Neural dynamics of learning sound-action associations
Open accessAbstract
A motor component is pre-requisite to any communicative act as one must inherently move to communicate. To learn to make a communicative act, the brain must be able to dynamically associate arbitrary percepts to the neural substrate underlying the pre-requisite motor activity. We aimed to investigate whether brain regions involved in complex gestures (ventral pre-motor cortex, Brodmann Area 44) were involved in mediating association between novel abstract auditory stimuli and novel gestural movements. In a functional resonance imaging (fMRI) study we asked participants to learn associations between previously unrelated novel sounds and meaningless gestures inside the scanner. We use functional connectivity analysis to eliminate the often present confound of 'strategic covert naming' when dealing with BA44 and to rule out effects of non-specific reductions in signal. Brodmann Area 44, a region incorporating Broca's region showed strong, bilateral, negative correlation of BOLD (blood oxygen level dependent) response with learning of sound-action associations during data acquisition. Left-inferior-parietal-lobule (l-IPL) and bilateral loci in and around visual area V5, right-orbital-frontal-gyrus, right-hippocampus, left-para-hippocampus, right-head-of-caudate, right-insula and left-lingual-gyrus also showed decreases in BOLD response with learning. Concurrent with these decreases in BOLD response, an increasing connectivity between areas of the imaged network as well as the right-middle-frontal-gyrus with rising learning performance was revealed by a psychophysiological interaction (PPI) analysis. The increasing connectivity therefore occurs within an increasingly energy efficient network as learning proceeds. Strongest learning related connectivity between regions was found when analysing BA44 and l-IPL seeds. The results clearly show that BA44 and l-IPL is dynamically involved in linking gesture and sound and therefore provides evidence that one of the mechanisms required for the evolution of human communication is found within these motor regions.
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Network coordination facilitating perceptual processing, including speech comprehension, has been detected as elevated FC.
“Network coordination facilitating perceptual processing, including speech comprehension, has been detected as elevated FC (17,20,43–47).”
From Elevated functional connectivity along a corticostriatal loop and the mechanism of auditory/verbal hallucinations in patients with schizophrenia (2011) · cites this paper as [45]
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“observed convergence of the sound and sight of hand actions as a generic feature of the mirror-neuron system recruitment. Here, we were interested in the effect of visual experience of watching dance, which includes enjoyment, conveyance of meaning, and emotion. This was measured by the effect of live dance performanc…”
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Simonyan, K., Ostuni, J. L., Ludlow, C. L., & Horwitz, B. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4897-09.2009 · Cited by 122 · see citing works
“…et al., 2005), it may play a role in mapping of the acoustic-phonetic cues into lexical representations and the articulatory-gestural representation of a sample auditory stimulus for syllable production (Bohland and Guenther, 2006; Guenther et al., 2006; Jardri et al., 2007; McNamara et al., 2008).”
Imitation and observational learning of hand actions: Prefrontal involvement and connectivity
Higuchi, S., Holle, H., Roberts, N., Eickhoff, S. B., & Vogt, S. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.09.021 · Cited by 112 · see citing works
“…and the FPMC, which is a critical assumption of our hierarchical model of imitation learning (for a related analysis in learning sound-action associations, see McNamara et al., 2008; and for a conectivity analysis of the network involved in imitative response inhibition, see Bien et al., 2009).”
BackgroundDifferent categories of living and non-living sound-sources activate distinct cortical networks
Engel, L. R., Frum, C., Puce, A., Walker, N. A., & Lewis, J. W. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.05.041 · Cited by 104 · see citing works
“These left IPL and IFG are involved in associating gestural movements with human-produced sounds: they are thought to play a role in interpreting realized goals of observed prehensile actions (Grèzes et al., 2003; Johnson-Frey et al., 2003, 2005; Lewis et al., 2005; Lahav et al., 2007; McNamara et al., 2008), and are…”
BackgroundKühn, S., Keizer, A. W., Rombouts, S. A. R. B., & Hommel, B. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21418 · Cited by 88 · see citing works
The Influence of Auditory Cues on Bodily and Movement Perception
Stanton, T. R., & Spence, C. J. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.03001 · Cited by 75 · see citing works
“, movement that is paired with the auditory cue) (McNamara et al., 2008).”
BackgroundFargier, R., Paulignan, Y., Véronique Boulenger, A., Padraic Monaghan, B., Reboul, A., & Nazir, T. A. (2011) · Cortex · doi:10.1016/j.cortex.2011.07.003 · Cited by 63 · see citing works
Joassin, F., Maurage, P., & Campanella, S. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.08.073 · Cited by 60 · see citing works
Jola, C., McAleer, P., Grosbras, M., Love, S., Morison, G., & Pollick, F. E. (2013) · i-Perception · doi:10.1068/i0536 · Cited by 56 · see citing works
“…for A or V. Theoretically, increased coherence can be postulated at the low level of unisensory processing (A and V), at the level of multisensory integration (AV; Grosbras, Beaton, & Eickhoff, 2011) or at the level of action understanding (fronto-parietal; Grafton, 2009; McNamara et al., 2008).”
