Publications by authors named "Ruth de Diego-Balaguer"

42 Publications

Rethinking attention in time: Expectancy violations reconcile contradictory developmental evidence.

J Exp Child Psychol 2021 Jun 15;206:105070. Epub 2021 Feb 15.

Department of Cognition, Development and Educational Psychology, University of Barcelona, 08035 Barcelona, Spain; Institute of Neurosciences, University of Barcelona, 08035 Barcelona, Spain; Cognition and Brain Plasticity Unit, Institut d'Investigació Biomèdica de Bellvitge (IDIBELL), 08908 L'Hospitalet de Llobregat, Barcelona, Spain; Institució Catalana de Recerca i Estudis Avançats (ICREA), 08010 Barcelona, Spain.

Temporal expectations critically influence perception and action. Previous research reports contradictory results in children's ability to endogenously orient attention in time as well as the developmental course. To reconcile this seemingly conflicting evidence, we put forward the hypothesis that expectancy violations-through the use of invalid trials-are the source of the mixed evidence reported in the literature. With the aim of offering new results that could reconcile previous findings, we tested a group of young children (4- to 7-year-olds), an older group (8- to 12-year-olds), and a group of adults. Temporal cues provided expectations about target onset time, and invalid trials were used such that the target appeared at the unexpected time in 25% of the trials. In both experiments, the younger children responded faster in valid trials than in invalid trials, showing that they benefited from the temporal cue. These results show that young children rely on temporal expectations to orient attention in time endogenously. Importantly, younger children exhibited greater validity effects than older children and adults, and these effects correlated positively with participants' performance in the invalid (unexpected) trials. We interpret the reduction of validity effects with age as an index of better adaptation to the invalid (unexpected) condition. By using invalid trials and testing three age groups, we demonstrate that previous findings are not inconsistent. Rather, evidence converges when considering the presence of expectancy violations that require executive control mechanisms, which develop progressively during childhood. We propose a distinction between rigid and flexible mechanisms of temporal orienting to accommodate all findings.
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http://dx.doi.org/10.1016/j.jecp.2020.105070DOI Listing
June 2021

Integrating when and what information in the left parietal lobe allows language rule generalization.

PLoS Biol 2020 11 2;18(11):e3000895. Epub 2020 Nov 2.

Cognition and Brain Plasticity Unit, IDIBELL, L'Hospitalet de Llobregat, Spain.

A crucial aspect when learning a language is discovering the rules that govern how words are combined in order to convey meanings. Because rules are characterized by sequential co-occurrences between elements (e.g., "These cupcakes are unbelievable"), tracking the statistical relationships between these elements is fundamental. However, purely bottom-up statistical learning alone cannot fully account for the ability to create abstract rule representations that can be generalized, a paramount requirement of linguistic rules. Here, we provide evidence that, after the statistical relations between words have been extracted, the engagement of goal-directed attention is key to enable rule generalization. Incidental learning performance during a rule-learning task on an artificial language revealed a progressive shift from statistical learning to goal-directed attention. In addition, and consistent with the recruitment of attention, functional MRI (fMRI) analyses of late learning stages showed left parietal activity within a broad bilateral dorsal frontoparietal network. Critically, repetitive transcranial magnetic stimulation (rTMS) on participants' peak of activation within the left parietal cortex impaired their ability to generalize learned rules to a structurally analogous new language. No stimulation or rTMS on a nonrelevant brain region did not have the same interfering effect on generalization. Performance on an additional attentional task showed that this rTMS on the parietal site hindered participants' ability to integrate "what" (stimulus identity) and "when" (stimulus timing) information about an expected target. The present findings suggest that learning rules from speech is a two-stage process: following statistical learning, goal-directed attention-involving left parietal regions-integrates "what" and "when" stimulus information to facilitate rapid rule generalization.
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http://dx.doi.org/10.1371/journal.pbio.3000895DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7660506PMC
November 2020

Names and their meanings: A dual-process account of proper-name encoding and retrieval.

Neurosci Biobehav Rev 2020 01 14;108:308-321. Epub 2019 Nov 14.

Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain; Cognition and Brain Plasticity Unit, Institut d'Investigació Biomèdica de Bellvitge, Barcelona, Spain; Department of Cognition, Development and Educational Psychology, University of Barcelona, Barcelona, Spain; Institute of Neuroscience, University of Barcelona, Barcelona, Spain.

The ability to pick out a unique entity with a proper name is an important component of human language. It has been a primary focus of research in the philosophy of language since the nineteenth century. Brain-based evidence has shed new light on this capacity, and an extensive literature indicates the involvement of distinct fronto-temporal and temporo-occipito-parietal association cortices in proper-name retrieval. However, comparatively few efforts have sought to explain how memory encoding processes lead to the later recruitment of these distinct regions at retrieval. Here, we provide a unified account of proper-name encoding and retrieval, reviewing evidence that socio-emotional and unitized encoding subserve the retrieval of proper names via anterior-temporal-prefrontal activations. Meanwhile, non-unitized item-item and item-context encoding support subsequent retrieval, largely dependent on the temporo-occipito-parietal cortex. We contend that this well-established divergence in encoding systems can explain how proper names are later retrieved from distinct neural structures. Furthermore, we explore how evidence reviewed here can inform a century-and-a-half-old debate about proper names and the meanings they pick out.
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http://dx.doi.org/10.1016/j.neubiorev.2019.11.005DOI Listing
January 2020

White matter cortico-striatal tracts predict apathy subtypes in Huntington's disease.

Neuroimage Clin 2019 30;24:101965. Epub 2019 Jul 30.

Cognition and Brain Plasticity Unit, Bellvitge Biomedical Research Institute - IDIBELL, 08097 L'Hospitalet de Llobregat, Barcelona, Spain. Electronic address:

Background: Apathy is the neuropsychiatric syndrome that correlates most highly with Huntington's disease progression, and, like early patterns of neurodegeneration, is associated with lesions to cortico-striatal connections. However, due to its multidimensional nature and elusive etiology, treatment options are limited.

Objectives: To disentangle underlying white matter microstructural correlates across the apathy spectrum in Huntington's disease.

