Atypical Organization of Praxis and Language: A Look Back

Grzegorz Króliczak; Mikołaj Buchwald; Michał Klichowski; Agnieszka M. Nowik; Brian J. Piper

doi:10.18290/rpsych21242-8s

Grzegorz Króliczak Action and Cognition Laboratory, Faculty of Psychology and Cognitive Science, Adam Mickiewicz University, Poznań, Poland https://orcid.org/0000-0001-6121-0536
Mikołaj Buchwald Action and Cognition Laboratory, Faculty of Psychology and Cognitive Science, Adam Mickiewicz University, Poznań, Poland https://orcid.org/0000-0001-8764-0032
Michał Klichowski Learning Laboratory, Faculty of Educational Studies, Adam Mickiewicz University, Poznan, Poland https://orcid.org/0000-0002-1614-926X
Agnieszka M. Nowik Action and Cognition Laboratory, Faculty of Psychology and Cognitive Science, Adam Mickiewicz University, Poznań, Poland https://orcid.org/0000-0002-3872-1685
Brian J. Piper Department of Medical Education, Geisinger Commonwealth School of Medicine, Scranton, PA, USA https://orcid.org/0000-0002-2295-445X

DOI: https://doi.org/10.18290/rpsych21242-8s

Keywords: tool use gestures, verbal fluency, hand dominance, interrelations, functional asymmetries, lateralization, segregation, dissociation

Abstract

Atypical representations of praxis and language were studied in two forms and combinations: bilateral organization, and right lateralization, independently for each function; when the atypically represented praxis dissociates from typically lateralized language; and when both praxis and language have atypical forms. Direct differences between bilateral and right-lateralized representations were either marginal (for praxis), or nonexistent (for language). Because atypical organization of praxis is over twice as frequent as language in its atypical form, sample size might be an issue only for the latter (as atypical organization of language is very rare). Group averages in their dissociations, and associations in atypical forms, revealed the expected representations of the two functions. These outcomes indicate that merging the two atypical representations of praxis, or language, into one atypical group can reveal the critical aspects of their atypicality, including subcortical contributions, without seriously impeding correct interpretation of the essential underlying neural mechanisms.

References

Amaral, L., Bergstrom, F., & Almeida, J. (2021). Overlapping but distinct: Distal connectivity dissociates hand and tool processing networks. Cortex, 140, 1–13. https://doi.org/10.1016/j.cortex.2021.03.011

Badzakova-Trajkov, G., Haberling, I. S., Roberts, R. P., & Corballis, M. C. (2010). Cerebral asymmetries: Complementary and independent processes. PLoS ONE, 5(3), e9682. https://doi.org/10.1371/journal.pone.0009682

Biduła, S. P., & Króliczak, G. (2015). Structural asymmetry of the insula is linked to the lateralization of gesture and language. European Journal of Neuroscience, 41(11), 1438–1447. https://doi.org/10.1111/ejn.12888

Biduła, S. P., Przybylski, L., Pawlak, M. A., & Króliczak, G. (2017). Unique neural characteristics of atypical lateralization of language in healthy individuals. Frontiers in Neuroscience, 11, 525. https://doi.org/10.3389/fnins.2017.00525

Binkofski, F., & Buxbaum, L. J. (2013). Two action systems in the human brain. Brain & Language, 127(2), 222–229. https://doi.org/10.1016/j.bandl.2012.07.007

Bohlhalter, S., Hattori, N., Wheaton, L., Fridman, E., Shamim, E. A., Garraux, G., & Hallett, M. (2009). Gesture subtype-dependent left lateralization of praxis planning: an event-related fMRI study. Cerebral Cortex, 19(6), 1256–1262. https://doi.org/10.1093/cercor/bhn168

Buchwald, M., Przybylski, L., & Króliczak, G. (2018). Decoding Brain States for Planning Functional Grasps of Tools: A Functional Magnetic Resonance Imaging Multivoxel Pattern Analysis Study. Journal of the International Neuropsychological Society, 24(10), 1013–1025. https://doi.org/10.1017/S1355617718000590

Cai, Q., Van der Haegen, L., & Brysbaert, M. (2013). Complementary hemispheric specialization for language production and visuospatial attention. Proceedings of the National Academy of Sciences (USA), 110(4), E322-330. https://doi.org/10.1073/pnas.1212956110

Carey, D. P., & Johnstone, L. T. (2014). Quantifying cerebral asymmetries for language in dextrals and adextrals with random-effects meta analysis. Frontiers in Psychology, 5, 1128. https://doi.org/10.3389/fpsyg.2014.01128

Chen, Q., Garcea, F. E., & Mahon, B. Z. (2016). The Representation of Object-Directed Action and Function Knowledge in the Human Brain. Cerebral Cortex, 26(4), 1609–1618. https://doi.org/10.1093/cercor/bhu328

Chlebus, P., Mikl, M., Brazdil, M., Pazourkova, M., Krupa, P., & Rektor, I. (2007). fMRI evaluation of hemispheric language dominance using various methods of laterality index calculation. Experimental Brain Research, 179(3), 365–374. https://doi.org/10.1007/s00221-006-0794-y

