The Brain's Asymmetric Frequency Tuning

The Brain's Asymmetric Frequency Tuning

S S symmetry Opinion The Brain’s Asymmetric Frequency Tuning: Asymmetric Behavior Originates from Asymmetric Perception Arianna Felisatti 1,*, David Aagten-Murphy 1,2, Jochen Laubrock 1,3, Samuel Shaki 4 and Martin H. Fischer 1 1 Department of Psychology, University of Potsdam, Karl-Liebknecht-Strasse 24-25 House 14, D-14476 Potsdam OT Golm, Germany; [email protected] (D.A.-M.); [email protected] (J.L.); [email protected] (M.H.F.) 2 Neuraltrain GmbH, Friedrichstr. 68, 10117 Berlin, Germany 3 Department of Psychology, Brandenburg Medical School Theodor Fontane Fehrbelliner Straße 38, 16816 Neuruppin, Germany 4 Department of Behavioral Sciences and Psychology, Ariel University, Ariel 40700, Israel; [email protected] * Correspondence: [email protected]; Tel.: +49-331-977-2895 Received: 11 September 2020; Accepted: 10 December 2020; Published: 15 December 2020 Abstract: To construct a coherent multi-modal percept, vertebrate brains extract low-level features (such as spatial and temporal frequencies) from incoming sensory signals. However, because frequency processing is lateralized with the right hemisphere favouring low frequencies while the left favours higher frequencies, this introduces asymmetries between the hemispheres. Here, we describe how this lateralization shapes the development of several cognitive domains, ranging from visuo-spatial and numerical cognition to language, social cognition, and even aesthetic appreciation, and leads to the emergence of asymmetries in behaviour. We discuss the neuropsychological and educational implications of these emergent asymmetries and suggest future research approaches. Keywords: asymmetry; global/local; spatial frequencies; temporal frequencies; embodied cognition 1. Introduction “The universe is asymmetric and I am persuaded that life, as it is known to us, is a direct result of the asymmetry of the universe or of its indirect consequences.” —Louis Pasteur Decades of research have revealed that our symmetrical anatomical arrangement of body, eyes, and brain obscures many surprising asymmetries in how our bodies sample the external world and later act upon it. In this review, we aim to address how sensory asymmetries interact with and drive functional changes and—in turn—influence and shape our behaviours, preferences, and even our cultural norms. We begin by describing behavioral, neuropsychological, neuroimaging, and comparative evidence for behavioral asymmetries that result from competition between global and local visual processing. Then, we describe models of processing asymmetries that aim to account for these findings. Based upon these reported results, we then introduce a new theoretical model to account for how brain functional lateralization, spatial frequency tuning, and object location in the external world relative to the observer interact to generate asymmetrical actions. This model is subsequently applied to higher-level cognitive asymmetries to illustrate its broader viability and explanatory power. We end our review by listing a few implications and outstanding questions. Symmetry 2020, 12, 2083; doi:10.3390/sym12122083 www.mdpi.com/journal/symmetry Symmetry 2020, 12, 2083 2 of 25 2. Global vs. Local Perception ASymmetry growing 2020,number 12, x FOR PEER of studies REVIEW suggest that perceptual and behavioral asymmetries originate2 of 26 from hemispheric lateralization. The left hemisphere is more efficient in the selection of fine detail, while the 2. Global vs. Local Perception right hemisphere is predominant in the selection of coarse elements [1–3]. Due to the cross-over of the optic fibres,A growing each number visual hemi-fieldof studies suggest projects that to perceptual the contralateral and behavioral brain hemisphere. asymmetries Here,originate we will specificallyfrom hemispheric review studies lateralization on visuo-spatial. The left hemisphere processing is more to explain efficient how in the this selection organization of fine shapesdetail, the while the right hemisphere is predominant in the selection of coarse elements [1–3]. Due to the cross- development of several cognitive domains. over of the optic fibres, each visual hemi-field projects to the contralateral brain hemisphere. Here, Wewe beginwill specifically our review review by reminding studies on readersvisuo-spatial of a seminal processing behavioral to explain study how conductedthis organization by Navon (1977)shapes [4]. He the presenteddevelopment artificially of several createdcognitive hierarchical domains. stimuli in the centre of participants’ visual field (seeWe Figure begin1, our central review panel). by reminding The stimuli readers were of a letter-shapedseminal behavioral figures study made conducted from manyby Navon smaller letters,(1977) and [4] participants. He presented had artificially to respond created either hierarchical to the stimuli global in or the the centre local of letter participants’ information visual with assignedfield button(see Figure responses. 