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Cover image provided by Ibbl sarl, Lausanne CH ISSN 1664-8714 ISBN 978-2-88919-411-7 DOI 10.3389/978-2-88919-411-7 February 2015 Frontiers in Psychology February 2015 | Lateralization and cognitive systems | 2 Topic Editors: Sebastian Ocklenburg, Ruhr Universität Bochum, Bochum, Germany Christian Beste, Cognitive Neurophysiology, Department of Child and Adolescent Psychiatry, Faculty of Medicine of the TU Dresden, Germany Onur Güntürkün, Ruhr University Bochum, Bochum, Germany Marco Hirnstein, University of Bergen, Bergen, Norway Left-right asymmetries of structure and function are a common organization principle in the brains of humans and non-human vertebrates alike. While there are inherently asymmetric systems such as the human language system or the song system of songbirds, the impact of structural or functional asymmetries on perception, cognition and behavior is not necessarily limited to these systems. For example, performance in experimental paradigms that assess executive functions such as inhibition, planning or action monitoring is influenced by information processing in the bottom-up channel. Depending on the type of stimuli used, one hemisphere can be more efficient in processing than the other and these functional cerebral asymmetries have been shown to modulate the efficacy of executive functions via the bottom-up channel. We only begin to understand the complex neuronal mechanisms underlying this interaction between hemispheric asymmetries and cognitive systems. Therefore, it is the aim of this Research Topics to further elucidate how structural or functional hemispheric asymmetries modulate perception, cognition and behavior in the broadest sense. LATERALIZATION AND COGNITIVE SYSTEMS Frontiers in Psychology February 2015 | Lateralization and cognitive systems | 3 Table of Contents 06 Lateralization and Cognitive Systems Sebastian Ocklenburg, Marco Hirnstein, Christian Beste and Onur Güntürkün 09 Brain and Behavioral Lateralization in Invertebrates Elisa Frasnelli 19 Functional and Structural Comparison of Visual Lateralization in Birds – Similar but Still Different Martina Manns and Felix Ströckens 29 Lateralized Mechanisms for Encoding of Object. Behavioral Evidence From an Animal Model: The Domestic Chick (Gallus Gallus) Rosa Rugani, Orsola Rosa Salva and Lucia Regolin 37 Poor Receptive Joint Attention Skills are Associated with Atypical Gray Matter Asymmetry in the Posterior Superior Temporal Gyrus of Chimpanzees (Pan Troglodytes) William D. Hopkins, Maria Misiura, Lisa A. Reamer, Jennifer A. Schaeffer, Mary C. Mareno and Steven J. Schapiro 45 An Overview of Human Handedness in Twins Syuichi Ooki 50 Differences in Cerebral Cortical Anatomy of Left- and Right-Handers Tulio Guadalupe, Roel M. Willems, Marcel P. Zwiers, Alejandro Arias Vasquez, Martine Hoogman, Peter Hagoort, Guillén Fernández, Jan Buitelaar, Barbara Franke, Simon E. Fisher and Clyde Francks 58 Quantifying Cerebral Asymmetries for Language in Dextrals and Adextrals with Random-Effects Meta Analysis. David P. Carey and Leah T. Johnstone 81 Effect of Handedness on the Occurrence of Semantic N400 Priming Effect in 18- and 24-Month-Old Children Jacqueline Fagard, Louah Sirri and Pia Rämä 89 Perceptual Asymmetries and Handedness: A Neglected Link? Daniele Marzoli, Giulia Prete and Luca Tommasi 98 Degree of Handedness, but not Direction, is a Systematic Predictor of Cognitive Performance Eric Prichard, Ruth E. Propper and Stephen D. Christman 104 Differences Between Left- and Right-Handers in Approach/Avoidance Motivation: Influence of Consistency of Handedness Measures Scott M. Hardie and Lynn Wright Frontiers in Psychology February 2015 | Lateralization and cognitive systems | 4 114 Hand Preference, Performance Abilities, and Hand Selection in Children Sara M. Scharoun and Pamela J. Bryden 129 The Influence of Prior Practice and Handedness on the Orthogonal Simon Effect Cristina Iani, Nadia Milanese and Sandro Rubichi 136 “Right on all Occasions?” – On the Feasibility of Laterality Research Using a Smartphone Dichotic Listening Application Josef J. Bless, René Westerhausen, Joanne Arciuli, Kristiina Kompus, Magne Gudmundsen and Kenneth Hugdahl 146 How Brain Asymmetry Relates to Performance – A Large-Scale Dichotic Listening Study Marco Hirnstein, Kenneth Hugdahl and Markus Hausmann 156 Erratum: How Brain Asymmetry Relates to Performance – A Large-Scale Dichotic Listening Study Marco Hirnstein, Kenneth Hugdahl and Markus Hausmann 157 The Cortical Microstructural Basis of Lateralized Cognition: A Review Steven A. Chance 165 Inferring Common Cognitive Mechanisms From Brain Blood-Flow Lateralization Data: A New Methodology for fTCD Analysis Georg F. Meyer, Amy Spray, Jo E. Fairlie and Natalie T. Uomini 180 Functional Asymmetry and Effective Connectivity of the Auditory System During Speech Perception is Modulated by the Place of Articulation of the Consonant- A 7T fMRI Study Karsten Specht, Florian Baumgartner, Jörg Stadler, Kenneth Hugdahl and Stefan Pollmann 190 The Effects of Visual Half-Field Priming on the Categorization of Familiar Intransitive Gestures, Tool Use Pantomimes, and Meaningless Hand Movements Honorata Helon and Gregory Króliczak 201 Switching Between Global and Local Levels: The Level Repetition Effect and its Hemispheric Asymmetry Luc Keita, Nathalie Bedoin, Jacob A. Burack and Franco Lepore 210 Brain Reorganization as a Function of Walking Experience in 12-Month-Old Infants: Implications for the Development of Manual Laterality Daniela Corbetta, Denise R. Friedman and Martha Ann Bell 220 Hemispheric Asymmetries in Word Recognition as Revealed by the Orthographic Uniqueness Point Effect Cristina Izura, Victoria C. Wright and Natalie Fouquet 226 Task Demands Modulate Decision and Eye Movement Responses in the Chimeric Face Test: Examining the Right Hemisphere Processing Account Jason C. Coronel and Kara D. Federmeier 236 In (or Outside of) Your Neck of the Woods: Laterality in Spatial Body Representation Sylvia Hach and Simone Schütz-Bosbach 248 Lateralization of Spatial Information Processing in Response Monitoring Ann-Kathrin Stock and Christian Beste Frontiers in Psychology February 2015 | Lateralization and cognitive systems | 5 256 Hemispheric Specialization in Selective Attention and Short-Term Memory: A Fine-Coarse Model of Left- and Right-Ear Disadvantages John E. Marsh, Lea K. Pilgrim and Patrik Sörqvist 262 Response Inhibition is Modulated by Functional Cerebral Asymmetries for Facial Expression Perception Sebastian Ocklenburg, Vanessa Ness, Onur Güntürkün, Boris Suchan and Christian Beste 270 Differences Between Visual Hemifields in Identifying Rapidly Presented Target Stimuli: Letters and Digits, Faces, and Shapes Dariusz Asanowicz, Kamila S ’migasiewicz and Rolf Verleger 283 Interhemispheric vs. Stimulus-Response Spatial Compatibility Effects in Bimanual Reaction Times to Lateralized Visual Stimuli Antonello Pellicano, Valeria Barna, Roberto Nicoletti, Sandro Rubichi and Carlo A. Marzi 289 Behavioral Laterality of the Brain: Support for the Binary Construct of Hemisity Bruce E. Morton 301 Lateralized Difference in Tympanic Membrane Temperature: Emotion and Hemispheric Activity Ruth E. Propper and Tad T. Brunyé 308 An Asymmetric Inhibition Model of Hemispheric Differences in Emotional Processing Gina M. Grimshaw and David Carmel EDITORIAL published: 08 October 2014 doi: 10.3389/fpsyg.2014.01143 Lateralization and cognitive systems Sebastian Ocklenburg 1 *, Marco Hirnstein 2 , Christian Beste 3 and Onur Güntürkün 1 1 Biopsychology, Institute of Cognitive Neuroscience, Ruhr-University Bochum, Bochum, Germany 2 Bergen fMRI Group, Department of Biological and Medical Psychology, University of Bergen, Bergen, Norway 3 Cognitive Neurophysiology, Department of Child and Adolescent Psychiatry, Faculty of Medicine of the Technische Universität Dresden, Dresden, Germany *Correspondence: sebastian.ocklenburg@rub.de Edited and reviewed by: Bernhard Hommel, Leiden University, Netherlands Keywords: handedness, executive function, laterality, lateralization, hemispheric asymmetry, brain, language, brain structure Lateralization of brain and behavior in both humans and non- human animals is a topic that has fascinated neuroscientists since its initial discovery in the mid of the nineteenth century (Broca, 1861; Dax, 1865; Oppenheimer, 1977; Ströckens et al., 2013). Hemispheric asymmetries are abundant in the anatomy, neuro- chemistry and cytoarchitecture of the vertebrate brain and over