Eklund, A., Nichols, T. E., & Knutsson, H. (2016). Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences (USA), 113(28), 7900–7905. https://doi.org/10.1073/pnas.1602413113

Garcea, F. E., & Buxbaum, L. J. (2019). Gesturing tool use and tool transport actions modulates inferior parietal functional connectivity with the dorsal and ventral object processing pathways. Human Brain Mapping, 40(10), 2867–2883. https://doi.org/10.1002/hbm.24565

Garcea, F. E., Greene, C., Grafton, S. T., & Buxbaum, L. J. (2020). Structural Disconnection of the Tool Use Network after Left Hemisphere Stroke Predicts Limb Apraxia Severity. Cerebral Cortex Communications, 1(1), tgaa035. https://doi.org/10.1093/texcom/tgaa035

Gerrits, R., Verhelst, H., & Vingerhoets, G. (2020). Mirrored brain organization: Statistical anomaly or reversal of hemispheric functional segregation bias? Proceedings of the National Academy of Sciences (USA), 117(25), 14057–14065. https://doi.org/10.1073/pnas.2002981117

Goldenberg, G. (2013). Apraxia in left-handers. Brain, 136, 2592–2601. https://doi.org/10.1093/brain/awt181

Goodale, M. A., Króliczak, G., & Westwood, D. A. (2005). Dual routes to action: contributions of the dorsal and ventral streams to adaptive behavior. Progress in Brain Research, 149, 269–283. https://doi.org/10.1016/S0079-6123(05)49019-6

Haberling, I. S., & Corballis, M. C. (2015). Cerebellar asymmetry, cortical asymmetry and handedness: Two independent networks. Laterality: Asymmetries of Body, Brain and Cognition, 19, 1–18. https://doi.org/10.1080/1357650X.2015.1110161

Homberg, V. (2013). Neurorehabilitation approaches to facilitate motor recovery. Handbook of Clinical Neurology, 110, 161–173. https://doi.org/10.1016/B978-0-444-52901-5.00014-9

Jenkinson, M., Beckmann, C. F., Behrens, T. E., Woolrich, M. W., & Smith, S. M. (2012). Fsl. Neuroimage, 62(2), 782–790. https://doi.org/10.1016/j.neuroimage.2011.09.015

Johnstone, L. T., Karlsson, E. M., & Carey, D. P. (2020). The validity and reliability of quantifying hemispheric specialisation using fMRI: Evidence from left and right handers on three different cerebral asymmetries. Neuropsychologia, 138, 107331. https://doi.org/10.1016/j.neuropsychologia.2020.107331

Johnstone, L. T., Karlsson, E. M., & Carey, D. P. (2021). Left-Handers Are Less Lateralized Than Right-Handers for Both Left and Right Hemispheric Functions. Cerebral Cortex, 31(8), 3780–3787. https://doi.org/10.1093/cercor/bhab048

Karlsson, E. M., Johnstone, L. T., & Carey, D. P. (2019). The depth and breadth of multiple perceptual asymmetries in right handers and non-right handers. Laterality, 24(6), 707–739. https://doi.org/10.1080/1357650X.2019.1652308

Kimura, D. (1983). Speech representation in an unbiased sample of left-handers. Human Neurobiology, 2(3), 147–154. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=6668232

Klichowski, M., Nowik, A. M., Króliczak, G., & Lewis, J. (2020). Functional lateralization of tool-sound and action-word processing in a bilingual brain. Health Psychology Report, 8(1), 10–30. https://doi.org/10.5114/hpr.2020.92718

Knecht, S., Drager, B., Deppe, M., Bobe, L., Lohmann, H., Floel, A., Ringelstein, E. B., & Henningsen, H. (2000). Handedness and hemispheric language dominance in healthy humans. Brain, 123, 2512–2518. https://doi.org/10.1093/brain/123.12.2512

Króliczak, G., Buchwald, M., Kleka, P., Klichowski, M., Potok, W., Nowik, A. M., Randerath, J., & Piper, B. J. (2021a). Manual praxis and language-production networks, and their links to handedness. Cortex, 140, 110–127. https://doi.org/10.1016/j.cortex.2021.03.022

Króliczak, G., Buchwald, M., Kleka, P., Klichowski, M., Potok, W., Nowik, A. M., Randerath, J., & Piper, B. J. (2021b). Manual praxis and language-production networks: An fMRI dataset. https://doi.org/10.17605/OSF.IO/63HJT

Króliczak, G., & Frey, S. H. (2009). A common network in the left cerebral hemisphere represents planning of tool use pantomimes and familiar intransitive gestures at the hand-independent level. Cerebral Cortex, 19(10), 2396–2410. https://doi.org/10.1093/cercor/bhn261

Króliczak, G., Gonzalez, C., & Carey, D. (2019). Editorial: Manual Skills, Handedness, and the Organization of Language in the Brain. Frontiers in Psychology, 10:930, 1–4. https://doi.org/10.3389/fpsyg.2019.00930

