Alfredo Brancucci
Nicole Angenstein- 1Dipartimento di Scienze Motorie, Umane e della Salute, Università di Roma “Foro Italico”, Rome, Italy
- 2Combinatorial NeuroImaging Core Facility, Leibniz Institute for Neurobiology, Magdeburg, Germany
Editorial on the Research Topic
Hemispheric Asymmetries in the Auditory Domain
The two cerebral hemispheres are specialized for different cognitive abilities and functional as well-structural asymmetries are present in many regions of the brain which control various types of functions, from sensory processing to motor activity (Brancucci and Tommasi, 2011; Corballis and Häberling, 2017; Westerhausen, 2019). The present issue focuses on Hemispheric Asymmetries in the Auditory Domain, a topic which has given rise to a huge amount of scientific work utilizing behavioral, neuropsychological, electrophysiological, and neuroimaging techniques (Bryden, 1963; Kimura, 1963; Brancucci et al., 2004, 2012; Prete et al., 2014, 2015, 2016, 2018a; D'Anselmo et al., 2016, 2018), possibly as auditory functions, as well as their underlying biological networks, are the most lateralized in the brain. The literature ranges from the study of the asymmetric processing during tasks on simple auditory stimuli (Brancucci and San Martini, 1999, 2003; Behne et al., 2005; Brancucci et al., 2005a; Brechmann and Scheich, 2005; Angenstein and Brechmann, 2013a,b; Brechmann and Angenstein, 2019), to the differential specialization of the hemispheres in the various aspects of language (Behne et al., 2006; Della Penna et al., 2007; Brancucci et al., 2008a; D'Anselmo et al., 2013; Wendt et al., 2021), to the latest evidence of asymmetries arising during social interactions (Brancucci et al., 2009). However, several points remain to be clarified, and there are still some unanswered questions, such as different plasticity processes in the two hemispheres especially with respect to clinical conditions, asymmetric functions of attention, and different asymmetric processes in language and music processing. The contributions to this Research Topic try to answer some of these questions, considering in particular aspects of auditory attention, plasticity processes in hearing impairment, the neural basis of language, and musical cognition.
Five papers focus on hemispheric asymmetries in the context of verbal processing (Kazimierczak et al.; Kljajevic; Moulin; Rødland et al.; Han et al.). In their fMRI study, Kazimierczak et al. looked for modulation of brain activity by top-down effects of forced-attention during a dichotic listening paradigm (Hugdahl, 2000). They observed the expected right-ear advantage. This behavioral effect was associated with a left-lateralized activity in speech perception areas of the temporal lobe. The directed forced attention to the left or right ear had the expected strong effects on the ear advantage. Unexpectedly, forced attention did not show a strong effect on brain activity neither with a traditional region analysis nor with a network analysis approach. They discuss their findings in relation to the classical theoretical models of dichotic listening and large scale cortical networks (Brancucci et al., 2005b, 2008b).
In an opinion paper, Kljajevic discusses different potential factors associated with sex differences in verbal learning (e.g., brain anatomy, sex hormones). The author emphasizes that sex differences in hemispheric asymmetry, namely planum temporale asymmetries, might be an important factor for the female advantage in verbal learning.
With a dichotic listening paradigm, Moulin showed that the word-level contextual influences during speech perception in hearing-impaired patients were stronger on the right than on the left ear. This asymmetry between the ears increased with increasing right-ear advantage and decreased with age, mainly due to an increasing contextual influence on the left ear. This age effect is consistent with reduced hemispheric asymmetry with age (see for example the HAROLD model, Cabeza, 2002).
Based on a visual language paradigm, Rødland et al. developed a short language paradigm for potential clinical application that can be used in the visual or auditory domain. Their fMRI-study showed that independent of the presented modality, the most central parts of the language system were activated by this paradigm mainly in the left hemisphere. Here, the connectivity patterns (revealed by dynamic causal modeling) were similar between presentation modalities whereas the right hemispheric involvement was different between modalities, e.g., more right frontal involvement during the visual than auditory condition.
In their paper on asymmetries in unilateral deafness, Han et al. start from the fact that unilateral deafness reduces the ability to localize binaural sounds and leads to a substantial change in auditory cortical processing. To unveil the underlying mechanisms, authors compared primary auditory cortical activity and hemispheric asymmetries of normal hearing, unilaterally deaf (right or left), and simulated hearing loss participants while listening to speech sounds delivered from different locations in the azimuth plane. The right ear hearing-loss group revealed slower reaction times for sound localization and prolonged neural latency compared to the left ear hearing-loss group. In addition, individuals of the right ear hearing-loss group with better sound localization showed increased responses in the hemisphere ipsilateral to the hearing ear. Conversely, the left ear hearing-loss group showed contralateral enhanced activity related to right ear stimulation. Thus, the authors demonstrated that right ear unilateral deafness can rely on better plastic reorganization compared to left ear deafness. This paper evidences the presence of potential plasticity targets, which should not be neglected in auditory rehabilitation.