Methods: Forty-six Huntington's disease individuals (premanifest (N = 22) and manifest (N = 24)) and 35 healthy controls were scanned at 3-tesla and underwent apathy evaluation using the short-Problem Behavior Assessment and short-Lille Apathy Rating Scale, with the latter being characterized into three apathy domains, namely emotional, cognitive, and auto-activation deficit. Diffusion tensor imaging was used to study whether individual differences in specific cortico-striatal tracts predicted global apathy and its subdomains.

Results: We elucidate that apathy profiles may develop along differential timelines, with the auto-activation deficit domain manifesting prior to motor onset. Furthermore, diffusion tensor imaging revealed that inter-individual variability in the disruption of discrete cortico-striatal tracts might explain the heterogeneous severity of apathy profiles. Specifically, higher levels of auto-activation deficit symptoms significantly correlated with increased mean diffusivity in the right uncinate fasciculus. Conversely, those with severe cognitive apathy demonstrated increased mean diffusivity in the right frontostriatal tract and left dorsolateral prefrontal cortex to caudate nucleus tract.

Conclusions: The current study provides evidence that white matter correlates associated with emotional, cognitive, and auto-activation subtypes may elucidate the heterogeneous nature of apathy in Huntington's disease, as such opening a door for individualized pharmacological management of apathy as a multidimensional syndrome in other neurodegenerative disorders.
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http://dx.doi.org/10.1016/j.nicl.2019.101965DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6700450PMC
September 2020

Specific patterns of brain alterations underlie distinct clinical profiles in Huntington's disease.

Neuroimage Clin 2019 15;23:101900. Epub 2019 Jun 15.

Cognition and Brain Plasticity Unit, L'Hospitalet de Llobregat (Barcelona), IDIBELL (Institut d'Investigació Biomèdica de Bellvitge), Spain.

Huntington's disease (HD) is a genetic neurodegenerative disease which involves a triad of motor, cognitive and psychiatric disturbances. However, there is great variability in the prominence of each type of symptom across individuals. The neurobiological basis of such variability remains poorly understood but would be crucial for better tailored treatments. Multivariate multimodal neuroimaging approaches have been successful in disentangling these profiles in other disorders. Thus we applied for the first time such approach to HD. We studied the relationship between HD symptom domains and multimodal measures sensitive to grey and white matter structural alterations. Forty-three HD gene carriers (23 manifest and 20 premanifest individuals) were scanned and underwent behavioural assessments evaluating motor, cognitive and psychiatric domains. We conducted a multimodal analysis integrating different structural neuroimaging modalities measuring grey matter volume, cortical thickness and white matter diffusion indices - fractional anisotropy and radial diffusivity. All neuroimaging measures were entered into a linked independent component analysis in order to obtain multimodal components reflecting common inter-subject variation across imaging modalities. The relationship between multimodal neuroimaging independent components and behavioural measures was analysed using multiple linear regression. We found that cognitive and motor symptoms shared a common neurobiological basis, whereas the psychiatric domain presented a differentiated neural signature. Behavioural measures of different symptom domains correlated with different neuroimaging components, both the brain regions involved and the neuroimaging modalities most prominently associated with each type of symptom showing differences. More severe cognitive and motor signs together were associated with a multimodal component consisting in a pattern of reduced grey matter, cortical thickness and white matter integrity in cognitive and motor related networks. In contrast, depressive symptoms were associated with a component mainly characterised by reduced cortical thickness pattern in limbic and paralimbic regions. In conclusion, using a multivariate multimodal approach we were able to disentangle the neurobiological substrates of two distinct symptom profiles in HD: one characterised by cognitive and motor features dissociated from a psychiatric profile. These results open a new view on a disease classically considered as a uniform entity and initiates a new avenue for further research considering these qualitative individual differences.
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http://dx.doi.org/10.1016/j.nicl.2019.101900DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6606833PMC
August 2020

Spontaneous synchronization to speech reveals neural mechanisms facilitating language learning.

Nat Neurosci 2019 04 4;22(4):627-632. Epub 2019 Mar 4.

Department of Psychology, New York University, New York, NY, USA.

We introduce a deceptively simple behavioral task that robustly identifies two qualitatively different groups within the general population. When presented with an isochronous train of random syllables, some listeners are compelled to align their own concurrent syllable production with the perceived rate, whereas others remain impervious to the external rhythm. Using both neurophysiological and structural imaging approaches, we show group differences with clear consequences for speech processing and language learning. When listening passively to speech, high synchronizers show increased brain-to-stimulus synchronization over frontal areas, and this localized pattern correlates with precise microstructural differences in the white matter pathways connecting frontal to auditory regions. Finally, the data expose a mechanism that underpins performance on an ecologically relevant word-learning task. We suggest that this task will help to better understand and characterize individual performance in speech processing and language learning.
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http://dx.doi.org/10.1038/s41593-019-0353-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6435400PMC
April 2019

An active cognitive lifestyle as a potential neuroprotective factor in Huntington's disease.

Neuropsychologia 2019 01 26;122:116-124. Epub 2018 Oct 26.

Cognition and Brain Plasticity Unit, Neuroscience Program, IDIBELL (Institut d'Investigació Biomèdica de Bellvitge), L'Hospitalet de Llobregat, Barcelona, Spain. Electronic address:

A cognitive stimulating lifestyle has been observed to confer cognitive benefits in multiple neurodegenerative diseases. However, the underlying neurobiological basis of this phenomenon remains unclear. Huntington's disease can provide a suitable model to study the effects and neural mechanisms of cognitive engagement in neurodegeneration. In this study, we investigate the effect of lifestyle factors such as education, occupation and engagement in cognitive activities in Huntington's disease gene carriers on cognitive performance and age of onset as well as the underlying neural changes sustaining these effects, measured by magnetic resonance imaging. Specifically, we analyzed both gray matter volume and the strength of connectivity of the executive control resting-state network. High levels of cognitive engagement were significantly associated with more preserved executive functions, a delay in the appearance of symptoms, reduced volume loss of the left precuneus and the bilateral caudate and a modulation of connectivity strength of anterior cingulate cortex and left angular gyrus with the executive control network. These findings suggest that a cognitively stimulating lifestyle may promote brain maintenance by modulating the executive control resting-state network and conferring protection against neurodegeneration, which results in a delayed onset of symptoms and improved performance in executive functions.
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http://dx.doi.org/10.1016/j.neuropsychologia.2018.10.017DOI Listing
January 2019

Implicit but not explicit extinction to threat-conditioned stimulus prevents spontaneous recovery of threat-potentiated startle responses in humans.

