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Brain Lateralization: a Comparative Perspective Physiological Reviews Review Article BRAIN LATERALIZATION: A COMPARATIVE PERSPECTIVE GRAPHICAL ABSTRACT AUTHORS Onur Güntürkün, Felix Ströckens, and Sebastian Ocklenburg CORRESPONDENCE [email protected] KEYWORDS birds; cerebral asymmetry; commissures; evolution; language; nodal; zebrafish CLINICAL HIGHLIGHTS Brain asymmetries are key components of sensory, cognitive, and motor systems of humans and other animals. This review tracks their development from embryological asymmetries of genetic expression patterns up to left-right differences of neural networks in adults. These insights are crucial to understand pathologies of the lateralized human brain. Güntürkün et al., 2020, Physiol Rev 100: 1019–1063 April 1, 2020; © 2020 the American Physiological Society https://doi.org/10.1152/physrev.00006.2019 Downloaded from journals.physiology.org/journal/physrev at Univ of Victoria (142.104.240.194) on April 4, 2020. Physiol Rev 100: 1019–1063, 2020 Published April 1, 2020; doi:10.1152/physrev.00006.2019 BRAIN LATERALIZATION: A COMPARATIVE PERSPECTIVE Onur Güntürkün, Felix Ströckens, and Sebastian Ocklenburg Department of Biopsychology, Institute of Cognitive Neuroscience, Ruhr University Bochum, Bochum, Germany Güntürkün O, Ströckens F, Ocklenburg S. Brain Lateralization: A Comparative Perspective. Physiol Rev 100: 1019–1063, 2020. Published April 1, 2020; doi:10.1152/physrev.00006. 2019.—Comparative studies on brain asymmetry date back to the 19th century but then largely disappeared due to the assumption that lateralization is uniquely human. Since the reemergence of this field in the 1970s, we learned that left-right differences of brain and behavior exist throughout the animal kingdom and pay off in terms of sensory, cognitive, and motor efficiency. Ontogenetically, lateralization starts in many species with asymmetrical expression patterns of genes within the Nodal cascade that set up the scene for later complex interactions of genetic, environmental, and epigenetic factors. These take effect during different time points of ontogeny and create asymme- tries of neural networks in diverse species. As a result, depending on task demands, left- or right-hemispheric loops of feedforward or feedback projections are then activated and can tempo- rarily dominate a neural process. In addition, asymmetries of commissural transfer can shape lateralized processes in each hemisphere. It is still unclear if interhemispheric interactions depend on an inhibition/excitation dichotomy or instead adjust the contralateral temporal neural structure to delay the other hemisphere or synchronize with it during joint action. As outlined in our review, novel animal models and approaches could be established in the last decades, and they already produced a substantial increase of knowledge. Since there is practically no realm of human perception, cognition, emotion, or action that is not affected by our lateralized neural organization, insights from these comparative studies are crucial to understand the functions and pathologies of our asymmetric brain. birds; cerebral asymmetry; commissures; evolution; language; nodal; zebrafish I. INTRODUCTION: HISTORY OF... 1019 ulty of spoken language to the Société d’anthropologie in Paris II. HOW ASYMMETRIES EMERGE 1028 (60). His presentation summarized his work of the last five III. THE LATERALIZED BRAIN... 1034 years in which he first analyzed speech deficits of patients to IV. HEMISPHERIC ASYMMETRIES... 1037 then meticulously reconstruct the damaged parts of their V. ASYMMETRIES IN EMOTIONAL... 1044 brains. His paper ended with the famous statement “Nous VI. SUMMARY 1050 parlons avec l’hémisphère gauche” (“We speak with the left hemisphere,” Broca, 1865, p. 384). The insights provided on this afternoon forever demolished two central scientific dogmata of 19th century, made Broca immortal, and Brain asymmetries are key components of sensory, cognitive, marked the onset of cerebral asymmetry research. But the and motor systems of humans and other animals. This review scientific events that unfolded around this time in France are tracks their development from embryological asymmetries of not only a testimony of the past, but are responsible for the genetic expression patterns up to left-right differences of neural networks in adults. These insights are crucial to understand century-long neglect of the comparative perspective of pathologies of the lateralized human brain. brain asymmetries, the limited number of animal models in this field, and our consequential lack of in-depth knowledge on the neurobiological foundations of cerebral left-right I. INTRODUCTION: HISTORY OF differences. COMPARATIVE RESEARCH ON LATERALIZATION B. Scientific Dogmata that Blocked the Path A. Broca’s Discovery