1, central Importantly, panel). The globalstimuli andwere local letter letters-shaped could figures be made either from response-incongruent many smaller or response-congruentletters, and participa (withoutnts had to necessarily respond either being to identical).the global or Navon the local (1977) letter [4 ]information reported anwith overall processingassigned speed button advantage responses. for Importantly, the global global level, and and local asymmetrical letters could interference,be either response which-incongruent was stronger or response-congruent (without necessarily being identical). Navon (1977) [4] reported an overall from the global to the local level than in the reverse direction. Together, these findings suggested processing speed advantage for the global level, and asymmetrical interference, which was stronger a coarse-to-fine visual processing sequence. An aspect of the stimuli influencing the salience of from the global to the local level than in the reverse direction. Together, these findings suggested a the globalcoarse/-localto-fine level visual is processing the low-pass sequence./high-pass An aspect filter. of Thethe stimuli low-pass influencing filtered the images salience (see of Figure the 1, left panel)global/local retain level the unifyingis the low big-pass global/high- structurepass filter. while The low removing-pass filtered the numerous images (see little Fig details.ure 1, left On the contrary,panel) high-pass retain the filtered unifying images big global (see structure Figure1, while right panel)removing retain the numerous the numerous little littledetails details. On the while removingcontrary, the high unifying-pass filtered big global images structure. (see Figure Since 1, right this panel) seminal retain work,the numerous there havelittle details been numerouswhile behavioural,removing neuropsychological, the unifying big global neuroimaging, structure. Since and this comparative seminal work, studies there of thesehave “globalbeen numerous precedence” and “globalbehavioural/local, interference”neuropsychological, effects. neuroimaging We review this, and research comparative here selectively studies toof illustrate these “global the current understandingprecedence” of and visual “global/local processing interference” asymmetries. effects. We review this research here selectively to illustrate the current understanding of visual processing asymmetries. FigureFigure 1. Example 1. Example of of hierarchical hierarchical stimulus stimulus beforebefore and and after after a alow low-pass-pass/high/high-pass-pass filter. filter. CentralCentral panel: example of hierarchical stimulus with letter “H” at the global level and letter “S” at the local panel: example of hierarchical stimulus with letter “H” at the global level and letter “S” at the local level. Left panel: low-pass filtered stimulus. Right panel: high-pass filtered stimulus. level. Left panel: low-pass filtered stimulus. Right panel: high-pass filtered stimulus. 2.1. Behavioral2.1. Behavioral Evidence Evidence In addition to the Navon task, there are multiple other sources of behavioural evidence for In addition to the Navon task, there are multiple other sources of behavioural evidence for hemispheric lateralization for global/local processing. Neural development is associated with hemisphericprogressive lateralization maturation forof the global corpus/local callosum processing., which is Neural a bundle development of fibres supporting is associated inter- with progressivehemispheric maturation communication. of the corpus Investigation callosum ,of which hemispheric is a bundle asymmetries of fibres in supportinghealthy populations inter-hemispheric relies communication. Investigation of hemispheric asymmetries in healthy populations relies on the use Symmetry 2020, 12, 2083 3 of 25 of lateralized stimulus presentation by means of hemi-field paradigms (consider Reference [5] for meta-analysis and Reference [6] for methodological considerations). Global stimuli are better perceived when briefly shown on the left side of the fixation point. However, local stimuli are better perceived when briefly displayed on the right side of the fixation point [7–11]. In addition, handedness, which is related to hemispheric asymmetry, influences local/global processing. In everyday life, we use our dominant hand to deal with fine-scale and uni-manual tasks [12]. By testing right-handers, Stankovi´cand Neši´c(2018) [13] reported how contraction of the right hand, activating the left hemisphere,

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