the decades, a number of cognitive abilities have been shown to heavily rely on lateralized processing in the brain, the most widely investigated being language (Corballis, 2012; Ocklenburg et al., 2013b). Other cognitive domains that depend on lateral- ized processing include emotional processing (Önal-Hartmann et al., 2012), face and body perception (Thoma et al., 2014), spa- tial attention (Duecker et al., 2013), fine motor skills (Arning et al., 2013) and memory (Habib et al., 2003)—just to name a few. However, the impact of lateralization of brain func- tion is not limited to these “classical” domains of lateralization research. The efficiency of higher cognitive processes in the ver- tebrate brain does not only depend on the involved cognitive systems themselves, but also on earlier information process- ing stages (Knudsen, 2007). Therefore, functional hemispheric asymmetries in stimulus processing can affect the efficiency of virtually any cognitive domain. This principle has recently been demonstrated for executive functions mediated by fronto-striatal networks, including working memory processes (Beste et al., 2010a,b, 2011, 2012). Ocklenburg et al. (2011, 2012) could show that the efficiency of executive functions like response inhibi- tion or task switching is modulated when functional hemispheric asymmetries affect stimulus processing. Based on these observations, the present Frontiers in Cognition Research Topic aimed to further investigate the rela- tionship of lateralization and cognitive systems in the vertebrate brain. Overall, the Research Topic encompasses more than 30 novel publications, ranging from Original Research Articles to Reviews and Mini Reviews, Perspective Articles and Hypothesis and Theory Articles. From the beginning, the present Research Topic was conceptualized with a comparative multi-disciplinary inter-species approach in mind. This idea is reflected in the broad diversity of animal models included in the Research Topic, rang- ing from invertebrates (Frasnelli, 2013) to different species of birds (Manns and Ströckens, 2014; Rugani et al., 2014) and pri- mates (Hopkins et al., 2014). In addition to animal research, sev- eral studies examined how lateralization impacts the functioning of different cognitive systems in the human brain. For example, it was investigated how handedness is related to other brain func- tions such as language lateralization (Carey and Johnstone, 2014), approach/avoidance motivation (Hardie and Wright, 2014), per- ceptual asymmetries (Marzoli et al., 2014), semantic priming (Fagard et al., 2014), response speed in the orthogonal Simon task (Iani et al., 2014) and cognitive performance in general (Prichard et al., 2013; Scharoun and Bryden, 2014). These stud- ies are complemented by a review article investigating how twin studies could be useful in the quest to understand the complex interrelations of lateralization and cognitive systems (Ooki, 2014) as well as by a large-scale anatomical work investigating the effect of handedness on the structure of the cerebral cortex (Guadalupe et al., 2014). The relation of structural and functional asymme- tries was also the topic of review article that investigated the cortical microstructural basis of lateralized cognition (Chance, 2014). Moreover, several authors investigated auditory lateral- ization (e.g., Specht et al., 2014). For example, Hirnstein et al. (2014a; Erratum in Hirnstein et al., 2014b) investigated how lan- guage lateralization measured with the Dichotic Listening Task relates to cognitive performance. The same task was used in a new smartphone version by Bless et al. (2013) who investigated the feasibility of conducting research on the interaction between lat- eralization and cognitive systems using a smartphone application. With more than 5500 article views and an AM score of more than 50 by the time this editorial was written, this article has gained more online attention than almost any other work published in Frontiers in Cognition. Other authors investigated visual lateral- ization (Asanowicz et al., 2013; Pellicano et al., 2013; Helon and Króliczak, 2014), asymmetries in emotional processing (Propper and Brunyé, 2013; Grimshaw and Carmel, 2014), behavioral later- alization (Morton, 2013; Corbetta