Brain Behav 2019 01 4;9(1):e01157. Epub 2018 Dec 4.

Department of Cognition, Development and Educational Psychology, University of Barcelona, Barcelona, Spain.

Introduction: It has long been posited that threat learning operates and forms under an affective and a cognitive learning system that is supported by different brain circuits. A primary drawback in exposure-based therapies is the high rate of relapse that occurs when higher order areas fail to inhibit responses driven by the defensive circuit. It has been shown that implicit exposure of fearful stimuli leads to a long-lasting reduction in avoidance behavior in patients with phobia. Despite the potential benefits of this approach in the treatment of phobias and posttraumatic stress disorder, implicit extinction is still underinvestigated.

Methods: Two groups of healthy participants were threat conditioned. The following day, extinction training was conducted using a stereoscope. One group of participants was explicitly exposed with the threat-conditioned image, while the other group was implicitly exposed using a continuous flash suppression (CFS) technique. On the third day, we tested the spontaneous recovery of defensive responses using explicit presentations of the images.

Results: On the third day, we found that only the implicit extinction group showed reduced spontaneous recovery of defensive responses to the threat-conditioned stimulus, measured by threat-potentiated startle responses but not by the electrodermal activity.

Conclusion: Our results suggest that implicit extinction using CFS might facilitate the modulation of the affective component of fearful memories, attenuating its expression after 24 hr. The limitations of the CFS technique using threatful stimuli urge the development of new strategies to improve implicit presentations and circumvent such limitations. Our study encourages further investigations of implicit extinction as a potential therapeutic target to further advance exposure-based psychotherapies.
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http://dx.doi.org/10.1002/brb3.1157DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6346649PMC
January 2019

Structural priming in sentence comprehension: A single prime is enough.

PLoS One 2018 2;13(4):e0194959. Epub 2018 Apr 2.

Département d'Etudes Cognitives, Ecole Normale Supérieure-PSL Research University, Paris, France.

Experiencing a syntactic structure affects how we process subsequent instances of that structure. This phenomenon, called structural priming, is observed both in language production and in language comprehension. However, while abstract syntactic structures can be primed independent of lexical overlap in sentence production, evidence for structural priming in comprehension is more elusive. In addition, when structural priming in comprehension is found, it can often be accounted for in terms of participants' explicit expectations. Participants may use the structural repetition over several sentences and build expectations, which create a priming effect. Here, we use a new experimental paradigm to investigate structural priming in sentence comprehension independent of lexical overlap and of participants' expectations. We use an outcome dependent variable instead of commonly used online measures, which allows us to more directly compare these effects with those found in sentence production studies. We test priming effects in syntactically homogeneous and heterogeneous conditions on a sentence-picture matching task that forces participants to fully parse the sentences. We observe that, while participants learn the structural regularity in the homogeneous condition, structural priming is also found in the heterogeneous condition, in which participants do not expect any particular structure. In fact, we find that a single prime is enough to trigger priming. Our results indicate that-like in sentence production-structural priming can be observed in sentence comprehension without lexical repetition and independent of participants' expectation.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0194959PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5880384PMC
July 2018

Language Learning Variability within the Dorsal and Ventral Streams as a Cue for Compensatory Mechanisms in Aphasia Recovery.

Front Hum Neurosci 2017 27;11:476. Epub 2017 Sep 27.

Cognition and Brain Plasticity Group, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain.

Dorsal and ventral pathways connecting perisylvian language areas have been shown to be functionally and anatomically segregated. Whereas the dorsal pathway integrates the sensory-motor information required for verbal repetition, the ventral pathway has classically been associated with semantic processes. The great individual differences characterizing language learning through life partly correlate with brain structure and function within these dorsal and ventral language networks. Variability and plasticity within these networks also underlie inter-individual differences in the recovery of linguistic abilities in aphasia. Despite the division of labor of the dorsal and ventral streams, studies in healthy individuals have shown how the interaction of them and the redundancy in the areas they connect allow for compensatory strategies in functions that are usually segregated. In this mini-review we highlight the need to examine compensatory mechanisms between streams in healthy individuals as a helpful guide to choosing the most appropriate rehabilitation strategies, using spared functions and targeting preserved compensatory networks for brain plasticity.
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http://dx.doi.org/10.3389/fnhum.2017.00476DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5623718PMC
September 2017

Reduced striato-cortical and inhibitory transcallosal connectivity in the motor circuit of Huntington's disease patients.

Hum Brain Mapp 2018 01 8;39(1):54-71. Epub 2017 Oct 8.

Cognition and Brain Plasticity Unit, IDIBELL (Institut d'Investigació Biomèdica de Bellvitge), L'Hospitalet de Llobregat, Barcelona, Spain.

Huntington's disease (HD) is a neurodegenerative disorder which is primarily associated with striatal degeneration. However, the alterations in connectivity of this structure in HD have been underinvestigated. In this study, we analyzed the functional and structural connectivity of the left putamen, while participants performed a finger-tapping task. Using fMRI and DW-MRI, 30 HD gene expansion carriers (HDGEC) and 29 healthy participants were scanned. Psychophysiological interaction analysis and DTI-based tractography were employed to examine functional and structural connectivity, respectively. Manifest HDGEC exhibited a reduced functional connectivity of the left putamen with the left and the right primary sensorimotor areas (SM1). Based on this result, the inhibitory functional connectivity between the left SM1 and the right SM1 was explored, appearing to be also decreased. In addition, the tract connecting these areas (motor corpus callosum), and the tract connecting the left putamen with the left SM1 appeared disrupted in HDGEC compared to controls. Significant correlations were found between measures of functional and structural connectivity of the motor corpus callosum, showing a coupling of both types of alterations in this tract. The observed reduction of functional and structural connectivity was associated with worse motor scores, which highlights the clinical relevance of these results. Hum Brain Mapp 39:54-71, 2018. © 2017 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/hbm.23813DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6866479PMC
January 2018

Endogenous temporal attention in the absence of stimulus-driven cues emerges in the second year of life.

