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Hoeksema, N., Verga, L., Mengede, J., Van Roessel, C., Villanueva, S., Salazar-Casals, A., Rubio-Garcia, A., Curcic-Blake, B., Vernes, S. C., & Ravignani, A. (2021). Neuroanatomy of the grey seal brain: Bringing pinnipeds into the neurobiological study of vocal learning. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences, 376: 20200252. doi:10.1098/rstb.2020.0252.
Abstract
Comparative studies of vocal learning and vocal non-learning animals can increase our understanding of the neurobiology and evolution of vocal learning and human speech. Mammalian vocal learning is understudied: most research has either focused on vocal learning in songbirds or its absence in non-human primates. Here we focus on a highly promising model species for the neurobiology of vocal learning: grey seals. We provide a neuroanatomical atlas (based on dissected brain slices and magnetic resonance images), a labelled MRI template, a 3D model with volumetric measurements of brain regions, and histological cortical stainings. Four main features of the grey seal brain stand out. (1) It is relatively big and highly convoluted. (2) It hosts a relatively large temporal lobe and cerebellum, structures which could support developed timing abilities and acoustic processing. (3) The cortex is similar to humans in thickness and shows the expected six-layered mammalian structure. (4) Expression of FoxP2 - a gene involved in vocal learning and spoken language - is present in deeper layers of the cortex. Our results could facilitate future studies targeting the neural and genetic underpinnings of mammalian vocal learning, thus bridging the research gap from songbirds to humans and non-human primates.Competing Interest StatementThe authors have declared no competing interest. -
Varola*, M., Verga*, L., Sroka, M., Villanueva, S., Charrier, I., & Ravignani, A. (2021). Can harbor seals (Phoca vitulina) discriminate familiar conspecific calls after long periods of separation? PeerJ, 9: e12431. doi:10.7717/peerj.12431.
Abstract
* - indicates joint first authorship -
The ability to discriminate between familiar and unfamiliar calls may play a key role in pinnipeds’ communication and survival, as in the case of mother-pup interactions. Vocal discrimination abilities have been suggested to be more developed in pinniped species with the highest selective pressure such as the otariids; yet, in some group-living phocids, such as harbor seals (Phoca vitulina), mothers are also able to recognize their pup’s voice. Conspecifics’ vocal recognition in pups has never been investigated; however, the repeated interaction occurring between pups within the breeding season suggests that long-term vocal discrimination may occur. Here we explored this hypothesis by presenting three rehabilitated seal pups with playbacks of vocalizations from unfamiliar or familiar pups. It is uncommon for seals to come into rehabilitation for a second time in their lifespan, and this study took advantage of these rare cases. A simple visual inspection of the data plots seemed to show more reactions, and of longer duration, in response to familiar as compared to unfamiliar playbacks in two out of three pups. However, statistical analyses revealed no significant difference between the experimental conditions. We also found no significant asymmetry in orientation (left vs. right) towards familiar and unfamiliar sounds. While statistics do not support the hypothesis of an established ability to discriminate familiar vocalizations from unfamiliar ones in harbor seal pups, further investigations with a larger sample size are needed to confirm or refute this hypothesis.Additional information
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Verga, L., & Ravignani, A. (2021). Strange seal sounds: Claps, slaps, and multimodal pinniped rhythms. Frontiers in Ecology and Evolution, 9: 644497. doi:10.3389/fevo.2021.644497.
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Verga, L., Schwartze, M., Stapert, S., Winkens, I., & Kotz, S. A. (2021). Dysfunctional timing in traumatic brain injury patients: Co-occurrence of cognitive, motor, and perceptual deficits. Frontiers in Psychology, 12: 731898. doi:10.3389/fpsyg.2021.731898.