et al., 2014), and asymmetries in face (Coronel and Federmeier, 2014) and body representation (Hach and Schütz-Bosbach, 2014), as well as in word generation (Meyer et al., 2014) and word recognition (Izura et al., 2014). Finally, some authors also investigated the impact of lateralized processing on executive functioning, the topic which had initially inspired this Research Topic (Marsh et al., 2013; Ocklenburg et al., 2013a; Kéïta et al., 2014; Stock and Beste, 2014). Taken together, the wide variety of cognitive systems in differ- ent species covered in the present Research Topic highlights the enormous importance of understanding how and why the verte- brate brain is asymmetrically organized for almost any subfield within cognitive neuroscience. We hope that the excellent papers www.frontiersin.org October 2014 | Volume 5 | Article 1143 | 6 Ocklenburg et al. Lateralization and cognitive systems assembled in the present Research Topic will help to stimulate more research aimed at understanding the complex mechanisms underlying the interaction between hemispheric asymmetries in stimulus perception and higher cognitive systems. REFERENCES Arning, L., Ocklenburg, S., Schulz, S., Ness, V., Gerding, W. 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Hand preference, performance abilities, and hand selection in children. Front. Psychol. 5:82. doi: 10.3389/fpsyg.2014.00082 Specht, K., Baumgartner, F. J., Stadler, J., Hugdahl, K., and Pollmann, S. (2014). Functional asymmetry and effective connectivity of the auditory system during speech perception is modulated by the place of articulation of the consonant- A 7T fMRI study. Front. Psychol. 5:549. doi: 10.3389/fpsyg.2014.00549 Stock, A. K., and Beste, C. (2014). Lateralization of spatial information processing in response monitoring. Front. Psychol. 5:22. doi: 10.3389/fpsyg.2014.00022 Ströckens, F., Güntürkün, O., and Ocklenburg, S. (2013). Limb preferences in non-human vertebrates. Laterality 18, 536–575. doi: 10.1080/1357650X.2012. 723008 Thoma, P., Soria Bauser, D., Norra, C., Brüne, M., Juckel, G., and Suchan, B. (2014). Do you see what I feel?–Electrophysiological correlates of emotional face and body perception in schizophrenia . Clin. Neurophysiol. 125, 1152–1163. doi: 10.1016/j.clinph.2013.10.046 Conflict of Interest Statement: The authors declare that the research was con- ducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received: 17 September 2014; accepted: 19 September 2014; published online: 08 October 2014. Citation: Ocklenburg S, Hirnstein M, Beste C and Güntürkün O (2014) Lateralization and cognitive systems. Front. Psychol. 5 :1143. doi: 10.3389/fpsyg.2014.01143 This article was submitted to Cognition, a section of the journal Frontiers in Psychology. Copyright © 2014 Ocklenburg, Hirnstein, Beste and Güntürkün. This is an open- access article distributed under the terms of the Creative Commons Attribution License (CC BY). 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No use, distribution or reproduction is permitted which does not comply with these terms. www.frontiersin.org October 2014 | Volume 5 | Article 1143 | 8 REVIEW ARTICLE published: 11 December 2013 doi: 10.3389/fpsyg.2013.00939 Brain and behavioral lateralization in invertebrates Elisa Frasnelli* Center for Mind/Brain Sciences, University of Trento, Rovereto, Italy Edited by: Marco Hirnstein, University of Bergen, Norway Reviewed by: Christelle Jozet-alves, Université de Caen Basse-Normadie, France Rena Klose, Ruhr-University Bochum, Germany *Correspondence: Elisa Frasnelli, Center for Mind/Brain Sciences, University of Trento, Corso Bettini 31, I-38068 Rovereto, Italy e-mail: elisa.frasnelli@unitn.it Traditionally, only humans were thought to exhibit brain and behavioral asymmetries, but several studies have revealed that most vertebrates are also lateralized. Recently, evidence of left–right asymmetries in invertebrates has begun to emerge, suggesting that lateralization of the nervous system may be a feature of simpler brains as well as more complex ones. Here I present some examples in invertebrates of sensory and motor asymmetries, as well as asymmetries in the nervous system. I illustrate two cases where an asymmetric brain is crucial for the development of some cognitive