- 1Action and Cognition Laboratory, Department of Social Sciences, Institute of Psychology, Adam Mickiewicz University in Poznan, Poznan, Poland
- 2Department of Kinesiology, University of Lethbridge, Lethbridge, AB, Canada
- 3Department of Neuroscience, University of Lethbridge, Lethbridge, AB, Canada
- 4Perception, Action and Memory Research Group, School of Psychology, Bangor University, Bangor, United Kingdom
Editorial on the Research Topic
Manual Skills, Handedness, and the Organization of Language in the Brain
Hand preference and cerebral dominance for some aspects of language processing are hallmarks of human brain functioning. Yet, their mutual relationships, similar to interrelations between hemispheric dominance for low-level sensorimotor control of the hand and the representations of higher-order, skilled actions (praxis) still remain unclear. Whereas in some accounts (Liepmann, 1900, 1908; Geschwind and Galaburda, 1985; Heilman, 1997; see also Goldenberg, 2013b) right handedness reflects (at least in part) the functioning of the left-lateralized manual praxis system, evidence from majority of left-handers weakens such a notion because they often represent praxis skills in their motor non-dominant—left—hemispheres, too (Lausberg et al., 1999; Frey et al., 2005; Goldenberg, 2013a; see also Gonzalez and Goodale, 2009; Grabowska et al., 2012; Haberling and Corballis, 2015; Kroliczak et al., 2016; cf. Carey et al., 2015). Although the putative links between praxis and language, and their interactions with handedness, have been long considered (Dejerine and Andre-Thomas, 1912; Heilman et al., 1973, 1974; McManus, 1985; Annett and Alexander, 1996; Meador et al., 1999), more recent studies clarify their relationships (Króliczak et al., 2011; Vingerhoets et al., 2013; Biduła and Króliczak, 2015; Goldenberg and Randerath, 2015; cf. Goldenberg, 2013b), further strengthening the idea that they are contingent on each other (Vingerhoets, 2014; Króliczak et al., 2018). Moreover, evidence from individuals with rarer forms of brain dominance now supports the idea that there is a longstanding evolutionary origin to the cerebral arrangement and distribution of both related and complementary skills, e.g., praxis and language vs. attention (Grabowska et al., 1994; Corballis, 2003; Cai et al., 2013; Goldenberg, 2013b).
The primary goal of this Research Topic is to present new pieces of evidence on the neural and functional organization of language and praxis, their links (or lack of thereof) with handedness and low-level motor skills, as well as behavioral consequences of their representations for other functions. Among the 12 contributing Original Research Articles, the considered functions include short-term tactile learning of Braille reading, visual word and number processing, and visuospatial discrimination. Yet, because the neural underpinnings of these functions are often strongly lateralized in the human brain, and may have common ancestry, their evolution and development is discussed in two Hypothesis and Theory articles.
Evolution and Early Development of Cerebral and Behavioral Asymmetries
The evolution of language and tool manufacture is considered by Corballis in the context of behavioral asymmetries that emerged in humans. Evidence is discussed that such asymmetries must have developed in an independent manner, triggered by multi-genetic sources, rather than a single overriding principle. It is also emphasized that representations of language and tool-use skills are rather poorly correlated with handedness. The relation of the individual development of hand preference to the critical development of human basic sensorimotor and cognitive abilities is, nevertheless, assumed in Michel. Based on earlier ideas that hand preference acquisition precedes unimanual object manipulation, and that both these skills must precede role-differentiated bimanual manipulation of objects, this contribution provides a description of an ideal paradigm for testing their development and relationships. The importance of studying developmental differences of cognitive skills across handedness is also emphasized.