Abstract
Timing is an essential part of human cognition and of everyday life activities, such as walking or holding a conversation. Previous studies showed that traumatic brain injury (TBI) often affects cognitive functions such as processing speed and time-sensitive abilities, causing long-term sequelae as well as daily impairments. However, the existing evidence on timing capacities in TBI is mostly limited to perception and the processing of isolated intervals. It is therefore open whether the observed deficits extend to motor timing and to continuous dynamic tasks that more closely match daily life activities. The current study set out to answer these questions by assessing audio motor timing abilities and their relationship with cognitive functioning in a group of TBI patients (n=15) and healthy matched controls. We employed a comprehensive set of tasks aiming at testing timing abilities across perception and production and from single intervals to continuous auditory sequences. In line with previous research, we report functional impairments in TBI patients concerning cognitive processing speed and perceptual timing. Critically, these deficits extended to motor timing: The ability to adjust to tempo changes in an auditory pacing sequence was impaired in TBI patients, and this motor timing deficit covaried with measures of processing speed. These findings confirm previous evidence on perceptual and cognitive timing deficits resulting from TBI and provide first evidence for comparable deficits in motor behavior. This suggests basic co-occurring perceptual and motor timing impairments that may factor into a wide range of daily activities. Our results thus place TBI into the wider range of pathologies with well-documented timing deficits (such as Parkinson’s disease) and encourage the search for novel timing-based therapeutic interventions (e.g., employing dynamic and/or musical stimuli) with high transfer potential to everyday life activities.Additional information
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Galbiati, A., Verga, L., Giora, E., Zucconi, M., & Ferini-Strambi, L. (2019). The risk of neurodegeneration in REM sleep behavior disorder: A systematic review and meta-analysis of longitudinal studies. Sleep Medicine Reviews, 43, 37-46. doi:10.1016/j.smrv.2018.09.008.
Abstract
Several studies report an association between REM Sleep Behavior Disorder (RBD) and neurodegenerative diseases, in particular synucleinopathies. Interestingly, the onset of RBD precedes the development of neurodegeneration by several years. This review and meta-analysis aims to establish the rate of conversion of RBD into neurodegenerative diseases. Longitudinal studies were searched from the PubMed, Web of Science, and SCOPUS databases. Using random-effect modeling, we performed a meta-analysis on the rate of RBD conversions into neurodegeneration. Furthermore, we fitted a Kaplan-Meier analysis and compared the differences between survival curves of different diseases with log-rank tests. The risk for developing neurodegenerative diseases was 33.5% at five years follow-up, 82.4% at 10.5 years and 96.6% at 14 years. The average conversion rate was 31.95% after a mean duration of follow-up of 4.75 ± 2.43 years. The majority of RBD patients converted to Parkinson's Disease (43%), followed by Dementia with Lewy Bodies (25%). The estimated risk for RBD patients to develop a neurodegenerative disease over a long-term follow-up is more than 90%. Future studies should include control group for the evaluation of REM sleep without atonia as marker for neurodegeneration also in non-clinical population and target RBD as precursor of neurodegeneration to develop protective trials. -
Ravignani, A., Verga, L., & Greenfield, M. D. (2019). Interactive rhythms across species: The evolutionary biology of animal chorusing and turn-taking. Annals of the New York Academy of Sciences, 1453(1), 12-21. doi:10.1111/nyas.14230.
Abstract
The study of human language is progressively moving toward comparative and interactive frameworks, extending the concept of turn‐taking to animal communication. While such an endeavor will help us understand the interactive origins of language, any theoretical account for cross‐species turn‐taking should consider three key points. First, animal turn‐taking must incorporate biological studies on animal chorusing, namely how different species coordinate their signals over time. Second, while concepts employed in human communication and turn‐taking, such as intentionality, are still debated in animal behavior, lower level mechanisms with clear neurobiological bases can explain much of animal interactive behavior. Third, social behavior, interactivity, and cooperation can be orthogonal, and the alternation of animal signals need not be cooperative. Considering turn‐taking a subset of chorusing in the rhythmic dimension may avoid overinterpretation and enhance the comparability of future empirical work. -
Verga, L., & Kotz, S. A. (2019). Putting language back into ecological communication contexts. Language, Cognition and Neuroscience, 34(4), 536-544. doi:10.1080/23273798.2018.1506886.
Abstract
Language is a multi-faceted form of communication. It is not until recently though that language research moved on from simple stimuli and protocols toward a more ecologically valid approach, namely “shifting” from words and simple sentences to stories with varying degrees of contextual complexity. While much needed, the use of ecologically valid stimuli such as stories should also be explored in interactive rather than individualistic experimental settings leading the way to an interactive neuroscience of language. Indeed, mounting evidence suggests that cognitive processes and their underlying neural activity significantly differ between social and individual experiences. We aim at reviewing evidence, which indicates that the characteristics of linguistic and extra-linguistic contexts may significantly influence communication–including spoken language comprehension. In doing so, we provide evidence on the use of new paradigms and methodological advancements that may enable the study of complex language features in a truly interactive, ecological way. -
Verga, L., & Kotz, S. A. (2019). Spatial attention underpins social word learning in the right fronto-parietal network. NeuroImage, 195, 165-173. doi:10.1016/j.neuroimage.2019.03.071.
