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Valentino Braitenberg: from Neuroanatomy to Behavior and Back

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Valentino Braitenberg: from Neuroanatomy to Behavior and Back Biol Cybern (2014) 108:527–539 DOI 10.1007/s00422-012-0533-3 REVIEW Valentino Braitenberg: From neuroanatomy to behavior and back Mario Negrello Received: 22 April 2012 / Accepted: 15 October 2012 / Published online: 13 March 2013 © The Author(s) 2013. This article is published with open access at Springerlink.com Abstract This article compiles an expose of Valentino Bra- bring us to better understand ourselves, and ourselves in the itenberg’s singular view on neuroanatomy and neuroscience. world.Throughtheworkofgreatmen,weapproachthatideal. The review emphasizes his topologically informed work on In great minds, tenacity is augmented by the ability to neuroanatomy and his dialectics of brain-based explanations channel the product of observations with clarity and flair. In of motor behavior. Some of his early ideas on topologically their descriptions the reality beneath the experiment becomes informed neuroanatomy are presented, together with some of alive, unencumbered by jargon, wants to speak itself. The his more obscure work on the taxonomy of neural fiber bun- constraints imposed by experiment rather than nuisances, dles and synaptic arborizations. His functionally informed appear as scaffolds. For them, nature both suggests and takes interpretations of neuroanatomy of the cerebellum, cortex, precedence over theoretical constructs. As a consequence, and hippocampus, are introduced. Finally, we will touch on their prose often reads as if it would have written itself, as if his philosophical views and the inextricable role of function truth yearned for light. in the explanation of neural behavior. This article was conceived before the passing of Valentino Braitenberg, in the hope that he would have the opportunity Keywords Neuroscience · Neuroanatomy · History · to personally review it. Due to that it will likely at times read Braitenberg · Behavioral function as an eulogy, but in that case, I believe, excusably. Braiten- berg was a model of scientific attitude, both sober and jovial, inspired and humble, strict, and flexible. Simultaneously able 1 Prolegomena to capture the essentials in an effortless glance, while swiftly accepting the burden of proof. With clarity, he indicated the Above great achievements, what brings the community to flimsy, the flaky, the incomplete, the obscure, the messy, the admire a scientist is a set of characteristics that transcend missing, meanwhile stressing the necessary, the inescapable, science and knowledge and approach nobility and wisdom. the solid. Sternly, he offered pondered and polished logical Science is a human endeavor with the commendable goal of foundations of his beliefs. understanding reality, in the hope that advancing science will The article attempts to characterize Valentino’s manner This article forms part of a special issue of Biological Cybernetics of doing neuroanatomy and neuroscience while enlisting entitled “Structural Aspects of Biological Cybernetics: Valentino some of his most significant contributions to theory, method, Braitenberg, Neuroanatomy, and Brain Function”. and philosophy of the functional interpretation of neuroanat- B omy. M. Negrello ( ) With the hope of becoming great, we attempt to mirror Computational Neuroscience Laboratory, Okinawa Institute of Science and Technology, Onna Prefecture, Japan ourselves against models. In neuroscience we have great e-mail: [email protected] men to mirror ourselves against. Cajal, Sherrington, Varel- a, Bernstein, von Helmholz, Reichardt, and now Braiten- Present Address: berg. Valentino Braitenberg was a living influence on many, M. Negrello Department of Neuroscience, Erasmus MC, Rotterdam, and his legacy will be there for many to discover and learn The Netherlands from. 123 528 Biol Cybern (2014) 108:527–539 2 Introduction in neuroarchitecture. Through the sibling concepts of sym- metry and invariance, his descriptions obtained a degree of During his six decades of nonstop scientific activity, Val- clarity unusual for statements about neuroanatomy. With the entino Braitenberg spanned broad contributions to neuro- set of topological transformations Braitenberg classified the science opening vast vistas from the standpoint of neuro- cortices. The cortex has rotational invariance, i.e., slices in anatomy. Meticulous, thorough, systematic, and insightful, any vertical plane rotated in any angle are indistinguishable, he furthered staining methods, proposed correction meth- and translational invariance in the two tangential directions ods for tissue shrinkage, contributed to our understanding of (locally). The hippocampus is a 2D sheet, with translational schizophrenia, exposed the computations of myelin bundles, invariance