Publications by authors named "Massimo Lumaca"

13 Publications

  • Page 1 of 1

Network Analysis of Human Brain Connectivity Reveals Neural Fingerprints of a Compositionality Bias in Signaling Systems.

Cereb Cortex 2021 Sep 2. Epub 2021 Sep 2.

Language Acquisition and Language Processing Lab, Department of Language and Literature, Norwegian University of Science and Technology, 7941 Trondheim, Norway.

Compositionality is a hallmark of human language and other symbolic systems: a finite set of meaningful elements can be systematically combined to convey an open-ended array of ideas. Compositionality is not uniformly distributed over expressions in a language or over individuals' communicative behavior: at both levels, variation is observed. Here, we investigate the neural bases of interindividual variability by probing the relationship between intrinsic characteristics of brain networks and compositional behavior. We first collected functional resting-state and diffusion magnetic resonance imaging data from a large participant sample (N = 51). Subsequently, participants took part in two signaling games. They were instructed to learn and reproduce an auditory symbolic system of signals (tone sequences) associated with affective meanings (human faces expressing emotions). Signal-meaning mappings were artificial and had to be learned via repeated signaling interactions. We identified a temporoparietal network in which connection length was related to the degree of compositionality introduced in a signaling system by each player. Graph-theoretic analysis of resting-state functional connectivity revealed that, within that network, compositional behavior was associated with integration measures in 2 semantic hubs: the left posterior cingulate cortex and the left angular gyrus. Our findings link individual variability in compositional biases to variation in the anatomy of semantic networks and in the functional topology of their constituent units.
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http://dx.doi.org/10.1093/cercor/bhab307DOI Listing
September 2021

White matter variability in auditory callosal pathways contributes to variation in the cultural transmission of auditory symbolic systems.

Brain Struct Funct 2021 Jul 29;226(6):1943-1959. Epub 2021 May 29.

Center for Music in the Brain, Department of Clinical Medicine, Aarhus University and The Royal Academy of Music, Aarhus/Aalborg, 8000, Aarhus C, Denmark.

The cultural transmission of spoken language and music relies on human capacities for encoding and recalling auditory patterns. In this experiment, we show that interindividual differences in this ability are associated with variation in the organization of cross-callosal white matter pathways. First, high-angular resolution diffusion MRI (dMRI) data were analyzed in a large participant sample (N = 51). Subsequently, these participants underwent a behavioral test that models in the laboratory the cultural transmission of auditory symbolic systems: the signaling game. Cross-callosal and intrahemispheric (arcuate fasciculus) pathways were reconstructed and analyzed using conventional diffusion tensor imaging (DTI) as well as a more advanced dMRI technique: fixel-based analysis (FBA). The DTI metric of fractional anisotropy (FA) in auditory callosal pathways predicted-weeks after scanning-the fidelity of transmission of an artificial tone system. The ability to coherently transmit auditory signals in one signaling game, irrespective of the signals learned during the previous game, was predicted by morphological properties of the fiber bundles in the most anterior portions of the corpus callosum. The current study is the first application of dMRI in the field of cultural transmission, and the first to connect individual characteristics of callosal pathways to core behaviors in the transmission of auditory symbolic systems.
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http://dx.doi.org/10.1007/s00429-021-02302-yDOI Listing
July 2021

Extracting human cortical responses to sound onsets and acoustic feature changes in real music, and their relation to event rate.

Brain Res 2021 03 6;1754:147248. Epub 2021 Jan 6.

Center for Music in the Brain, Department of Clinical Medicine, Aarhus University & The Royal Academy of Music, Aarhus/Aalborg, Denmark; Department of Education, Psychology, Communication, University of Bari Aldo Moro, Italy. Electronic address:

Evoked cortical responses (ERs) have mainly been studied in controlled experiments using simplified stimuli. Though, an outstanding question is how the human cortex responds to the complex stimuli encountered in realistic situations. Few electroencephalography (EEG) studies have used Music Information Retrieval (MIR) tools to extract cortical P1/N1/P2 to acoustical changes in real music. However, less than ten events per music piece could be detected leading to ERs due to limitations in automatic detection of sound onsets. Also, the factors influencing a successful extraction of the ERs have not been identified. Finally, previous studies did not localize the sources of the cortical generators. This study is based on an EEG/MEG dataset from 48 healthy normal hearing participants listening to three real music pieces. Acoustic features were computed from the audio signal of the music with the MIR Toolbox. To overcome limits in automatic methods, sound onsets were also manually detected. The chance of obtaining detectable ERs based on ten randomly picked onset points was less than 1:10,000. For the first time, we show that naturalistic P1/N1/P2 ERs can be reliably measured across 100 manually identified sound onsets, substantially improving the signal-to-noise level compared to <10 trials. More ERs were measurable in musical sections with slow event rates (0.2 Hz-2.5 Hz) than with fast event rates (>2.5 Hz). Furthermore, during monophonic sections of the music only P1/P2 were measurable, and during polyphonic sections only N1. Finally, MEG source analysis revealed that naturalistic P2 is located in core areas of the auditory cortex.
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http://dx.doi.org/10.1016/j.brainres.2020.147248DOI Listing
March 2021

Perceptual learning of tone patterns changes the effective connectivity between Heschl's gyrus and planum temporale.