Abstract
In a multi- and inter-cultural world, we daily encounter new words. Adult learners often rely on a situational context to learn and understand a new word's meaning. Here, we explored whether interactive learning facilitates word learning by directing the learner's attention to a correct new word referent when a situational context is non-informative. We predicted larger involvement of inferior parietal, frontal, and visual cortices involved in visuo-spatial attention during interactive learning. We scanned participants while they played a visual word learning game with and without a social partner. As hypothesized, interactive learning enhanced activity in the right Supramarginal Gyrus when the situational context provided little information. Activity in the right Inferior Frontal Gyrus during interactive learning correlated with post-scanning behavioral test scores, while these scores correlated with activity in the Fusiform Gyrus in the non-interactive group. These results indicate that attention is involved in interactive learning when the situational context is minimal and suggest that individual learning processes may be largely different from interactive ones. As such, they challenge the ecological validity of what we know about individual learning and advocate the exploration of interactive learning in naturalistic settings. -
Dalla Bella, S., Farrugia, F., Benoit, C.-E., Begel, V., Verga, L., Harding, E., & Kotz, S. A. (2017). BAASTA: Battery for the Assessment of Auditory Sensorimotor and Timing Abilities. Behavior Research Methods, 49(3), 1128-1145. doi:10.3758/s13428-016-0773-6.
Abstract
The Battery for the Assessment of Auditory Sensorimotor and Timing Abilities (BAASTA) is a new tool for the systematic assessment of perceptual and sensorimotor timing skills. It spans a broad range of timing skills aimed at differentiating individual timing profiles. BAASTA consists of sensitive time perception and production tasks. Perceptual tasks include duration discrimination, anisochrony detection (with tones and music), and a version of the Beat Alignment Task. Perceptual thresholds for duration discrimination and anisochrony detection are estimated with a maximum likelihood procedure (MLP) algorithm. Production tasks use finger tapping and include unpaced and paced tapping (with tones and music), synchronization-continuation, and adaptive tapping to a sequence with a tempo change. BAASTA was tested in a proof-of-concept study with 20 non-musicians (Experiment 1). To validate the results of the MLP procedure, less widespread than standard staircase methods, three perceptual tasks of the battery (duration discrimination, anisochrony detection with tones, and with music) were further tested in a second group of non-musicians using 2 down / 1 up and 3 down / 1 up staircase paradigms (n = 24) (Experiment 2). The results show that the timing profiles provided by BAASTA allow to detect cases of timing/rhythm disorders. In addition, perceptual thresholds yielded by the MLP algorithm, although generally comparable to the results provided by standard staircase, tend to be slightly lower. In sum, BAASTA provides a comprehensive battery to test perceptual and sensorimotor timing skills, and to detect timing/rhythm deficits. -
Verga, L., & Kotz, S. A. (2017). Help me if I can't: Social interaction effects in adult contextual word learning. Cognition, 168, 76-90. doi:10.1016/j.cognition.2017.06.018.
Abstract
A major challenge in second language acquisition is to build up new vocabulary. How is it possible to identify the meaning of a new word among several possible referents? Adult learners typically use contextual information, which reduces the number of possible referents a new word can have. Alternatively, a social partner may facilitate word learning by directing the learner’s attention toward the correct new word meaning. While much is known about the role of this form of ‘joint attention’ in first language acquisition, little is known about its efficacy in second language acquisition. Consequently, we introduce and validate a novel visual word learning game to evaluate how joint attention affects the contextual learning of new words in a second language. Adult learners either acquired new words in a constant or variable sentence context by playing the game with a knowledgeable partner, or by playing the game alone on a computer. Results clearly show that participants who learned new words in social interaction (i) are faster in identifying a correct new word referent in variable sentence contexts, and (ii) temporally coordinate their behavior with a social partner. Testing the learned words in a post-learning recall or recognition task showed that participants, who learned interactively, better recognized words originally learned in a variable context. While this result may suggest that interactive learning facilitates the allocation of attention to a target referent, the differences in the performance during recognition and recall call for further studies investigating the effect of social interaction on learning performance. In summary, we provide first evidence on the role joint attention in second language learning. Furthermore, the new interactive learning game offers itself to further testing in complex neuroimaging research, where the lack of appropriate experimental set-ups has so far limited the investigation of the neural basis of adult word learning in social interaction.
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