYE20005CARR; by a Juan de la Cierva Fellowship to LA (IJCI 2017 31373); and by the Spanish Ministry of Economy and Competitiveness through the Plan Nacional RTI2018 096216 A I00 (MEGLIOMA) to LA and RTI2018 093547 B I00 (LANGCONN) to MC and IQ

Tracing the interplay between syntactic and lexical features: fMRI evidence from agreement comprehension

Available online 29 March 2018The current fMRI study was designed to investigate whether the processing of different gender-related cues embedded in nouns affects the computation of agreement dependencies and, if so, where this possible interaction is mapped in the brain. We used the Spanish gender agreement system, which makes it possible to manipulate two different factors: the agreement between different sentence constituents (i.e., by contrasting congruent versus incongruent determiner-noun pairs) and the formal (i.e., orthographical/morphological) and/or lexical information embedded in the noun –i.e., by contrasting transparent (e.g., libromasc. [book]; lunafem. [moon]) and opaque nouns (e.g., l apizmasc. [pencil]; vejezfem. [old age]). Crucially, these data illustrated, for the first time, how the network underlying agreement is sensitive to different gender-to-ending cues: different sources of gender information associated with nouns affect the neural circuits involved in the computation of local agreement dependencies. When the gender marking is informative (as in the case of transparent nouns), both formal and lexical information is used to establish grammatical relations. In contrast, when no formal cues are available (as in the case of opaque nouns), gender information is retrieved from the lexicon. We demonstrated the involvement of the posterior MTG/STG, pars triangularis within the IFG, and parietal regions during gender agreement computation. Critically, in order to integrate the different available information sources, the dynamics of this fronto-temporal loop change and additional regions, such as the hippocampus, the angular and the supramarginal gyri are recruited. These results underpin previous neuroanatomical models proposed in the context of both gender processing and sentence comprehension. But, more importantly, they provide valuable information regarding how and where the brain's language system dynamically integrates all the available form-based and lexical cues during comprehension.This research was partially supported by Severo Ochoa program grant SEV-2015-049; grant ERC-2011-ADG-295362 from the European Research Council, and grants PSI2015-67353-R and PSI2015-65694-P from the MINECO

Distinctive Frontal and Occipitotemporal Surface Features in Neglectful Parenting.

Although the brain signatures of adaptive human parenting are well documented, the cortical features associated with maladaptive caregiving are underexplored. We investigated whether cortical thickness and surface area vary in a small group of mothers who had neglected their children (24 in the neglect group, NG) compared to a control group of mothers with non-neglectful caregiving (21 in the control group, CG). We also tested whether the cortical differences were related to dyadic mother-child emotional availability (EA) in a play task with their children and whether alexithymia involving low emotional awareness that characterizes the NG could play a role in the cortical-EA associations. Whole-brain analysis of the cortical mantle identified reduced cortical thickness in the right rostral middle frontal gyrus and an increased surface area in the right lingual and lateral occipital cortices for the NG with respect to the CG. Follow-up path analysis showed direct effects of the right rostral middle frontal gyrus (RMFG) on the emotional availability (EA) and on the difficulty to identify feelings (alexithymia factor), with a marginal indirect RMFG-EA effect through this factor. These preliminary findings extend existing work by implicating differences in cortical features associated with neglectful parenting and relevant to mother-child interactive bonding

Distinctive Frontal and Occipitotemporal Surface Features in Neglectful Parenting.

Although the brain signatures of adaptive human parenting are well documented, the cortical features associated with maladaptive caregiving are underexplored. We investigated whether cortical thickness and surface area vary in a small group of mothers who had neglected their children (24 in the neglect group, NG) compared to a control group of mothers with non-neglectful caregiving (21 in the control group, CG). We also tested whether the cortical differences were related to dyadic mother-child emotional availability (EA) in a play task with their children and whether alexithymia involving low emotional awareness that characterizes the NG could play a role in the cortical-EA associations. Whole-brain analysis of the cortical mantle identified reduced cortical thickness in the right rostral middle frontal gyrus and an increased surface area in the right lingual and lateral occipital cortices for the NG with respect to the CG. Follow-up path analysis showed direct effects of the right rostral middle frontal gyrus (RMFG) on the emotional availability (EA) and on the difficulty to identify feelings (alexithymia factor), with a marginal indirect RMFG-EA effect through this factor. These preliminary findings extend existing work by implicating differences in cortical features associated with neglectful parenting and relevant to mother-child interactive bonding