PLoS One 2017 8;12(9):e0184698. Epub 2017 Sep 8.

Department of Cognition, Development, and Educational Psychology, University of Barcelona, Barcelona, Spain.

Anticipating both where and when an object will appear is a critical ability for adaptation. Research in the temporal domain in adults indicate that dissociable mechanisms relate to endogenous attention driven by the properties of the stimulus themselves (e.g. rhythmic, sequential, or trajectory cues) and driven by symbolic cues. In infancy, we know that the capacity to endogenously orient attention progressively develops through infancy. However, the above-mentioned distinction has not yet been explored since previous studies involved stimulus-driven cues. The current study tested 12- and 15-month-olds in an adaptation of the anticipatory eye movement procedure to determine whether infants were able to anticipate a specific location and temporal interval predicted only by symbolic pre-cues. In the absence of stimulus-driven cues, results show that only 15-month-olds could show anticipatory behavior based on the temporal information provided by the symbolic cues. Distinguishing stimulus-driven expectations from those driven by symbolic cues allowed dissecting more clearly the developmental progression of temporal endogenous attention.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0184698PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5590992PMC
October 2017

A systematic linguistic profile of spontaneous narrative speech in pre-symptomatic and early stage Huntington's disease.

Cortex 2018 03 9;100:71-83. Epub 2017 Aug 9.

ICREA (Catalan Institution for Research and Advanced Studies), Barcelona, Spain; Cognition and Brain Plasticity Unit, IDIBELL, L'Hospitalet de Llobregat, Spain; Department of Cognition, Development and Educational Psychology, Universitat de Barcelona, Barcelona, Spain; Institute of Neurosciences, Universitat de Barcelona, Barcelona, Spain. Electronic address:

Cognitive decline accompanying the clinically more salient motor symptoms of Huntington's disease (HD) has been widely noted and can precede motor symptoms onset. Less clear is how such decline bears on language functions in everyday life, though a small number of experimental studies have revealed difficulties with the application of rule-based aspects of language in early stages of the disease. Here we aimed to determine whether there is a systematic linguistic profile that characterizes spontaneous narrative speech in both pre-manifest and/or early manifest HD, and how it is related to striatal degeneration and neuropsychological profiles. Twenty-eight early-stage patients (19 manifest and 9 gene-carriers in the pre-manifest stage), matched with 28 controls, participated in a story-telling task. Speech was blindly scored by independent raters according to fine-grained linguistic variables distributed over 5 domains for which composite scores were computed (Quantitative, Fluency, Reference, Connectivity, and Concordance). Voxel-based morphometry (VBM) was used to link specific brain degeneration patterns to loci of linguistic decline. In all of these domains, significant differences were observed between groups. Deficits in Reference and Connectivity were seen in the pre-manifest stage, where no other neuropsychological impairment was detected. Among HD patients, there was a significant positive correlation only between the values in the Quantitative domain and gray matter volume bilaterally in the putamen and pallidum. These results fill the gap of qualitative data of spontaneous narrative speech in HD and reveal that HD is characterized by systematic linguistic impairments leading to dysfluencies and disorganization in core domains of grammatical organization. This includes the referential use of noun phrases and the embedding of clauses, which mediate crucial dimensions of meaning in language in its normal social use. Moreover, such impairment is seen prior to motor symptoms onset and when standardized neuropsychological test profiles are otherwise normal.
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http://dx.doi.org/10.1016/j.cortex.2017.07.022DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5845634PMC
March 2018

Semantic and phonological schema influence spoken word learning and overnight consolidation.

Q J Exp Psychol (Hove) 2018 Jun 19;71(6):1469-1481. Epub 2018 Jan 19.

4 Cognition and Brain Sciences Unit, Medical Research Council, Cambridge, UK.

We studied the initial acquisition and overnight consolidation of new spoken words that resemble words in the native language (L1) or in an unfamiliar, non-native language (L2). Spanish-speaking participants learned the spoken forms of novel words in their native language (Spanish) or in a different language (Hungarian), which were paired with pictures of familiar or unfamiliar objects, or no picture. We thereby assessed, in a factorial way, the impact of existing knowledge (schema) on word learning by manipulating both semantic (familiar vs unfamiliar objects) and phonological (L1- vs L2-like novel words) familiarity. Participants were trained and tested with a 12-hr intervening period that included overnight sleep or daytime awake. Our results showed (1) benefits of sleep to recognition memory that were greater for words with L2-like phonology and (2) that learned associations with familiar but not unfamiliar pictures enhanced recognition memory for novel words. Implications for complementary systems accounts of word learning are discussed.
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http://dx.doi.org/10.1080/17470218.2017.1329325DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6711762PMC
June 2018

Targeted Memory Reactivation during Sleep Adaptively Promotes the Strengthening or Weakening of Overlapping Memories.

J Neurosci 2017 08 10;37(32):7748-7758. Epub 2017 Jul 10.

Department of Cognition, Development and Educational Psychology, University of Barcelona, 08035 Barcelona, Spain.

System memory consolidation is conceptualized as an active process whereby newly encoded memory representations are strengthened through selective memory reactivation during sleep. However, our learning experience is highly overlapping in content (i.e., shares common elements), and memories of these events are organized in an intricate network of overlapping associated events. It remains to be explored whether and how selective memory reactivation during sleep has an impact on these overlapping memories acquired during awake time. Here, we test in a group of adult women and men the prediction that selective memory reactivation during sleep entails the reactivation of associated events and that this may lead the brain to adaptively regulate whether these associated memories are strengthened or pruned from memory networks on the basis of their relative associative strength with the shared element. Our findings demonstrate the existence of efficient regulatory neural mechanisms governing how complex memory networks are shaped during sleep as a function of their associative memory strength. Numerous studies have demonstrated that system memory consolidation is an active, selective, and sleep-dependent process in which only subsets of new memories become stabilized through their reactivation. However, the learning experience is highly overlapping in content and thus events are encoded in an intricate network of related memories. It remains to be explored whether and how memory reactivation has an impact on overlapping memories acquired during awake time. Here, we show that sleep memory reactivation promotes strengthening and weakening of overlapping memories based on their associative memory strength. These results suggest the existence of an efficient regulatory neural mechanism that avoids the formation of cluttered memory representation of multiple events and promotes stabilization of complex memory networks.
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http://dx.doi.org/10.1523/JNEUROSCI.3537-16.2017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6596642PMC
August 2017

Neuroimaging as a tool to study the sources of phenotypic heterogeneity in Huntington's disease.