Language Laterality, its Sources, and (in)Activity-Dependent Word Processing and Learning
Unique characteristics of atypical organization of language are considered by Biduła et al. Whereas, most of atypical cases are indeed found in left-handers, they are also present in ambidextrous and right-handed people (cf. Carey and Johnstone, 2014). Indeed, Biduła et al. demonstrated that although group results indicate mirror-reversed organization of language in atypical participants, evidence for this is less compelling at an individual level of analysis. The relationships between language laterality and handedness are also discussed by Schmitz et al., but now from the point of genetic influences. Evidence is shown that handedness and language organization are complex phenotypes that are ontogenetically independent. This report ends with conclusions that genes involved in ontogenesis of handedness contribute primarily to structural development, whereas genes underlying language laterality also contribute to the development of other cognitive processes (but seem also associated with mental and neurological disorders).
Given language-praxis links, certain kinds of actions, or inaction, could affect language processing and learning. For example, changes in motor system functioning could flexibly influence comprehension and acquisition of words (cf. Shebani and Pülvermuller, 2018). An intriguing paper by Yasuda et al. demonstrates that while peripheral body states influence action verb processing, in contrast to a strong embodiment view, constrained arm posture affected responses to both manual and non-manual action verbs. The opposite issue, that is, an impact of word processing on movement kinematics was investigated by Rugani et al. They showed that automatic numerical processing affects action execution in a context of kicking small balls with the index finger. Their participants responded faster to small numbers while kicking the ball to the left, and vice versa. Notably, Rugani et al. argue that similar paradigms could be used to study the impact of cognition on action in an unbiased way.
Learning new vocabulary can be a challenge, especially in elder people. Yet, as Heim and collaborators show (Heim et al.), a nap, in contrast to activity or even rest, helps to consolidate language learning. While these results are less relevant to the language-praxis debate, their translation to clinical settings for improvement of speech-language therapy following brain injuries would be welcome. Still, in some circumstances learning to read new words is not possible without the involvement of certain kinds of actions, as in tactile learning of Braille (Debowska et al.). This study established that even short-term tactile training can introduce functional and structural changes in the fusiform gyrus, linked to visual processing of language, including single word reading. This is yet another demonstration how language and praxis can be related.
When Handedness Does Not Matter, Does it?
Some manual actions seem so simple that one would expect mainly contralateral control of their performance. Yet, as Begliomini et al. show, grasping with the left (dominant) hand in left handers is not controlled only by the right (contralateral) hemisphere. They found increased connectivity with the left hemisphere parieto-frontal resources. Notably, the right (non-dominant) hand is controlled as in right-handers. These outcomes are consistent with a notion that hemispheric specialization for higher-order visuomotor control does not depend on handedness (Gonzalez et al., 2006). Nevertheless, reports on the impact of handedness, the used hand/eye, and/or other cognitive abilities on performance of the line bisection task (Ochando and Zago), and left-right discrimination (Constant and Mellet) reveal a more complex picture. In the line bisection task, performance depends on integration of differently weighted visuospatial hemispheric mechanisms, the motor component of the used hand, and individual laterality factors. When they are congruent, the strongest behavioral biases are observed. As to left-right discrimination, left-handers were found better at identifying their left hands and verifying “left” propositions. Nonetheless, numerous interactions of other factors provide new insights into the links between cognitive skills and left-right discrimination.
Functions Still To-be-Tested in Left-Handers
The last three papers focus entirely on specific aspects of motor control. They shed new light on the impact of spatial alignment and response hand in processing visual illusions (Scocchia et al.), competition between functional and situational affordances (Roche and Chainay), and the influence of action mode on efficiency in rule- vs. plan-based movements (Scheib et al.). Of course, the studied skills are less likely to depend on linguistic representations. Yet, although some differences contingent on the responding hand were suggested, they are less likely to emerge when directed at tools. As such, these approaches can stimulate new research and reveal new findings of theoretical interest for our debate.
Conclusions
This Research Topic highlights the findings on the relationships between manual skills and language, and their putative links to handedness and associated motor functions. Research showing both similarities and disparities in their organization in right-handed and left-handed (but also ambidextrous) individuals is featured. The debate includes the evolution and early development of cerebral and behavioral asymmetries, as well as their genetic foundations. We hope that further discussions and research ideas will emerge out of this work.