Distinctive Frontal and Occipitotemporal Surface Features in Neglectful Parenting

Published: 18 March 2021Although the brain signatures of adaptive human parenting are well documented, the cortical features associated with maladaptive caregiving are underexplored. We investigated whether cortical thickness and surface area vary in a small group of mothers who had neglected their children (24 in the neglect group, NG) compared to a control group of mothers with non-neglectful caregiving (21 in the control group, CG). We also tested whether the cortical differences were related to dyadic mother-child emotional availability (EA) in a play task with their children and whether alexithymia involving low emotional awareness that characterizes the NG could play a role in the cortical-EA associations. Whole-brain analysis of the cortical mantle identified reduced cortical thickness in the right rostral middle frontal gyrus and an increased surface area in the right lingual and lateral occipital cortices for the NG with respect to the CG. Follow-up path analysis showed direct effects of the right rostral middle frontal gyrus (RMFG) on the emotional availability (EA) and on the difficulty to identify feelings (alexithymia factor), with a marginal indirect RMFG-EA effect through this factor. These preliminary findings extend existing work by implicating differences in cortical features associated with neglectful parenting and relevant to mother-child interactive bonding.This research was funded by the Spanish Ministry of Economy and Competitiveness and the European Regional Development Fund, grant number RTI2018‐098149‐B‐I00 to M.J.R. and I.L, and by the European Union’s Horizon 2020 Research and Innovation Programme under the Marie Sklodowska‐Curie Individual Fellowship, grant agreement number 893329 to L.G.P

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

Published online: 8 September 2020Picture 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.Funded by Severo Ochoa (SEV-2015-049); the European Research Council (ERC-2011-ADG-295362), and MINECO (RTI2018- 093547-B-I00)

Grey Matter Reshaping of Language-Related Regions Depends on Tumor Lateralization

Published: 28 July 2023A brain tumor in the left hemisphere can decrease language laterality as assessed through fMRI. However, it remains unclear whether or not this decreased language laterality is associated with a structural reshaping of the grey matter, particularly within the language network. Here, we examine if the disruption of the language hubs exclusively affects the macrostructural properties of the contralateral homologues or whether it affects both hemispheres. This study uses voxel-based morphometry applied to high-resolution MR T1-weighted MPRAGE images from 31 adult patients’ left hemisphere, which is dominant for language. Eighteen patients had brain tumors in the left hemisphere, and thirteen had tumors in the right hemisphere. A cohort of 71 healthy individuals matched with respect to age and sex was used as a baseline. We defined 10 ROIs per hemisphere involved in language function. Two separate repeated-measure ANOVAs were conducted with the volume per region as the dependent variable. For the patients, tumor lateralization (right versus left) served as a between-subject factor. The current study demonstrated that the presence of a brain tumor generates global volumetric changes affecting the left language regions and their contralateral homologues. These changes are mediated by the lateralization of the lesion. Our findings suggest that functional mechanisms are supported by the rearrangement of the grey matter.This research was supported by the Basque Government through the BERC 2022–2025 program; the Spanish State Research Agency through BCBL Severo Ochoa excellence accreditation CEX2020−001010-S; the Fundación Científica AECC (FCAECC) through the project PROYE20005CARR; the Spanish Ministry of Economy and Competitiveness through the Plan Nacional RTI2018 093547 B I00 (LANGCONN) awarded to I.Q.; the Spanish Ministry of Science, Innovation and Universities through the predoctoral grant PRE2019-091492 awarded to L.M.-O.; and the NIH (NIDCD) grant K01DC016904 (Comprehensive presurgical identification of the critical language network in tumor patients) awarded to M.M.P

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 (similar to 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 lifeBasque Government, Grant/Award Number: BERC 2018-2021; Spanish Ministry of Economy and Competitiveness, Grant/Award Number: RTI2018-096216-A-I00 (MEGLIOMA) and RTI2018-093547-B-I00 (LangConn); Spanish State Research Agency, Grant/Award Number: SEV-2015-0490 and IJCI-2017-3137