Curr Opin Neurol 2017 08;30(4):398-404

aCognition and Brain Plasticity Unit, IDIBELL (Institut d'Investigació Biomèdica de Bellvitge), L'Hospitalet de Llobregat bDepartment of Cognition, Development and Educational Psychology, University of Barcelona cICREA (Catalan Institute for Research and Advanced Studies), Barcelona, Spain.

Purpose Of Review: Huntington's disease is a neurodegenerative disorder characterized by a triad of motor, cognitive and psychiatric disturbances. There is great variability regarding the prominence and evolution of each type of clinical sign. One possible source of phenotypic heterogeneity could be the more prominent degeneration of specific brain circuits. The scope of this review is to highlight the most recent neuroimaging studies that have analysed the relationship between brain changes and motor, cognitive and psychiatric alterations in Huntington's disease.

Recent Findings: The results from recent neuroimaging studies are heterogeneous. Although there is a great overlap between the different regions associated with each symptomatic domain, there is some degree of differentiation. For example, the motor network is associated with motor impairment, whereas the ventral striatum is especially involved in emotional deficits related with psychiatric problems.

Summary: Motor, cognitive and psychiatric impairments are associated with structural and functional brain biomarkers. However, the specificity of the regions involved remains unknown, because these studies focused on specific regions and symptoms. In order to tease apart the neural substrates that underlie the phenotypic heterogeneity in Huntington's disease, multivariate approaches combining brain and behavioural measures related to all symptomatic domains should be considered in the future.
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http://dx.doi.org/10.1097/WCO.0000000000000461DOI Listing
August 2017

Semantic Congruence Accelerates the Onset of the Neural Signals of Successful Memory Encoding.

J Neurosci 2017 01;37(2):291-301

Cognition and Brain Plasticity Group (Bellvitge Biomedical Research Institute) IDIBELL, L'Hospitalet de Llobregat, Barcelona 08908, Spain.

As the stream of experience unfolds, our memory system rapidly transforms current inputs into long-lasting meaningful memories. A putative neural mechanism that strongly influences how input elements are transformed into meaningful memory codes relies on the ability to integrate them with existing structures of knowledge or schemas. However, it is not yet clear whether schema-related integration neural mechanisms occur during online encoding. In the current investigation, we examined the encoding-dependent nature of this phenomenon in humans. We showed that actively integrating words with congruent semantic information provided by a category cue enhances memory for words and increases false recall. The memory effect of such active integration with congruent information was robust, even with an interference task occurring right after each encoding word list. In addition, via electroencephalography, we show in 2 separate studies that the onset of the neural signals of successful encoding appeared early (∼400 ms) during the encoding of congruent words. That the neural signals of successful encoding of congruent and incongruent information followed similarly ∼200 ms later suggests that this earlier neural response contributed to memory formation. We propose that the encoding of events that are congruent with readily available contextual semantics can trigger an accelerated onset of the neural mechanisms, supporting the integration of semantic information with the event input. This faster onset would result in a long-lasting and meaningful memory trace for the event but, at the same time, make it difficult to distinguish it from plausible but never encoded events (i.e., related false memories).

Significance Statement: Conceptual or schema congruence has a strong influence on long-term memory. However, the question of whether schema-related integration neural mechanisms occur during online encoding has yet to be clarified. We investigated the neural mechanisms reflecting how the active integration of words with congruent semantic categories enhances memory for words and increases false recall of semantically related words. We analyzed event-related potentials during encoding and showed that the onset of the neural signals of successful encoding appeared early (∼400 ms) during the encoding of congruent words. Our findings indicate that congruent events can trigger an accelerated onset of neural encoding mechanisms supporting the integration of semantic information with the event input.
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http://dx.doi.org/10.1523/JNEUROSCI.1622-16.2016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6596570PMC
January 2017

COMT Val158Met Polymorphism Modulates Huntington's Disease Progression.

PLoS One 2016;11(9):e0161106. Epub 2016 Sep 22.

INSERM U955, Equipe 01 Neuropsychologie Interventionnelle, 94000, Créteil, France.

Little is known about the genetic factors modulating the progression of Huntington's disease (HD). Dopamine levels are affected in HD and modulate executive functions, the main cognitive disorder of HD. We investigated whether the Val158Met polymorphism of the catechol-O-methyltransferase (COMT) gene, which influences dopamine (DA) degradation, affects clinical progression in HD. We carried out a prospective longitudinal multicenter study from 1994 to 2011, on 438 HD gene carriers at different stages of the disease (34 pre-manifest; 172 stage 1; 130 stage 2; 80 stage 3; 17 stage 4; and 5 stage 5), according to Total Functional Capacity (TFC) score. We used the Unified Huntington's Disease Rating Scale to evaluate motor, cognitive, behavioral and functional decline. We genotyped participants for COMT polymorphism (107 Met-homozygous, 114 Val-homozygous and 217 heterozygous). 367 controls of similar ancestry were also genotyped. We compared clinical progression, on each domain, between groups of COMT polymorphisms, using latent-class mixed models accounting for disease duration and number of CAG (cytosine adenine guanine) repeats. We show that HD gene carriers with fewer CAG repeats and with the Val allele in COMT polymorphism displayed slower cognitive decline. The rate of cognitive decline was greater for Met/Met homozygotes, which displayed a better maintenance of cognitive capacity in earlier stages of the disease, but had a worse performance than Val allele carriers later on. COMT polymorphism did not significantly impact functional and behavioral performance. Since COMT polymorphism influences progression in HD, it could be used for stratification in future clinical trials. Moreover, DA treatments based on the specific COMT polymorphism and adapted according to disease duration could potentially slow HD progression.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5033325PMC
http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0161106PLOS
September 2016

Motivated encoding selectively promotes memory for future inconsequential semantically-related events.