Two other papers in this series look at hemispheric asymmetries in non-verbal processing (Kim et al.; Tanaka and Kirino). Tanaka and Kirino deal with a very interesting topic concerning musical imagery. They exploit the common condition of subjects who lie in an fMRI scanner and hear the typical machine noise using this condition as a baseline. During the musical imagery condition, in which musicians imagined to perform a music piece, they found enhanced right-lateralized connectivity of the auditory cortical areas with other brain regions devoted to cognitive, memory, and emotional processing. This outcome demonstrates that auditory cortex is involved with other areas in imagined music performance (Prete et al., 2018b).
Kim et al. investigate the intriguing issue of neural correlates of non-verbal syntax analyzing how syntactic irregularity and perceptual ambiguity on musical syntax are dissociated in terms of effective connectivity. Presenting three conditions in which a simple musical sequence ended with dominant- tonic, dominant-submediant or dominant-supertonic, they showed that left to right connectivity in bilateral inferior frontal gyrus was enhanced for the most irregular condition (dominant-supertonic) whereas connectivity from the right to the left superior temporal gyrus was enhanced for the most ambiguous condition (dominant-submediant). Thus, they showed that syntactic irregularity and perceptual ambiguity elicit dissociated processing between bilateral auditory areas.
The overall message that this Research Topic conveys is that Hemispheric Asymmetries in the Auditory Domain embrace competences that arise from various scientific fields whose interaction can bear fruit for cognitive neuroscience and for the other subject areas ranging around brain science. Exploiting the knowledge acquired on auditory hemispheric and functional asymmetries will generate further studies facing the question at different levels of analysis to disentangle the intriguing processes underlying such complex psychobiological functions.
Author Contributions
All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Angenstein, N., and Brechmann, A. (2013a). Division of labor between left and right human auditory cortices during the processing of intensity and duration. Neuroimage 83, 1–11. doi: 10.1016/j.neuroimage.2013.06.071
Angenstein, N., and Brechmann, A. (2013b). Left auditory cortex is involved in pairwise comparisons of the direction of frequency modulated tones. Front. Neurosci. 7:115. doi: 10.3389/fnins.2013.00115
Behne, N., Scheich, H., and Brechmann, A. (2005). Contralateral white noise selectively changes right human auditory cortex activity caused by a FM-direction task. J. Neurophysiol. 93, 414–423. doi: 10.1152/jn.00568.2004
Behne, N., Wendt, B., Scheich, H., and Brechmann, A. (2006). Contralateral white noise selectively changes left human auditory cortex activity in a lexical decision task. J. Neurophysiol. 95, 2630–2637. doi: 10.1152/jn.01201.2005
Brancucci, A., Babiloni, C., Babiloni, F., Galderisi, S., Mucci, A., Tecchio, F., et al. (2004). Inhibition of auditory cortical responses to ipsilateral stimuli during dichotic listening: evidence from magnetoencephalography. Eur. J. Neurosci. 19, 2329–2336. doi: 10.1111/j.0953-816X.2004.03302.x
Brancucci, A., Babiloni, C., Rossini, P. M., and Romani, G. L. (2005a). Right hemisphere specialization for intensity discrimination of musical and speech sounds. Neuropsychologia 43, 1916–1923. doi: 10.1016/j.neuropsychologia.2005.03.005
Brancucci, A., Babiloni, C., Vecchio, F., Galderisi, S., Mucci, A., Tecchio, F., et al. (2005b). Decrease of functional coupling between left and right auditory cortices during dichotic listening: an electroencephalography study. Neuroscience 136, 323–332. doi: 10.1016/j.neuroscience.2005.06.046
Brancucci, A., D'Anselmo, A., Martello, F., and Tommasi, L. (2008a). Left hemisphere specialization for duration discrimination of musical and speech sounds. Neuropsychologia 46, 2013–2019. doi: 10.1016/j.neuropsychologia.2008.01.019
Brancucci, A., Lucci, G., Mazzatenta, A., and Tommasi, L. (2009). Asymmetries of the human social brain in the visual, auditory and chemical modalities. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 895–914. doi: 10.1098/rstb.2008.0279
Brancucci, A., Penna, S. D., Babiloni, C., Vecchio, F., Capotosto, P., Rossi, D., et al. (2008b). Neuromagnetic functional coupling during dichotic listening of speech sounds. Hum. Brain Mapp. 29, 253–264. doi: 10.1002/hbm.20385
Brancucci, A., Prete, G., Meraglia, E., di Domenico, A., Lugli, V., Penolazzi, B., et al. (2012). Asymmetric cortical adaptation effects during alternating auditory stimulation. PLoS One 7:e34367. doi: 10.1371/journal.pone.0034367