Hum Brain Mapp 2021 03 4;42(4):941-952. Epub 2020 Nov 4.

Center for Music in the Brain, Department of Clinical Medicine, Aarhus University and The Royal Academy of Music Aarhus/Aalborg, Aarhus, Denmark.

Learning of complex auditory sequences such as music can be thought of as optimizing an internal model of regularities through unpredicted events (or "prediction errors"). We used dynamic causal modeling (DCM) and parametric empirical Bayes on functional magnetic resonance imaging (fMRI) data to identify modulation of effective brain connectivity that takes place during perceptual learning of complex tone patterns. Our approach differs from previous studies in two aspects. First, we used a complex oddball paradigm based on tone patterns as opposed to simple deviant tones. Second, the use of fMRI allowed us to identify cortical regions with high spatial accuracy. These regions served as empirical regions-of-interest for the analysis of effective connectivity. Deviant patterns induced an increased blood oxygenation level-dependent response, compared to standards, in early auditory (Heschl's gyrus [HG]) and association auditory areas (planum temporale [PT]) bilaterally. Within this network, we found a left-lateralized increase in feedforward connectivity from HG to PT during deviant responses and an increase in excitation within left HG. In contrast to previous findings, we did not find frontal activity, nor did we find modulations of backward connections in response to oddball sounds. Our results suggest that complex auditory prediction errors are encoded by changes in feedforward and intrinsic connections, confined to superior temporal gyrus.
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http://dx.doi.org/10.1002/hbm.25269DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7856650PMC
March 2021

Functional connectivity in human auditory networks and the origins of variation in the transmission of musical systems.

Elife 2019 10 29;8. Epub 2019 Oct 29.

Language Acquisition and Language Processing Lab, Department of Language and Literature, Norwegian University of Science and Technology, Trondheim, Norway.

Music producers, whether original composers or performers, vary in their ability to acquire and faithfully transmit music. This form of variation may serve as a mechanism for the emergence of new traits in musical systems. In this study, we aim to investigate whether individual differences in the social learning and transmission of music relate to intrinsic neural dynamics of auditory processing systems. We combined auditory and resting-state functional magnetic resonance imaging (fMRI) with an interactive laboratory model of cultural transmission, the signaling game, in an experiment with a large cohort of participants (N=51). We found that the degree of interhemispheric rs-FC within fronto-temporal auditory networks predicts-weeks after scanning-learning, transmission, and structural modification of an artificial tone system. Our study introduces neuroimaging in cultural transmission research and points to specific neural auditory processing mechanisms that constrain and drive variation in the cultural transmission and regularization of musical systems.
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http://dx.doi.org/10.7554/eLife.48710DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6819097PMC
October 2019

Weighting of neural prediction error by rhythmic complexity: A predictive coding account using mismatch negativity.

Eur J Neurosci 2019 06 20;49(12):1597-1609. Epub 2019 Jan 20.

Department of Clinical Medicine, Center for Music in the Brain, Aarhus University & The Royal Academy of Music, Aarhus C, Denmark.

The human brain's ability to extract and encode temporal regularities and to predict the timing of upcoming events is critical for music and speech perception. This work addresses how these mechanisms deal with different levels of temporal complexity, here the number of distinct durations in rhythmic patterns. We use electroencephalography (EEG) to relate the mismatch negativity (MMN), a proxy of neural prediction error, to a measure of information content of rhythmic sequences, the Shannon entropy. Within each of three conditions, participants listened to repeatedly presented standard rhythms of five tones (four inter-onset intervals) and of a given level of entropy: zero (isochronous), medium entropy (two distinct interval durations), or high entropy (four distinct interval durations). Occasionally, the fourth tone was moved forward in time that is it occurred 100 ms (small deviation) or 300 ms early (large deviation). According to the predictive coding framework, high-entropy stimuli are more difficult to model for the brain, resulting in less confident predictions and yielding smaller prediction errors for deviant sounds. Our results support this hypothesis, showing a gradual decrease in MMN amplitude as a function of entropy, but only for small timing deviants. For large timing deviants, in contrast, a modulation of activity in the opposite direction was observed for the earlier N1 component, known to also be sensitive to sudden changes in directed attention. Our results suggest the existence of a fine-grained neural mechanism that weights neural prediction error to the complexity of rhythms and that mostly manifests in the absence of directed attention.
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http://dx.doi.org/10.1111/ejn.14329DOI Listing
June 2019

Why Do Durations in Musical Rhythms Conform to Small Integer Ratios?