Neurobiol Learn Mem 2016 09 17;133:1-6. Epub 2016 May 17.

Cognition and Brain Plasticity Group [Bellvitge Biomedical Research Institute] IDIBELL, Spain; Department of Cognition, Development and Educational Psychology, Faculty of Psychology, University of Barcelona, Spain; Institute of Neurosciences, University of Barcelona, Spain.

Neurobiological models of long-term memory explain how memory for inconsequential events fades, unless these happen before or after other relevant (i.e., rewarding or aversive) or novel events. Recently, it has been shown in humans that retrospective and prospective memories are selectively enhanced if semantically related events are paired with aversive stimuli. However, it remains unclear whether motivating stimuli, as opposed to aversive, have the same effect in humans. Here, participants performed a three phase incidental encoding task where one semantic category was rewarded during the second phase. A memory test 24h after, but not immediately after encoding, revealed that memory for inconsequential items was selectively enhanced only if items from the same category had been previously, but not subsequently, paired with rewards. This result suggests that prospective memory enhancement of reward-related information requires, like previously reported for aversive memories, of a period of memory consolidation. The current findings provide the first empirical evidence in humans that the effects of motivated encoding are selectively and prospectively prolonged over time.
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http://dx.doi.org/10.1016/j.nlm.2016.05.005DOI Listing
September 2016

Attentional effects on rule extraction and consolidation from speech.

Cognition 2016 07 28;152:61-69. Epub 2016 Mar 28.

Cognition and Brain Plasticity Unit. Bellvitge Research Biomedical Institute (IDIBELL), Hospitalet de Llobregat, 08097, Spain; Department of Basic Psychology, University of Barcelona, Campus Bellvitge, Hospitalet de Llobregat, 08097, Spain; Institució Catalana de Recerca i Estudis Avançats (ICREA), 08010 Barcelona, Spain; Institute of Neurosciences, University of Barcelona, Spain. Electronic address:

Incidental learning plays a crucial role in the initial phases of language acquisition. However the knowledge derived from implicit learning, which is based on prediction-based mechanisms, may become explicit. The role that attention plays in the formation of implicit and explicit knowledge of the learned material is unclear. In the present study, we investigated the role that attention plays in the acquisition of non-adjacent rule learning from speech. In addition, we also tested whether the amount of attention during learning changes the representation of the learned material after a 24h delay containing sleep. For that, we developed an experiment run on two consecutive days consisting on the exposure to an artificial language that contained non-adjacent dependencies (rules) between words whereas different conditions were established to manipulate the amount of attention given to the rules (target and non-target conditions). Furthermore, we used both indirect and direct measures of learning that are more sensitive to implicit and explicit knowledge, respectively. Whereas the indirect measures indicated that learning of the rules occurred regardless of attention, more explicit judgments after learning showed differences in the type of learning reached under the two attention conditions. 24 hours later, indirect measures showed no further improvements during additional language exposure and explicit judgments indicated that only the information more robustly learned in the previous day, was consolidated.
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http://dx.doi.org/10.1016/j.cognition.2016.03.016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4869066PMC
July 2016

Temporal Attention as a Scaffold for Language Development.

Front Psychol 2016 2;7:44. Epub 2016 Feb 2.

Department of Basic Psychology, University of BarcelonaBarcelona, Spain; Department of Basic Psychology, Institute for Brain, Cognition and Behavior (IR3C), University of BarcelonaBarcelona, Spain.

Language is one of the most fascinating abilities that humans possess. Infants demonstrate an amazing repertoire of linguistic abilities from very early on and reach an adult-like form incredibly fast. However, language is not acquired all at once but in an incremental fashion. In this article we propose that the attentional system may be one of the sources for this developmental trajectory in language acquisition. At birth, infants are endowed with an attentional system fully driven by salient stimuli in their environment, such as prosodic information (e.g., rhythm or pitch). Early stages of language acquisition could benefit from this readily available, stimulus-driven attention to simplify the complex speech input and allow word segmentation. At later stages of development, infants are progressively able to selectively attend to specific elements while disregarding others. This attentional ability could allow them to learn distant non-adjacent rules needed for morphosyntactic acquisition. Because non-adjacent dependencies occur at distant moments in time, learning these dependencies may require correctly orienting attention in the temporal domain. Here, we gather evidence uncovering the intimate relationship between the development of attention and language. We aim to provide a novel approach to human development, bridging together temporal attention and language acquisition.
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http://dx.doi.org/10.3389/fpsyg.2016.00044DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4735410PMC
February 2016

Task-specific preparatory neural activations in low-interference contexts.

Brain Struct Funct 2016 11 16;221(8):3997-4006. Epub 2015 Nov 16.

Mind, Brain and Behavior Research Center, University of Granada, 18071, Granada, Spain.

How the brain prepares for forthcoming events is a pivotal question in human neuroscience. In the last years, several studies have suggested that expectations of perceiving upcoming stimuli engage relevant perceptual areas. Similarly, some experiments manipulating the task to be performed with targets have also found pre-activations in task-related brain areas. However, the usual configuration of this type of paradigms entails high levels of interference and/or working memory load, together with a small set of target stimuli. We designed a cued task paradigm in which interference was reduced to a minimum, as evidenced by behavioral indices of performance, and that included a high number of targets to avoid their anticipation. This was achieved using a large set of univalent target stimuli preceded by fully valid cues in a functional magnetic resonance imaging experiment. We found category-specific patterns of activity in which semantic cues engaged the left inferior frontal gyrus whereas spatial cues preactivated the right superior parietal lobe. Together with functional connectivity analyses, the activation maps showed the specific involvement of semantic and spatial processes upon the presentation of the cues that are coherent with previous literature. Our results thus suggest that even in contexts of low interference that prevent the anticipation of specific targets, our brain takes advantage of current information to deal with upcoming demands.
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http://dx.doi.org/10.1007/s00429-015-1141-5DOI Listing
November 2016

Prosodic cues enhance rule learning by changing speech segmentation mechanisms.