in one direction (along the Schaffer collateral theorized about information and control, advanced our under- pathway), and hence, no rotational invariance, i.e., slices in standing of the hippocampal anatomy, described, quantified, different orientations can be distinguished by whether they and interpreted the architecture of the cerebral and cerebel- are along the pathway or severing it. The cerebellum has no lar cortex, provided the most comprehensive quantification rotational invariance, but has two mirror symmetries, along of the mouse cortex to date, and if that were not enough, the parallel fibers, and perpendicular to them. Furthermore, invented robot psychology. because the pattern between Purkinje cells and parallel fibers This article compiles an expose of Braitenberg’s singu- is repeated along the direction perpendicular to the parallel lar view on neuroanatomy and neuroscience. We illustrate fibers, the cerebellar cortex is essentially one-dimensional. his abilities as a scientific diagrammer, as a taxonomist Not limited to vertebrates, analysis of symmetries includes of connectivities, and his functionally informed interpreta- other arrangements, such as the periodic patterns of the ret- tions of neuroanatomy of the cerebellum, the cortex, and ina and lamina, which imply a rotational group with exactly the hippocampus. Excursi on the philosophy behind his six symmetries. Symmetry features are rich with meaning, observations and opinions will be interspersed within the and in a later section some paragraphs will be devoted to text. Because of his towering output, this review will, per- his inspired suggestions. With such descriptions, it becomes force, have exclusions. Notably, only passing mentions of possible to identify subtle differences [for instance, that the his contributions to insect neuroethology, his deep insights hippocampus does not look all that different from the cor- into theories of cortical function, his theory of language, tex (Braitenberg and Schüz 1983)], and to give discerning and the lauded book “Vehicles” (Braitenberg 1984). These criteria between brain organs. Also the appearance of par- are left for the reader to discover. The review empha- ticular symmetries, such as columns in the visual cortex sizes his topologically informed work on neuroanatomy (Braitenberg and Braitenberg 1979) or the barrel cortex of and his dialectics of brain-based explanations of motor rodents, can be explained with relation to behavior (Braiten- behavior. berg 1977). Through the lenses of topology, the distinctions between cortical areas are amplified, and the need of explanation for 3 The primacy of neuroanatomy these disparities highlighted. Lest his readership should forget, throughout his publications Braitenberg indefatigably reinstated that neuroarchitecture is Some Symmetry Types (from Braitenberg 1999): the grounding for the understanding of the brain. As he put Isotropic networks, with full symmetry (locally). it, “Neuroanatomy is what is left when all the problems of Examples are the amigdala or the caudate nucleus, the neuron are solved” (Braitenberg 1959). Though prima which are invariant to both translations and rotations. facie few would disagree, there are significant variations in Many subcortical structures are locally isotropic. the different approaches on how to proceed with an interpre- Rotationally invariant are the networks that have tation of neuroanatomy. Braitenberg’s unique take involved one preferential direction in which neuronal making sense of the duals of constancy and variability by components are stratified and oriented, as the layers localizing invariances and necessities, those aspects of the of the cerebral cortex, the optic tectum, or the phenomenon that remained unchanged with respect to par- dentate nucleus of the cerebellum. ticular transformations, and then relating them to behavioral Flip symmetry, with two clearly defined directions at and organismic function. right angles to each other—along the third axis the Braitenberg was perhaps the first neuroanatomist to adopt structure repeats homogeneously. E.g., concepts of topology as a tool to describe and understand hippocampus, where perpendicular direction dentate neuroanatomy (Braitenberg and Kemali 1970; Braitenberg gyrus–subiculum, also well defined by the course of 1977, 1999, 1991). The vocabulary of topology provided him hippocampal mossy fibers and schaffer collaterals. with conceptual scalpels to effectively describe differences 123 Biol Cybern (2014) 108:527–539 529 Lattice, with mirror symmetries and translational invariance as in the cerebellum. Translatory symmetry in one direction, as in the spinal cord. Periodic, with discrete translatory symmetry, such as in the periodic ganglia of some insects [e.g., the Lamina of the fly, the central complex of sophisticated insects (Strausfeld et al.
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