Brancucci, A., and San Martini, P. (1999). Laterality in the perception of temporal cues of musical timbre. Neuropsychologia 37, 1445–1451. doi: 10.1016/S0028-3932(99)00065-2
Brancucci, A., and San Martini, P. (2003). Hemispheric asymmetries in the perception of rapid (timbral) and slow (nontimbral) amplitude fluctuations of complex tones. Neuropsychology 17, 451–457. doi: 10.1037/0894-4105.17.3.451
Brancucci, A., and Tommasi, L. (2011). “Binaural rivalry”: dichotic listening as a tool for the investigation of the neural correlate of consciousness. Brain Cogn. 76, 218–224. doi: 10.1016/j.bandc.2011.02.007
Brechmann, A., and Angenstein, N. (2019). The impact of task difficulty on the lateralization of processing in the human auditory cortex. Hum. Brain Mapp. 40, 5341–5353. doi: 10.1002/hbm.24776
Brechmann, A., and Scheich, H. (2005). Hemispheric shifts of sound representation in auditory cortex with conceptual listening. Cereb. Cortex 15, 578–587. doi: 10.1093/cercor/bhh159
Bryden, M. P. (1963). Ear preference in auditory perception. J. Exp. Psychol. 65, 103–105. doi: 10.1037/h0042773
Cabeza, R. (2002). Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol. Aging 17, 85–100. doi: 10.1037/0882-7974.17.1.85
Corballis, M. C., and Häberling, I. S. . (2017). The many sides of hemispheric asymmetry: a selective review and outlook. J. Int. Neuropsychol. Soc. 23, 710–718. doi: 10.1017/S1355617717000376
D'Anselmo, A., Giuliani, F., Campopiano, F., Carta, E., and Brancucci, A. (2018). Hemispheric asymmetries in setticlavio reading. Neuropsychology 32, 337–343. doi: 10.1037/neu0000430
D'Anselmo, A., Marzoli, D., and Brancucci, A. (2016). The influence of memory and attention on the ear advantage in dichotic listening. Hear. Res. 342, 144–149. doi: 10.1016/j.heares.2016.10.012
D'Anselmo, A., Reiterer, S., Zuccarini, F., Tommasi, L., and Brancucci, A. (2013). Hemispheric asymmetries in bilinguals: tongue similarity affects lateralization of second language. Neuropsychologia 51, 1187–1194. doi: 10.1016/j.neuropsychologia.2013.03.016
Della Penna, S., Brancucci, A., Babiloni, C., Franciotti, R., Pizzella, V., Rossi, D., et al. (2007). Lateralization of dichotic speech stimuli is based on specific auditory pathway interactions: neuromagnetic evidence. Cereb. Cortex 17, 2303–2311. doi: 10.1093/cercor/bhl139
Hugdahl, K. (2000). Lateralization of cognitive processes in the brain. Acta Psychol. (Amst). 105, 211–235. doi: 10.1016/S0001-6918(00)00062-7
Kimura, D. (1963). Speech lateralization in young children as determined by an auditory test. J. Comp. Physiol. Psychol. 56, 899–902. doi: 10.1037/h0047762
Prete, G., D'Anselmo, A., Brancucci, A., and Tommasi, L. (2018b). Evidence of a Right Ear Advantage in the absence of auditory targets. Sci. Rep. 8:15569. doi: 10.1038/s41598-018-34086-3
Prete, G., D'Anselmo, A., Tommasi, L., and Brancucci, A. (2018a). Modulation of the dichotic right ear advantage during bilateral but not unilateral transcranial random noise stimulation. Brain Cogn. 123, 81–88. doi: 10.1016/j.bandc.2018.03.003
Prete, G., Fabri, M., Foschi, N., Brancucci, A., and Tommasi, L. (2015). The “consonance effect” and the hemispheres: a study on a split-brain patient. Laterality 20, 257–269. doi: 10.1080/1357650X.2014.959525
Prete, G., Marzoli, D., Brancucci, A., Fabri, M., Foschi, N., and Tommasi, L. (2014). The processing of chimeric and dichotic emotional stimuli by connected and disconnected cerebral hemispheres. Behav. Brain Res. 271, 354–364. doi: 10.1016/j.bbr.2014.06.034
Prete, G., Marzoli, D., Brancucci, A., and Tommasi, L. (2016). Hearing it right: evidence of hemispheric lateralization in auditory imagery. Hear. Res. 332, 80–86. doi: 10.1016/j.heares.2015.12.011
Wendt, B., Stadler, J., Verhey, J. L., Hessel, H., and Angenstein, N. (2021). Effect of contralateral noise on speech intelligibility. Neuroscience 459, 59–69. doi: 10.1016/j.neuroscience.2021.01.034
Keywords: hemispheric asymmetries, functional lateralization, auditory perception, functional connectivity, verbal cognition, musical cognition
Citation: Brancucci A and Angenstein N (2022) Editorial: Hemispheric Asymmetries in the Auditory Domain. Front. Behav. Neurosci. 16:892786. doi: 10.3389/fnbeh.2022.892786
Received: 09 March 2022; Accepted: 18 March 2022;
Published: 06 April 2022.
Edited and reviewed by:
Nuno Sousa, University of Minho, PortugalCopyright © 2022 Brancucci and Angenstein. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Alfredo Brancucci, YWxmcmVkby5icmFuY3VjY2kmI3gwMDA0MDt1bmljaC5pdA==