Lewis, J. W., Talkington, W. J., Puce, A., Engel, L. R., & Frum, C. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21570 · Cited by 46 · see citing works
“heard sound to oneʼs own repertoire of meaningful soundproducing motor actions (Engel et al., 2009; Aglioti, Cesari, Romani, & Urgesi, 2008; Galati et al., 2008; McNamara et al., 2008; Pazzaglia, Pizzamiglio, Pes, & Aglioti, 2008; Lahav et al., 2007; Gazzola et al., 2006; Lewis et al., 2005, 2006; Bidet-Caulet et al.,…”
BackgroundAuditory object perception: A neurobiological model and prospective review
Brefczynski‐Lewis, J. A., & Lewis, J. W. (2017) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2017.04.034 · Cited by 45 · see citing works
“in the human cortical hemispheres show strong lateralizations that are proposed to have their origins in gestural networks (Johannesson, 1950; Hewes, 1973; Grigor'eva and Deriagina, 1987; Corballis, 1999; Li et al., 2000; Zatorre et al., 2002; McNamara et al., 2008; Morillon et al., 2010), which in turn are thought to…”
BackgroundKnoblauch, A., Körner, E., Körner, U., & Sommer, F. T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096485 · Cited by 41 · see citing works
FMRI adaptation during performance of learned arbitrary visuomotor conditional associations
Chouinard, P. A., & Goodale, M. A. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.07.020 · Cited by 28 · see citing works
“Indeed, neuroimaging studies that have examined the neural correlates underlying the learning of new arbitrary conditional associations demonstrate decreases in VL-PFC activity as a function of learning (Toni et al., 2001b, 2002b; Eliassen et al., 2003; McNamara et al., 2008; Brovelli et al., 2008).”
Impact of Structural Plasticity on Memory Formation and Decline
Knoblauch, A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-803784-3.00017-2 · Cited by 16 · see citing works
Audio-Visual Perception of Everyday Natural Objects – Hemodynamic Studies in Humans
Lewis, J. W. (2010) · Springer eBooks · doi:10.1007/978-1-4419-5615-6_10 · Cited by 16 · see citing works
Adapting to Changes in Communication: The Orbitofrontal Cortex in Language and Speech Processing
Jiang, X., Ma, X., Sanford, R., & Li, X. (2024) · Brain Sciences · doi:10.3390/brainsci14030264 · Cited by 15 · see citing works
“The right OFC activity was negatively associated with an improvement in learning performance, such that the reduced activity showed greater improvement in the judgment task [78].”
ResultFargier, R., Ploux, S., Cheylus, A., Reboul, A., Paulignan, Y., & Nazir, T. A. (2014) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00669 · Cited by 12 · see citing works
“…Bellebaum et al. (2013) recently showed that the perception of manipulable novel objects is modulated by sensorimotor experience and involves frontoparietal regions (see also Catmur et al., 2008; McNamara et al., 2008; Catmur, Walsh, & Heyes, 2007; Weisberg, van Turennout, & Martin, 2007).”
BackgroundWebster, P. J., Skipper‐Kallal, L. M., Frum, C., Still, H. N., Ward, B. D., & Lewis, J. W. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00579 · Cited by 12 · see citing works
“However, many earlier human neuroimaging studies using human-produced sound stimuli, which in adult listeners tend to inherently entail complex semantic associations, likely recruited brain regions well outside of auditory cortex proper for processing higher order cognitive information, including linguistic features,…”
BackgroundNeural control of fundamental frequency rise and fall in Mandarin tones
Howell, P., Jiang, J., Peng, D., & Lu, C. (2012) · Brain and Language · doi:10.1016/j.bandl.2012.01.004 · Cited by 8 · see citing works
“McNamara et al. (2008) found that brain activity showed negative correlation with behavioral performance during sound–action association learning.”
Csonka, M., Mardmomen, N., Webster, P. J., Brefczynski‐Lewis, J. A., Frum, C., & Lewis, J. W. (2021) · Cerebral Cortex Communications · doi:10.1093/texcom/tgab002 · Cited by 5 · see citing works
“…foci Number of foci 43 62 First author Year Experimental code and abbreviated task 682 177 148 325 Brief description of experimental paradigm 43 70 McNamara 2008 Table (BA44 and IPL) 12 2 2 4 Videos of meaningless hand gestures and synthetic tone sounds: Increases in functional connectivity with…”
BackgroundInfluentialŻygierewicz, J., Sielużycki, C., Zacharias, N., Suffczyński, P., Kordowski, P., Scheich, H., Durka, P. J., & König, R. (2011) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2011.12.013 · Cited by 2 · see citing works
Campanella, S., & Joassin, F. (2012) · Springer eBooks · doi:10.1007/978-1-4614-3585-3_8
- Authors
- McNamara, A., Buccino, G., Menz, M. M., Gläscher, J., Wolbers, T., Baumgärtner, A., & Binkofski, F.
- Affiliations
- University of Surrey (GB)
- University of Parma (IT)
- University Medical Center Hamburg-Eppendorf (DE)
- University Hospital Schleswig-Holstein (DE)
- Corresponding author
- McNamara, Adam
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2008-12-03
- Volume
- 3
- Issue
- 12
- Pages
- e3845
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2585816
- OpenAlex
- W2130177912
- Cited by
- 25
- References
- 67
- Citations by year
- 2024: 1 · 2021: 1 · 2020: 1 · 2019: 1 · 2017: 3 · 2014: 2 · 2013: 1 · 2012: 3
- FWCI
- 2.07
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Surrey Research Insight Open Access (The University of Surrey) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
- Funders
- Deutsche Forschungsgemeinschaft
- Volkswagen Foundation
- Bundesministerium für Bildung und Forschung (01GW0571, 01GO0207)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neurobiology of Language and Bilingualism
- Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Keywords
- ventral premotor cortex, Brodmann area 44, inferior parietal lobule, functional connectivity, auditory-motor integration, psychophysiological interaction, BOLD signal
- MeSH terms
- Acoustic Stimulation, Adult, Association, Brain, Brain Mapping, Female, Gestures, Humans, Learning, Magnetic Resonance Imaging, Male, Mental Processes, Psychomotor Performance, Sound, Speech
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