abilities. The first case is the nematode Caenorhabditis elegans , which has asymmetric odor sensory neurons and taste perception neurons. In this worm left/right asymmetries are responsible for the sensing of a substantial number of salt ions, and lateralized responses to salt allow the worm to discriminate between distinct salt ions. The second case is the fruit fly Drosophila melanogaster , where the presence of asymmetry in a particular structure of the brain is important in the formation or retrieval of long-term memory. Moreover, I distinguish two distinct patterns of lateralization that occur in both vertebrates and invertebrates: individual- level and population-level lateralization. Theoretical models on the evolution of lateralization suggest that the alignment of lateralization at the population level may have evolved as an evolutionary stable strategy in which individually asymmetrical organisms must coordinate their behavior with that of other asymmetrical organisms. This implies that lateralization at the population-level is more likely to have evolved in social rather than in solitary species. I evaluate this new hypothesis with a specific focus on insects showing different level of sociality. In particular, I present a series of studies on antennal asymmetries in honeybees and other related species of bees, showing how insects may be extremely useful to test the evolutionary hypothesis. Keywords: brain and behavioral lateralization, invertebrates, individual efficiency, directional asymmetry, evolu- tionary stable strategy, bee, sociality INTRODUCTION Until some decades ago, it was widely and incorrectly assumed that lateralization of structure and behavior was unique to the human brain, and having a lateralized brain was a mark of the cognitive superiority of humans. Now it is well known that most vertebrates have strong left–right asymmetries in their brain and in their behavior and lateralization is widespread in the verte- brate subphylum (for a review on handedness, see Ströckens et al., 2013; for a review on language lateralization, see Ocklenburg et al., 2013). Moreover, lateralization has a similar plan of organiza- tion in different species (for a review, see Rogers et al., 2013a). Recently, new evidence has shown the presence of lateralization in invertebrate species, suggesting that lateralization of the ner- vous system may be a feature of simpler brains as well as more complex ones (for a fully comprehensive review, see Frasnelli et al., 2012a). Some invertebrates show a lateralized behavior in motor control, other species exhibit asymmetries in several sen- sory modalities, such as in olfaction or vision, and in some cases behavioral lateralization seems to be correlated with a morpho- logical one. In this section I present briefly some examples. In the second section I focus on two examples of brain asymme- tries in invertebrates – fruit fly and nematode – that show how lateralization at the individual level is important to perform spe- cific cognitive abilities. Then, in the third section, I explain that two patterns of lateralization exist, i.e., individual level and popu- lation level lateralization, I discuss how the latter may have evolved as an evolutionary stable strategy (ESS) and I focus on insects to provide evidence to test the ESS hypothesis. Finally, in the forth and last section, I conclude by comparing lateralization in inver- tebrates and vertebrates and discussing its possible evolutionary origins. MOTOR ASYMMETRIES Ants ( Formicidae ) and spiders ( Araneae ) were found to be later- alized (Heuts et al., 2003). A significant majority of spiders were observed to have mainly left leg lesions, and the process of catch- ing them caused less severe leg lesions that were also significantly biased to the left. Similarly, Ades and Ramires (2002) showed that the spitting spider Scytodes globula (Arachnida, Araneae, Scytodi- dae) uses its left anterior legs considerably more frequently than the right anterior legs during prey handling. Twelve ant species of Lasius niger kept mainly to the right on their foraging “streets,” whereas there was only one species that kept to the left (Heuts et al., 2003). www.frontiersin.org December 2013 | Volume 4 | Article 939 | 9 Frasnelli Brain