Front Comput Neurosci 2018 28;12:86. Epub 2018 Nov 28.

Department of Clinical Medicine, Center for Music in the Brain, Aarhus University, Aarhus, Denmark.

One curious aspect of human timing is the organization of rhythmic patterns in small integer ratios. Behavioral and neural research has shown that adjacent time intervals in rhythms tend to be perceived and reproduced as approximate fractions of small numbers (e.g., 3/2). Recent work on iterated learning and reproduction further supports this: given a randomly timed drum pattern to reproduce, participants subconsciously transform it toward small integer ratios. The mechanisms accounting for this "attractor" phenomenon are little understood, but might be explained by combining two theoretical frameworks from psychophysics. The scalar expectancy theory describes time interval perception and reproduction in terms of Weber's law: just detectable durational differences equal a constant fraction of the reference duration. The notion of categorical perception emphasizes the tendency to perceive time intervals in categories, i.e., "short" vs. "long." In this piece, we put forward the hypothesis that the integer-ratio bias in rhythm perception and production might arise from the interaction of the scalar property of timing with the categorical perception of time intervals, and that neurally it can plausibly be related to oscillatory activity. We support our integrative approach with mathematical derivations to formalize assumptions and provide testable predictions. We present equations to calculate durational ratios by: (i) parameterizing the relationship between durational categories, (ii) assuming a scalar timing constant, and (iii) specifying one (of K) category of ratios. Our derivations provide the basis for future computational, behavioral, and neurophysiological work to test our model.
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http://dx.doi.org/10.3389/fncom.2018.00086DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6282044PMC
November 2018

From random to regular: neural constraints on the emergence of isochronous rhythm during cultural transmission.

Soc Cogn Affect Neurosci 2018 09;13(8):877-888

SISSA International School for Advanced Studies, 34136 Trieste, Italy.

A core design feature of human communication systems and expressive behaviours is their temporal organization. The cultural evolutionary origins of this feature remain unclear. Here, we test the hypothesis that regularities in the temporal organization of signalling sequences arise in the course of cultural transmission as adaptations to aspects of cortical function. We conducted two experiments on the transmission of rhythms associated with affective meanings, focusing on one of the most widespread forms of regularity in language and music: isochronicity. In the first experiment, we investigated how isochronous rhythmic regularities emerge and change in multigenerational signalling games, where the receiver (learner) in a game becomes the sender (transmitter) in the next game. We show that signalling sequences tend to become rhythmically more isochronous as they are transmitted across generations. In the second experiment, we combined electroencephalography (EEG) and two-player signalling games over 2 successive days. We show that rhythmic regularization of sequences can be predicted based on the latencies of the mismatch negativity response in a temporal oddball paradigm. These results suggest that forms of isochronicity in communication systems originate in neural constraints on information processing, which may be expressed and amplified in the course of cultural transmission.
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http://dx.doi.org/10.1093/scan/nsy054DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6123518PMC
September 2018

Music Evolution in the Laboratory: Cultural Transmission Meets Neurophysiology.

Front Neurosci 2018 16;12:246. Epub 2018 Apr 16.

Language Acquisition and Language Processing Lab, Department of Language and Literature, Norwegian University of Science and Technology, Trondheim, Norway.

In recent years, there has been renewed interest in the biological and cultural evolution of music, and specifically in the role played by perceptual and cognitive factors in shaping core features of musical systems, such as melody, harmony, and rhythm. One proposal originates in the language sciences. It holds that aspects of musical systems evolve by adapting gradually, in the course of successive generations, to the structural and functional characteristics of the sensory and memory systems of learners and "users" of music. This hypothesis has found initial support in laboratory experiments on music transmission. In this article, we first review some of the most important theoretical and empirical contributions to the field of music evolution. Next, we identify a major current limitation of these studies, i.e., the lack of direct support for the hypothesis of cognitive adaptation. Finally, we discuss a recent experiment in which this issue was addressed by using event-related potentials (ERPs). We suggest that the introduction of neurophysiology in cultural transmission research may provide novel insights on the micro-evolutionary origins of forms of variation observed in cultural systems.
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http://dx.doi.org/10.3389/fnins.2018.00246DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5911491PMC
April 2018

Signaling Games and the Evolution of Structure in Language and Music: A Reply to Ravignani and Verhoef (2018) .