Author Contributions
GK conceived this work and drafted the editorial. CG and DC contributed intellectually to this work, revised, and approved the draft for publication.
Funding
GK was supported by National Science Centre (Narodowe Centrum Nauki, NCN) grant Maestro 2011/02/A/HS6/00174.
Conflict of Interest Statement
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.
Acknowledgments
None of this would be possible without the contributing authors, their study participants, the reviewers, editors, the additional guest editor, funding agencies, and the Frontiers platform. Thank you.
References
Annett, M., and Alexander, M. P. (1996). Atypical cerebral dominance: predictions and tests of the right shift theory. Neuropsychologia 34, 1215–1227. doi: 10.1016/0028-3932(96)00048-6
Biduła, S. P., and Króliczak, G. (2015). Structural asymmetry of the insula is linked to the lateralization of gesture and language. Eur. J. Neurosci. 41, 1438–1447. doi: 10.1111/ejn.12888
Cai, Q., Van der Haegen, L., and Brysbaert, M. (2013). Complementary hemispheric specialization for language production and visuospatial attention. Proc. Natl. Acad. Sci. U.S.A. 110, E322–E330. doi: 10.1073/pnas.1212956110
Carey, D. P., and Johnstone, L. T. (2014). Quantifying cerebral asymmetries for language in dextrals and adextrals with random-effects meta analysis. Front. Psychol. 5:1128. doi: 10.3389/fpsyg.2014.01128
Carey, D. P., Otto-de Haart, E. G., Buckingham, G., Dijkerman, H. C., Hargreaves, E. L., and Goodale, M. A. (2015). Are there right hemisphere contributions to visually-guided movement? Manipulating left hand reaction time advantages in dextrals. Front. Psychol. 6:1203. doi: 10.3389/fpsyg.2015.01203
Corballis, M. C. (2003). From mouth to hand: gesture, speech, and the evolution of right-handedness. Behav. Brain Sci. 26, 199–208; discussion 208–160. doi: 10.1017/S0140525X03000062
Dejerine, J., and Andre-Thomas (1912). Contribution a l'etude de l'aphasie chez les gauchers. Revue Neurol. 24, 213–226.
Frey, S. H., Funnell, M. G., Gerry, V. E., and Gazzaniga, M. S. (2005). A dissociation between the representation of tool-use skills and hand dominance: insights from left- and right-handed callosotomy patients. J. Cogn. Neurosci. 17, 262–272. doi: 10.1162/0898929053124974
Geschwind, N., and Galaburda, A. M. (1985). Cerebral lateralization. Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. Arch. Neurol. 42, 428–459. doi: 10.1001/archneur.1985.04060050026008
Goldenberg, G. (2013b). Apraxia: The Cognitive Side of Motor Control. Oxford: Oxfrod University Press.
Goldenberg, G., and Randerath, J. (2015). Shared neural substrates of apraxia and aphasia. Neuropsychologia 75, 40–49. doi: 10.1016/j.neuropsychologia.2015.05.017
Gonzalez, C. L., Ganel, T., and Goodale, M. A. (2006). Hemispheric specialization for the visual control of action is independent of handedness. J. Neurophysiol. 95, 3496–3501. doi: 10.1152/jn.01187.2005
Gonzalez, C. L., and Goodale, M. A. (2009). Hand preference for precision grasping predicts language lateralization. Neuropsychologia 47, 3182–3189. doi: 10.1016/j.neuropsychologia.2009.07.019
Grabowska, A., Gut, M., Binder, M., Forsberg, L., Rymarczyk, K., and Urbanik, A. (2012). Switching handedness: fMRI study of hand motor control in right-handers, left-handers and converted left-handers. Acta Neurobiol. Exp. (Wars) 72, 439–451.
