Discovering General Principles of Nervous System Organization by Comparing Brain Maps Across Species

Highlights and Perspectives on Evolutionary Neuroscience Brain Behav Evol 2014;83:1–8 Published online: February 28, 2014 DOI: 10.1159/000360152 NSF Workshop Report: Discovering General Principles of Nervous System Organization by Comparing Brain Maps across Species a b c d Georg F. Striedter T. Grant Belgard Chun-Chun Chen Fred P. Davis e f g h i Barbara L. Finlay Onur Güntürkün Melina E. Hale Julie A. Harris Erin E. Hecht j k l m c Patrick R. Hof Hans A. Hofmann Linda Z. Holland Andrew N. Iwaniuk Erich D. Jarvis n o p q r Harvey J. Karten Paul S. Katz William B. Kristan Eduardo R. Macagno Partha P. Mitra s t u v Leonid L. Moroz Todd M. Preuss Clifton W. Ragsdale Chet C. Sherwood w f x o Charles F. Stevens Maik C. Stüttgen Tadaharu Tsumoto Walter Wilczynski a b Department of Neurobiology and Behavior, University of California Irvine, Irvine, Calif. , Semel Institute for Neuroscience and c Human Behavior, University of California Los Angeles, Los Angeles, Calif. , Department of Neurobiology, Duke University, Durham, d e N.C. , Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, Va. , Department of Psychology, Cornell University, f g Ithaca, N.Y. , USA; Department of Psychology, Ruhr University Bochum, Bochum , Germany; Department of Organismal Biology and h i Anatomy, University of Chicago, Chicago, Ill. , Allen Institute for Brain Science, Seattle, Wash. , Department of Psychology, Georgia j State University, Atlanta, Ga. , Fishberg Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount k l Sinai, New York, N.Y. , Department of Cell and Molecular Biology, University of Texas at Austin, Austin, Tex. , Scripps Institution of m Oceanography, University of California San Diego, San Diego, Calif. , USA; Department of Neuroscience, University of Lethbridge, n o Lethbridge, Alta. , Canada; Department of Neurosciences, University of California San Diego, San Diego, Calif. , Neuroscience p q Institute, Georgia State University, Atlanta, Ga. , Sections of Neurobiology and Cell and Developmental Biology, Division of r Biological Sciences, University of California San Diego, San Diego, Calif. , Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y. , s Department of Neuroscience and The Whitney Laboratory for Marine Bioscience, University of Florida, St. Augustine, Fla. , t Division of Neuropharmacology and Neurologic Diseases, Yerkes National Primate Research Center, Emory University, Atlanta, Ga. , u v Department of Neurobiology, University of Chicago, Chicago, Ill. , Department of Anthropology, The George Washington University, w x Washington, D.C. , The Salk Institute for Biological Studies, La Jolla, Calif. , USA; Brain Science Institute RIKEN, Wako , Japan Abstract anatomical, and physiological data. This research will iden- Efforts to understand nervous system structure and function tify which neural features are likely to generalize across spe- have received new impetus from the federal Brain Research cies, and which are unlikely to be broadly conserved. It will through Advancing Innovative Neurotechnologies (BRAIN) also suggest causal relationships between genes, develop- Initiative. Comparative analyses can contribute to this effort ment, adult anatomy, physiology, and, ultimately, behavior. by leading to the discovery of general principles of neural These causal hypotheses can then be tested experimentally. circuit design, information processing, and gene-structure- Finally, insights from comparative research can inspire and function relationships that are not apparent from studies on single species. We here propose to extend the comparative This article is simultaneously published in the Journal of Comparative approach to nervous system ‘maps’ comprising molecular, Neurology (DOI 10.1002/cne.23568). © 2014 John Wiley & Sons, Inc. and S. Karger AG, Basel Georg F. Striedter 0006–8977/14/0831–0001$39.50/0 Department of Neurobiology and Behavior Center for the Neurobiology of Learning and Memory, University of California Irvine E-Mail [email protected] 2205 McGaugh Hall, Irvine, CA 92697-4550 (USA) www.karger.com/bbe E-Mail georg.striedter @ gmail.com Downloaded by: 89.245.253.175 - 3/25/2014 10:12:59 AM guide technological development. To promote this research and distribution must be developed and respected. To that agenda, we recommend that teams of investigators coalesce end, it will help to form networks or consortia of researchers around specific research questions and select a set of ‘refer- and centers for science, technology, and education that fo- ence species’ to anchor their comparative analyses. These cus on organized data collection, distribution, and training. reference species should be chosen not just for practical ad- These activities could be