and behavioral lateralization in invertebrates Behavior of the common American cockroach, Periplaneta americana (Linnaeus) has been investigated to determine whether lateralization is evident in a bias to turn left or right (Cooper et al., 2011). The cockroaches were allowed to run through a Y-tube and make a choice of which direction to take. Vanilla and ethanol were placed randomly at the ends of the Y-tube to entice the cockroaches to reach the end of the tubes. Thirty-eight adult cockroaches were tested for each of the following five conditions: both antennae intact, half of the left antenna cut, all of the left antenna cut, half of the right antenna cut, and all of the right antenna cut. Results showed that the odors of vanilla and ethanol play an insignificant role in the decision-making. Injury of one antenna affected the choice of direction, but not in a consistent way. While the majority of cockroaches with an amputated left antenna chose to go right, this did not happen when the entire right antenna was removed. In fact, similar injuries to either the right or the left antenna revealed an innate bias for turning right. Similar results were obtained when either antenna was cut in half. More evident was the skew towards the right path when both antennae were intact. The antennae of these gregarious insects are very long and, in addition to their role in detecting chemi- cals, they are very important as tactile organs (Okada and Toh, 2004). The study by Cooper et al. (2011) thus suggests that Peri- planeta americana has a motor bias towards the right and not that this species is right-side dominant in its tactile and odor senses. Cockroaches turn right when there is no sensory input from the antennae, showing that they have a motor bias, and input from the antennae modifies this motor bias, often to reduce its strength. Evidence of lateralized behavior has been found in the giant water bugs, Belostoma flumineum Say (Heteroptera: Belostomati- dae; Kight et al., 2008). Giant water bugs are large aquatic insects, predators of other aquatic invertebrates, and small fishes. Bugs were trained to swim left or right in a T-maze and a significant preference to turn left, even when not reinforced, was observed, revealing a naïve bias in this species. To control for environmental cues that might bias the turning direction of water bugs in the maze, Kight et al. (2008) ran two separate experiments on inde- pendent groups of 20 water bugs. Both experiments were identical with the exception that, after the first group of 20 water bugs had been tested, the maze apparatus was rotated 180 ◦ , thereby reversing the polarity of all directional environmental cues such as lighting or electromagnetic fields. Again the same left turn ten- dency was observed. Hence, the explanation of the presence of this bias could be the existence of asymmetries in the nervous system or asymmetric exoskeletal morphology (i.e., leg length) that could cause biased swimming behavior. PERCEPTUAL ASYMMETRIES Fruit flies Drosophila melanogaster present a consistent asym- metry in the antenna-mediated flight control, in which the sensory signals coming from the left antenna contribute more to odor tracking than the sensory signals coming from the right antenna (Duistermars et al., 2009). The rapid odor lateraliza- tion in Drosophila is enabled by an asymmetric neurotransmitter release (Gaudry et al., 2013): each olfactory receptor neuron (ORN) spike releases ∼ 40% more neurotransmitter from the axon branch ipsilateral to the soma, as compared to the con- tralateral branch. This implies that, when an odor activates the antennae asymmetrically, ipsilateral central neurons begin to spike a few milliseconds before contralateral neurons, and ipsilateral central neurons also fire at a 30–50% higher rate. As a conse- quence, a walking fly can detect a 5% asymmetry in total ORN input to its left and right antennal lobes, and can turn toward the odor in less time than it requires the fly to complete a stride (Gaudry et al., 2013). Red wood ants Formica aquilonia were found to use mainly their right antenna during “feeding” contacts where a “donor” ant exchanges food with a “receiver” ant through trophallaxis (Frasnelli et al., 2012b). Honeybees Apis mellifera seemed