Grabowska, A., Herman, A., Nowicka, A., Szatkowska, I., and Szelag, E. (1994). Individual differences in the functional asymmetry of the human brain. Acta Neurobiol. Exp. (Wars) 54, 155–162.
Haberling, I. S., and Corballis, M. C. (2015). Cerebellar asymmetry, cortical asymmetry and handedness: two independent networks. Laterality 19, 1–18. doi: 10.1080/1357650X.2015
Heilman, K. M. (1997). “Handedness,” in Apraxia: The Neuropsychology of Action, eds L. J. G. Rothi and K. M. Heilman (Hove: Psychology Press; Erlbaum (UK) Taylor & Francis), 19–28.
Heilman, K. M., Coyle, J. M., Gonyea, E. F., and Geschwind, N. (1973). Apraxia and agraphia in a left-hander. Brain 96, 21–28. doi: 10.1093/brain/96.1.21
Heilman, K. M., Gonyea, E. F., and Geschwind, N. (1974). Apraxia and agraphia in a right-hander. Cortex 10, 284–288. doi: 10.1016/S0010-9452(74)80021-3
Króliczak, G., Buchwald, M., Potok, W., and Przybylski, L. (2018). Ręczność, praksja i język: nowe spojrzenie na delikatną triadę [Handedness, praxis and language: a tricky triad revisited]. Polskie Forum Psychologiczne [Polish Psychological Forum]. 23, 22–34. doi: 10.14656/PFP20180102
Króliczak, G., Piper, B. J., and Frey, S. H. (2011). Atypical lateralization of language predicts cerebral asymmetries in parietal gesture representations. Neuropsychologia 49, 1698–1702. doi: 10.1016/j.neuropsychologia.2011.02.044
Kroliczak, G., Piper, B. J., and Frey, S. H. (2016). Specialization of the left supramarginal gyrus for hand-independent praxis representation is not related to hand dominance. Neuropsychologia 93, 501–512. doi: 10.1016/j.neuropsychologia.2016.03.023
Lausberg, H., Göttert, R., Münssinger, U., Boegner, F., and Marx, P. (1999). Callosal disconnection syndrome in a left-handed patient due to infarction of the total length of the corpus callosum. Neuropsychologia 37, 253–265. doi: 10.1016/S0028-3932(98)00079-7
Liepmann, H. (1900). Das Krankheitshild der Apraxie (Motorischen/Asymbolie). Monatschrift fur Psychiatrie und Neurologie 8, 15–44, 102–132, 182–197.
McManus, I. C. (1985). Handedness, language dominance and aphasia: a genetic model. Psychol. Med. Monogr. Suppl. 8, 1–40. doi: 10.1017/S0264180100001879
Meador, K. J., Loring, D. W., Lee, K., Hughes, M., Lee, G., Nichols, M., et al. (1999). Cerebral lateralization: relationship of language and ideomotor praxis. Neurology 53, 2028–2031. doi: 10.1212/WNL.53.9.2028
Shebani, Z., and Pülvermuller, F. (2018). Flexibility in language action interaction: the influence of movement type. Front Hum Neurosci, 12, 252. doi: 10.3389/fnhum.2018.00252
Vingerhoets, G. (2014). Praxis, language, and handedness: a tricky triad. Cortex 57, 294–296; discussion 306-298. doi: 10.1016/j.cortex.2014.01.019
Keywords: hand preference, cerebral dominance, brain functioning, sensorimotor control, higher-order processing, skilled actions, praxis
Citation: Króliczak G, Gonzalez CLR and Carey DP (2019) Editorial: Manual Skills, Handedness, and the Organization of Language in the Brain. Front. Psychol. 10:930. doi: 10.3389/fpsyg.2019.00930
Received: 15 March 2019; Accepted: 08 April 2019;
Published: 26 April 2019.
Copyright © 2019 Króliczak, Gonzalez and Carey. 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: Gregory Króliczak, krolgreg@amu.edu.pl