Króliczak, G., Piper, B. J., & Frey, S. H. (2011). Atypical lateralization of language predicts cerebral asymmetries in parietal gesture representations. Neuropsychologia, 49(7), 1698–1702. https://doi.org/10.1016/j.neuropsychologia.2011.02.044

Króliczak, G., Piper, B. J., Potok, W., Buchwald, M., Kleka, P., Przybylski, L., & Styrkowiec, P. P. (2020). Praxis and language organization in left-handers. Acta Neuropsychologica, 18(1), 15–28. https://doi.org/10.5604/01.3001.0013.9738

Króliczak, G., Potok, W., & Nowik, A. M. (2020). Język, praksja i ręczność: Delikatna triada z perspektywy leworęczności. Kosmos, 69(1), 123–134. https://doi.org/10.36921/kos.2020_2630

Lesourd, M., Servant, M., Baumard, J., Reynaud, E., Ecochard, C., Medjaoui, F. T., Bartolo, A., & Osiurak, F. (2021). Semantic and action tool knowledge in the brain: Identifying common and distinct networks. Neuropsychologia, 159, 107918. https://doi.org/10.1016/j.neuropsychologia.2021.107918

Liew, S. L., Garrison, K. A., Ito, K. L., Heydari, P., Sobhani, M., Werner, J., Damasio, H., Winstein, C. J., & Aziz-Zadeh, L. (2018). Laterality of Poststroke Cortical Motor Activity during Action Observation Is Related to Hemispheric Dominance. Neural Plasticity, 2018, 3524960. https://doi.org/10.1155/2018/3524960

Malfatti, G., & Turella, L. (2021). Neural encoding and functional interactions underlying pantomimed movements. Brain Structure and Function, 226(7), 2321–2337. https://doi.org/10.1007/s00429-021-02332-6

Mazoyer, B., Zago, L., Jobard, G., Crivello, F., Joliot, M., Perchey, G., Mellet, E., Petit, L., & Tzourio-Mazoyer, N. (2014). Gaussian mixture modeling of hemispheric lateralization for language in a large sample of healthy individuals balanced for handedness. PLoS ONE, 9(6), e101165. https://doi.org/10.1371/journal.pone.0101165

Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9, 97–113. https://doi.org/10.1016/0028-3932(71)90067-4

Osiurak, F., Cretel, C., Uomini, N., Bryche, C., Lesourd, M., & Reynaud, E. (2021). On the Neurocognitive Co-Evolution of Tool Behavior and Language: Insights from the Massive Redeployment Framework. Topics in Cognitive Science, 13(4), 684–707. https://doi.org/10.1111/tops.12577

Potok, W., Maskiewicz, A., Króliczak, G., & Marangon, M. (2019). The temporal involvement of the left supramarginal gyrus in planning functional grasps: A neuronavigated TMS study. Cortex, 111, 16–34. https://doi.org/10.1016/j.cortex.2018.10.010

Przybylski, L., & Króliczak, G. (2017). Planning functional grasps of simple tools invokes the hand-independent praxis representation network: an fMRI study. Journal of the International Neuropsychological Society, 23(2), 108–120. https://doi.org/10.1017/S1355617716001120

Riccardi, N., Yourganov, G., Rorden, C., Fridriksson, J., & Desai, R. (2020). Degradation of Praxis Brain Networks and Impaired Comprehension of Manipulable Nouns in Stroke. Journal of Cognitive Neuroscience, 32(3), 467–483. https://doi.org/10.1162/jocn_a_01495

Rizzolatti, G., & Matelli, M. (2003). Two different streams form the dorsal visual system: anatomy and functions. Experimental Brain Research, 153(2), 146–157. https://doi.org/10.1007/s00221-003-1588-0

Thirion, B., Pinel, P., Meriaux, S., Roche, A., Dehaene, S., & Poline, J. B. (2007). Analysis of a large fMRI cohort: Statistical and methodological issues for group analyses. Neuroimage, 35(1), 105–120. https://doi.org/10.1016/j.neuroimage.2006.11.054

Vingerhoets, G. (2019). Phenotypes in hemispheric functional segregation? Perspectives and challenges. Physics of Life Reviews, 30, 1–18. https://doi.org/10.1016/j.plrev.2019.06.002

Vingerhoets, G., Alderweireldt, A. S., Vandemaele, P., Cai, Q., Van der Haegen, L., Brysbaert, M., & Achten, E. (2013). Praxis and language are linked: evidence from co-lateralization in individuals with atypical language dominance. Cortex, 49(1), 172–183. https://doi.org/10.1016/j.cortex.2011.11.003

Woodhead, Z. V. J., Thompson, P. A., Karlsson, E. M., & Bishop, D. V. M. (2021). An updated investigation of the multidimensional structure of language lateralization in left- and right-handed adults: a test–retest functional transcranial Doppler sonography study with six language tasks. Royal Society Open Science, 8:200696. https://doi.org/10.1098/rsos.200696