Artif Life 2018 17;24(2):154-156. Epub 2018 Apr 17.

Language Acquisition and Language Processing Lab, Department of Language and Literature, Norwegian University of Science and Technology.

In their commentary on our work, Ravignani and Verhoef (2018) raise concerns about two methodological aspects of our experimental paradigm (the signaling game): (1) the use of melodic signals of fixed length and duration, and (2) the fact that signals are endowed with meaning. They argue that music is hardly a semantic system and that our methodological choices may limit the capacity of our paradigm to shed light on the emergence and evolution of a number of putative musical universals. We reply that musical systems are semantic systems and that the aim of our research is not to study musical universals as such, but to compare more closely the kinds of principles that organize meaning and structure in linguistic and musical systems.
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http://dx.doi.org/10.1162/artl_a_00258DOI Listing
June 2019

Cultural Transmission and Evolution of Melodic Structures in Multi-generational Signaling Games.

Artif Life 2017 ;23(3):406-423

SISSA International School for Advanced Studies.

It has been proposed that languages evolve by adapting to the perceptual and cognitive constraints of the human brain, developing, in the course of cultural transmission, structural regularities that maximize or optimize learnability and ease of processing. To what extent would perceptual and cognitive constraints similarly affect the evolution of musical systems? We conducted an experiment on the cultural evolution of artificial melodic systems, using multi-generational signaling games as a laboratory model of cultural transmission. Signaling systems, using five-tone sequences as signals, and basic and compound emotions as meanings, were transmitted from senders to receivers along diffusion chains in which the receiver in each game became the sender in the next game. During transmission, structural regularities accumulated in the signaling systems, following principles of proximity, symmetry, and good continuation. Although the compositionality of signaling systems did not increase significantly across generations, we did observe a significant increase in similarity among signals from the same set. We suggest that our experiment tapped into the cognitive and perceptual constraints operative in the cultural evolution of musical systems, which may differ from the mechanisms at play in language evolution and change.
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http://dx.doi.org/10.1162/ARTL_a_00238DOI Listing
June 2019

Brain potentials predict learning, transmission and modification of an artificial symbolic system.

Soc Cogn Affect Neurosci 2016 12 10;11(12):1970-1979. Epub 2016 Aug 10.

Language Acquisition and Language Processing Lab Department of Language and Literature, Norwegian University of Science and Technology, Trondheim.

It has recently been argued that symbolic systems evolve while they are being transmitted across generations of learners, gradually adapting to the relevant brain structures and processes. In the context of this hypothesis, little is known on whether individual differences in neural processing capacity account for aspects of 'variation' observed in symbolic behavior and symbolic systems. We addressed this issue in the domain of auditory processing. We conducted a combined behavioral and EEG study on 2 successive days. On day 1, participants listened to standard and deviant five-tone sequences: as in previous oddball studies, an mismatch negativity (MMN) was elicited by deviant tones. On day 2, participants learned an artificial signaling system from a trained confederate of the experimenters in a coordination game in which five-tone sequences were associated to affective meanings (emotion-laden pictures of human faces). In a subsequent game with identical structure, participants transmitted and occasionally changed the signaling system learned during the first game. The MMN latency from day 1 predicted learning, transmission and structural modification of signaling systems on day 2. Our study introduces neurophysiological methods into research on cultural transmission and evolution, and relates aspects of variation in symbolic systems to individual differences in neural information processing.
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http://dx.doi.org/10.1093/scan/nsw112DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5141963PMC
December 2016

Extinction partially reverts structural changes associated with remote fear memory.

Learn Mem 2011 15;18(9):554-7. Epub 2011 Aug 15.

Cell Biology and Neurobiology Institute, National Research Council of Italy, Rome, Italy.

Structural synaptic changes occur in medial prefrontal cortex circuits during remote memory formation. Whether extinction reverts or further reshapes these circuits is, however, unknown. Here we show that the number and the size of spines were enhanced in anterior cingulate (aCC) and infralimbic (ILC) cortices 36 d following contextual fear conditioning. Upon extinction, aCC spine density returned to baseline, but the enhanced proportion of large spines did not. Differently, ILC spine density remained elevated, but the size of spines decreased dramatically. Thus, extinction partially erases the remote memory network, suggesting that the preserved network properties might sustain reactivation of extinguished conditioned fear.
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http://dx.doi.org/10.1101/lm.2246711DOI Listing
December 2011
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