Front Psychol 2015 30;6:1478. Epub 2015 Sep 30.

INSERM U955, Equipe 01, Neuropsychologie Interventionnelle, Institut Mondor de Recherche Biomédicale Créteil, France ; Département d'Etudes Cognitives, École Normale Supérieure Paris, France ; Faculté de Médecine, Université Paris-Est Créteil, France ; Assistance Publique-Hôpitaux de Paris, Centre de Référence Maladie de Huntington, Unité de Neurologie Cognitive, Hôpital Henri Mondor-Albert Chenevier Créteil, France.

Prosody has been claimed to have a critical role in the acquisition of grammatical information from speech. The exact mechanisms by which prosodic cues enhance learning are fully unknown. Rules from language often require the extraction of non-adjacent dependencies (e.g., he plays, he sings, he speaks). It has been proposed that pauses enhance learning because they allow computing non-adjacent relations helping word segmentation by removing the need to compute adjacent computations. So far only indirect evidence from behavioral and electrophysiological measures comparing learning effects after exposure to speech with and without pauses support this claim. By recording event-related potentials during the acquisition process of artificial languages with and without pauses between words with embedded non-adjacent rules we provide direct evidence on how the presence of pauses modifies the way speech is processed during learning to enhance segmentation and rule generalization. The electrophysiological results indicate that pauses as short as 25 ms attenuated the N1 component irrespective of whether learning was possible or not. In addition, a P2 enhancement was present only when learning of non-adjacent dependencies was possible. The overall results support the claim that the simple presence of subtle pauses changed the segmentation mechanism used reflected in an exogenously driven N1 component attenuation and improving segmentation at the behavioral level. This effect can be dissociated from the endogenous P2 enhancement that is observed irrespective of the presence of pauses whenever non-adjacent dependencies are learned.
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http://dx.doi.org/10.3389/fpsyg.2015.01478DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4588126PMC
October 2015

Electrical stimulation mapping of nouns and verbs in Broca's area.

Brain Lang 2015 Jun-Jul;145-146:53-63. Epub 2015 May 16.

Cognition and Brain Plasticity Group [Bellvitge Biomedical Research Institute-] IDIBELL, L'Hospitalet de Llobregat, Barcelona 08097, Spain; Dept. of Basic Psychology, Campus Bellvitge, University of Barcelona, L'Hospitalet de Llobregat, Barcelona 08097, Spain; Catalan Institution for Research and Advanced Studies, ICREA, Barcelona, Spain.

Electric stimulation mapping (ESM) is frequently used during brain surgery to localise higher cognitive functions to avoid post-chirurgical disabilities. Experiments with brain imaging techniques and neuropsychological studies showed differences in the cortical representation and processing of nouns and verbs. The goal of the present study was to investigate whether electric stimulation in specific sites in the frontal cortex disrupted noun and verb production selectively. We found that most of the stimulated areas showed disruption of both verbs and nouns at the inferior frontal gyrus. However, when selective effects were obtained, verbs were more prone to disruption than nouns with important individual differences. The overall results indicate that selective impairments can be observed at inferior and middle frontal regions and the action naming task seems to be more suitable to avoid post-chirurgical language disabilities, as it shows a greater sensitivity to disruption with ESM than the classical object naming task.
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http://dx.doi.org/10.1016/j.bandl.2015.04.005DOI Listing
September 2015

Morphological derivation overflow as a result of disruption of the left frontal aslant white matter tract.

Brain Lang 2015 Mar 3;142:54-64. Epub 2015 Feb 3.

Cognition and Brain Plasticity Group [Bellvitge Biomedical Research Institute - IDIBELL], 08097 L'Hospitalet de Llobregat, Barcelona, Spain; Dept. of Basic Psychology, Campus Bellvitge, University of Barcelona, 08097 L'Hospitalet de Llobregat, Barcelona, Spain; Catalan Institution for Research and Advanced Studies, ICREA, 08010 Barcelona, Spain. Electronic address:

The frontal aslant tract (FAT) is a recently described major connection between the preSMA and Broca's area, whose functional role remains undefined. In this study we examined a patient presenting a morphological overregularization strategy in a verb generation task during awake surgery. This specific language deficit coincided with brain tumor resection at the level of the left FAT. During the task execution the patient formed the non-existent verbs by applying a morphological derivation rule to the given nouns, instead of retrieving the appropriate verbs. DTI results confirmed left FAT damage. Neuropsychological follow-up showed that this morphological derivation impairment partially persisted after surgery, whereas the results on a wide spectrum of other language-related tasks remained satisfactory. Additionally, we compared the pre- and the post-operational fMRI activation maps for the same verb generation task. We discuss the potential role of the left FAT in the morphological derivation process and in lexical retrieval.
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http://dx.doi.org/10.1016/j.bandl.2015.01.005DOI Listing
March 2015

Multiple brain networks underpinning word learning from fluent speech revealed by independent component analysis.

Neuroimage 2015 Apr 22;110:182-93. Epub 2015 Jan 22.

Cognition and Brain Plasticity Unit, Bellvitge Research Biomedical Institute (IDIBELL), Hospitalet de Llobregat, 08907 Barcelona, Spain; Dept. of Basic Psychology, University of Barcelona, 08035 Barcelona, Spain; Ecole Normale Superieure, Departement d'Etudes Cognitives, Paris, France; Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain.