and Its Consequences The most important neuroscientific dispute of the first half of the 19th century concerned the question whether the On Thursday, June 15, 1865, the young physician Pierre Paul cortex can be subdivided into functional entities or is orga- Broca (1824–1880) delivered his paper on the seat of the fac- nized as a holistic structure in which each part serves all 0031-9333/20 Copyright © 2020 the American Physiological Society 1019 Downloaded from journals.physiology.org/journal/physrev at Univ of Victoria (142.104.240.194) on April 4, 2020. GÜNTÜRKÜN ET AL. mental functions (204). The person who strongly advocated tions of the dorsal and ventral horns of the spinal cord a functional topography of the cortex was Franz Joseph (300). Later on, he also studied motor functions of the Gall (1758–1828), a German neuroanatomist who fasci- cerebellum and the basal ganglia (301, 302). Additionally, nated lay people throughout Europe but was dismissed as a other early animal researchers discovered that the cerebel- charlatan by his fellow scientists. Gall had observed that lum was a key structure in the production of organized several colleagues with high verbosity and an excellent movement patterns (135, 416). However, all of these dis- memory for text passages had protuberant and baggy eyes. coveries on functional topographies were related to subcor- Being an excellent neuroanatomist, he knew that large in- tical structures. The key concern of scientists of the early dividual differences of brain shape and size exist. Thus he 19th century, however, was the cortex. And here, the con- assumed that these people had especially enlarged retro- clusion of Flourens that no cortical functional subdivisions and supraorbital cortical areas that pushed the eyeballs to exist was readily accepted by the majority of scientists, and the front and down. From this hypothesis it was only a soon the holistic functional nature of the cortex became a small step to conclude that the seat of language faculties had scientific dogma. to be located in the frontal lobes in an area surrounding the eye sockets. Consequently, he thought that we should be Clinical scientists, however, objected. One of them was able to discover the seat of further functions by tracking Jean-Baptiste Bouillaud (1796–1881) who later on became bulging spots on the uneven surface of the cortex of people president of the French Académie de Médecine. Bouillaud with exaggerated mental abilities or characters. Gall further argued that clinicians often observe specific motor or sen- assumed that it would suffice to analyze the landscape of the sory deficits in patients with circumscribed brain lesions. skull since it should reflect the shape of the underlying cor- So, there must be a cortical functional map. Although Bouil- tex (153). Armed with this theory, he analyzed the heads of laud was fully aware how much the ideas of Gall were great poets, spirituals leaders, cruel murderers, and many dismissed in the scientific community, he defended the idea more to come up with the cortical localization of 26 mental of the frontal seat of language based on large numbers of faculties like vanity, courage, mercy, etc. Accompanied by carefully conducted patient studies (45). Several colleagues his assistant Johann Spurzheim, a servant, two monkeys, countered Bouillaud’s arguments by reporting a phasic pa- numerous skulls, and colored plaster casts, he then started tient with lesions in temporal or parietal areas or cases with on a hugely successful tour through the public lecture halls frontal lesions without language problems (277). One core of Europe and convinced many people of his idea of “phre- problem of this time was a lack of awareness that expressive nology” (277). Scientists of his time, however, were out- and receptive language problems should be distinguished raged by his poor conclusions and soon (and since then) and are differently localized. Only much later, Carl Wer- phrenology became a catchword for a sloppy way to map nicke (1884–1905) could clarify this issue by disambiguat- cortical functions. This quick and negative response made it ing between what is now called Wernicke’s and Broca’s area later difficult to realize that Gall could have been right, but (506). A further problem was the unawareness of language for the wrong reasons. asymmetry. As reconstructed a century later, most of the reports on negative cases that were thrown against Bouil- The main counterargument to Gall was put forward by the laud had had right hemisphere lesions (32). young anatomist Marie-Jean-Pierre Flourens (1794–1867) who conducted careful lesion experiments with pigeons and The second, equally important dogma of this time relates to many more animal species. After ablating diverse regions of the
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