supported, at least in part, through vantages, but also with regard for their phylogenetic posi- existing mechanisms at NSF, NIH, and other agencies. It will tion, behavioral repertoire, well-annotated genome, or other also be important to develop new integrated software and strategic reasons. We envision that the nervous systems of database systems for cross-species data analyses. Multidisci- these reference species will be mapped in more detail than plinary efforts to develop such analytical tools should be sup- those of other species. The collected data may range from ported financially. Finally, training opportunities should be the molecular to the behavioral, depending on the research created to stimulate multidisciplinary, integrative research question. To integrate across levels of analysis and across into brain structure, function, and evolution. species, standards for data collection, annotation, archiving, © 2014 S. Karger AG, Basel Introduction The use of traditional laboratory model thors of this essay gathered for an NSF- species has been extremely successful, both sponsored workshop at the Janelia Farm A major focus of the Brain Research in neuroscience and more generally [Krebs, Research Campus of the Howard Hughes through Advancing Innovative Neurotech- 2005], but comparative neurobiology of Medical Institute on October 23–25, 2013. nologies (BRAIN) Initiative, announced by non-model species can provide critical ad- After several introductory presentations, President Obama on April 2, 2013, is to ditional insights into fundamental princi- the participants formed six small groups, produce ‘dynamic pictures of the brain that ples of nervous system organization. For each tackling a different central question show how individual brain cells and com- example, more than 100 years ago, Brod- but also thinking about overarching issues. plex circuits interact at the speed of thought’ mann [1909] compared the cerebral cortex The following day, each group presented [quoted in: BRAIN Working Group, 2013, of many different mammals and discov- their main recommendations, and then all p. 4]. The ultimate aim of this research ef- ered that, although some cortical areas participants engaged in an extensive dis- fort, as well as others like it around the contain more or less than 6 layers, a divi- cussion. Also participating were represen- world, is to understand the functioning of sion into 6 layers best captures the complex tatives from the NSF, the NIH, and the human brains. However, much of the re- pattern of similarities and differences in White House Office of Science and Tech- search will necessarily focus on nonhuman cortical lamination seen across species. nology. After lively debate, several core ar- species, in which novel technologies can be Similarly, comparisons of central pattern eas of agreement emerged. A white paper developed and applied more efficiently, generators across a wide variety of species, summarizing these debates and the emerg- and research can be conducted at more re- both invertebrate and vertebrate, revealed ing consensus, as well as statements from ductionist levels. For example, the Japanese important principles of how groups of neu- individual participants and video footage, brain mapping initiative will focus on mar- rons generate rhythmic patterns of activi- can be found at understandingthebrain. moset monkeys (Callithrix jacchus) , a spe- ty through the interaction of membrane org (see also brainsacrossphylogeny.org). cies that can be manipulated genetically properties and synaptic connectivity [Mar- The present document is a more formal re- [Sakai et al., 2009], yet has a neocortex that der and Bucher, 2001]. In both examples, port on the group discussions and recom- is more similar to human neocortex than general principles emerged from a compar- mendations. that of other common laboratory species. ative analysis of both similarities and dif- In brief, we agreed that comparative Other brain mapping projects will include ferences across species. A third instructive studies, including both broad comparisons research on species with smaller nervous illustration of the fruits of a comparative across widely divergent organisms and tar- systems, such as nematodes (Caenorhabdi- approach is the discovery that similar com- geted studies of more closely related spe- tis elegans) , fruit flies (Drosophila melano- putations involving learning and memory cies, can provide important information gaster) , zebra fish (Danio rerio) , and a few may be performed by very different neural about fundamental principles of nervous other species, because those nervous sys- networks even in closely related taxa, nota- system organization, including principles tems are easier to map in their entirety

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