Although neuroimaging studies using standard subtraction-based analysis from functional magnetic resonance imaging (fMRI) have suggested that frontal and temporal regions are involved in word learning from fluent speech, the possible contribution of different brain networks during this type of learning is still largely unknown. Indeed, univariate fMRI analyses cannot identify the full extent of distributed networks that are engaged by a complex task such as word learning. Here we used Independent Component Analysis (ICA) to characterize the different brain networks subserving word learning from an artificial language speech stream. Results were replicated in a second cohort of participants with a different linguistic background. Four spatially independent networks were associated with the task in both cohorts: (i) a dorsal Auditory-Premotor network; (ii) a dorsal Sensory-Motor network; (iii) a dorsal Fronto-Parietal network; and (iv) a ventral Fronto-Temporal network. The level of engagement of these networks varied through the learning period with only the dorsal Auditory-Premotor network being engaged across all blocks. In addition, the connectivity strength of this network in the second block of the learning phase correlated with the individual variability in word learning performance. These findings suggest that: (i) word learning relies on segregated connectivity patterns involving dorsal and ventral networks; and (ii) specifically, the dorsal auditory-premotor network connectivity strength is directly correlated with word learning performance.
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http://dx.doi.org/10.1016/j.neuroimage.2014.12.085DOI Listing
April 2015

Speaker's hand gestures modulate speech perception through phase resetting of ongoing neural oscillations.

Cortex 2015 Jul 20;68:76-85. Epub 2014 Dec 20.

Multisensory Research Group, Center for Brain and Cognition, Universitat Pompeu Fabra, Barcelona, Spain; Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain. Electronic address:

Speakers often accompany speech with spontaneous beat gestures in natural spoken communication. These gestures are usually aligned with lexical stress and can modulate the saliency of their affiliate words. Here we addressed the consequences of beat gestures on the neural correlates of speech perception. Previous studies have highlighted the role played by theta oscillations in temporal prediction of speech. We hypothesized that the sight of beat gestures may influence ongoing low-frequency neural oscillations around the onset of the corresponding words. Electroencephalographic (EEG) recordings were acquired while participants watched a continuous, naturally recorded discourse. The phase-locking value (PLV) at word onset was calculated from the EEG from pairs of identical words that had been pronounced with and without a concurrent beat gesture in the discourse. We observed an increase in PLV in the 5-6 Hz theta range as well as a desynchronization in the 8-10 Hz alpha band around the onset of words preceded by a beat gesture. These findings suggest that beats help tune low-frequency oscillatory activity at relevant moments during natural speech perception, providing a new insight of how speech and paralinguistic information are integrated.
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http://dx.doi.org/10.1016/j.cortex.2014.11.018DOI Listing
July 2015

ERP evidence of adaptive changes in error processing and attentional control during rhythm synchronization learning.

Neuroimage 2014 Oct 21;100:460-70. Epub 2014 Jun 21.

Cognition and Brain Plasticity Group, Bellvitge Biomedical Research Institute (IDIBELL), Spain; Department of Basic Psychology, University of Barcelona, Spain; Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain. Electronic address:

The ability to detect and use information from errors is essential during the acquisition of new skills. There is now a wealth of evidence about the brain mechanisms involved in error processing. However, the extent to which those mechanisms are engaged during the acquisition of new motor skills remains elusive. Here we examined rhythm synchronization learning across 12 blocks of practice in musically naïve individuals and tracked changes in ERP signals associated with error-monitoring and error-awareness across distinct learning stages. Synchronization performance improved with practice, and performance improvements were accompanied by dynamic changes in ERP components related to error-monitoring and error-awareness. Early in learning, when performance was poor and the internal representations of the rhythms were weaker we observed a larger error-related negativity (ERN) following errors compared to later learning. The larger ERN during early learning likely results from greater conflict between competing motor responses, leading to greater engagement of medial-frontal conflict monitoring processes and attentional control. Later in learning, when performance had improved, we observed a smaller ERN accompanied by an enhancement of a centroparietal positive component resembling the P3. This centroparietal positive component was predictive of participant's performance accuracy, suggesting a relation between error saliency, error awareness and the consolidation of internal templates of the practiced rhythms. Moreover, we showed that during rhythm learning errors led to larger auditory evoked responses related to attention orientation which were triggered automatically and which were independent of the learning stage. The present study provides crucial new information about how the electrophysiological signatures related to error-monitoring and error-awareness change during the acquisition of new skills, extending previous work on error processing and cognitive control mechanisms to a more ecologically valid context.
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http://dx.doi.org/10.1016/j.neuroimage.2014.06.034DOI Listing
October 2014

Atypical language organization in temporal lobe epilepsy revealed by a passive semantic paradigm.

BMC Neurol 2014 May 6;14:98. Epub 2014 May 6.

Cognition and Brain Plasticity Group [Bellvitge Biomedical Research Institute]- IDIBELL, L'Hospitalet de Llobregat, Barcelona 08907, Spain.

Background: Mesial temporal lobe epilepsy (MTLE) is the most common type of focal epilepsy in adults and can be successfully cured by surgery. One of the main complications of this surgery however is a decline in language abilities. The magnitude of this decline is related to the degree of language lateralization to the left hemisphere. Most fMRI paradigms used to determine language dominance in epileptic populations have used active language tasks. Sometimes, these paradigms are too complex and may result in patient underperformance. Only a few studies have used purely passive tasks, such as listening to standard speech.

Methods: In the present study we characterized language lateralization in patients with MTLE using a rapid and passive semantic language task. We used functional magnetic resonance imaging (fMRI) to study 23 patients [12 with Left (LMTLE), 11 with Right mesial temporal lobe epilepsy (RMTLE)] and 19 healthy right-handed controls using a 6 minute long semantic task in which subjects passively listened to groups of sentences (SEN) and pseudo sentences (PSEN). A lateralization index (LI) was computed using a priori regions of interest of the temporal lobe.

Results: The LI for the significant contrasts produced activations for all participants in both temporal lobes. 81.8% of RMTLE patients and 79% of healthy individuals had a bilateral language representation for this particular task. However, 50% of LMTLE patients presented an atypical right hemispheric dominance in the LI. More importantly, the degree of right lateralization in LMTLE patients was correlated with the age of epilepsy onset.

Conclusions: The simple, rapid, non-collaboration dependent, passive task described in this study, produces a robust activation in the temporal lobe in both patients and controls and is capable of illustrating a pattern of atypical language organization for LMTLE patients. Furthermore, we observed that the atypical right-lateralization patterns in LMTLE patients was associated to earlier age at epilepsy onset. These results are in line with the idea that early onset of epileptic activity is associated to larger neuroplastic changes.
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http://dx.doi.org/10.1186/1471-2377-14-98DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4017227PMC
May 2014