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Characterizing this mapping is a major challenge for systems biology. Though experiments that probe internal states are developing rapidly, organismal complexity presents a fundamental obstacle given the many possible ways internal states could map to behavior. Using <jats:italic>C. elegans<\/jats:italic> as an example, we propose a protocol for systematic perturbation of neural states that limits experimental complexity and could eventually help characterize collective aspects of the neural-behavioral map. We consider experimentally motivated small perturbations\u2014ones that are most likely to preserve natural dynamics and are closer to internal control mechanisms\u2014to neural states and their impact on collective neural activity. Then, we connect such perturbations to the local information geometry of collective statistics, which can be fully characterized using pairwise perturbations. Applying the protocol to a minimal model of <jats:italic>C. elegans<\/jats:italic> neural activity, we find that collective neural statistics are most sensitive to a few principal perturbative modes. Dominant eigenvalues decay initially as a power law, unveiling a hierarchy that arises from variation in individual neural activity and pairwise interactions. Highest-ranking modes tend to be dominated by a few, \u201cpivotal\u201d neurons that account for most of the system\u2019s sensitivity, suggesting a sparse mechanism of collective control.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1010072","type":"journal-article","created":{"date-parts":[[2022,5,27]],"date-time":"2022-05-27T17:22:16Z","timestamp":1653672136000},"page":"e1010072","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":2,"title":["Discovering sparse control strategies in neural activity"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2075-6342","authenticated-orcid":true,"given":"Edward D.","family":"Lee","sequence":"first","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4029-1805","authenticated-orcid":true,"given":"Xiaowen","family":"Chen","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5870-1059","authenticated-orcid":true,"given":"Bryan C.","family":"Daniels","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2022,5,27]]},"reference":[{"issue":"21","key":"pcbi.1010072.ref001","doi-asserted-by":"crossref","first-page":"8685","DOI":"10.1073\/pnas.0701361104","article-title":"The Human Disease Network","volume":"104","author":"KI Goh","year":"2007","journal-title":"Proc Natl Acad Sci USA"},{"key":"pcbi.1010072.ref002","doi-asserted-by":"crossref","first-page":"986","DOI":"10.1016\/j.cell.2011.02.016","article-title":"Interactome Networks and Human Disease","volume":"144","author":"M Vidal","year":"2011","journal-title":"Cell"},{"issue":"3","key":"pcbi.1010072.ref003","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1016\/j.cell.2013.03.030","article-title":"Integrated Systems Approach Identifies Genetic Nodes and Networks in Late-Onset Alzheimer\u2019s Disease","volume":"153","author":"B Zhang","year":"2013","journal-title":"Cell"},{"key":"pcbi.1010072.ref004","doi-asserted-by":"crossref","first-page":"e66135","DOI":"10.7554\/eLife.66135","article-title":"Decoding Locomotion from Population Neural Activity in Moving C. 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Spin Glass Models for a Network of Real Neurons. arXiv:09125409 [q-bio]. 2009;."},{"issue":"1","key":"pcbi.1010072.ref070","doi-asserted-by":"crossref","first-page":"e1003408","DOI":"10.1371\/journal.pcbi.1003408","article-title":"Searching for Collective Behavior in a Large Network of Sensory Neurons","volume":"10","author":"G Tka\u010dik","year":"2014","journal-title":"PLoS Comput Biol"},{"issue":"17","key":"pcbi.1010072.ref071","doi-asserted-by":"crossref","first-page":"178103","DOI":"10.1103\/PhysRevLett.123.178103","article-title":"Coarse Graining, Fixed Points, and Scaling in a Large Population of Neurons","volume":"123","author":"L Meshulam","year":"2019","journal-title":"Phys Rev Lett"},{"issue":"03","key":"pcbi.1010072.ref072","doi-asserted-by":"crossref","first-page":"P03002","DOI":"10.1088\/1742-5468\/2013\/03\/P03002","article-title":"Ising Models for Neural Activity Inferred via Selective Cluster Expansion: Structural and Coding Properties","volume":"2013","author":"J Barton","year":"2013","journal-title":"J Stat Mech"},{"issue":"5","key":"pcbi.1010072.ref073","doi-asserted-by":"crossref","first-page":"e1000380","DOI":"10.1371\/journal.pcbi.1000380","article-title":"Pairwise Maximum Entropy Models for Studying Large Biological Systems: When They Can Work and When They Can\u2019t","volume":"5","author":"Y Roudi","year":"2009","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1010072.ref074","doi-asserted-by":"crossref","unstructured":"Amari Si. Information Geometry and Its Applications. vol. 194 of Applied Mathematical Sciences. Springer Japan; 2016.","DOI":"10.1007\/978-4-431-55978-8"},{"key":"pcbi.1010072.ref075","unstructured":"Bialek W, Ranganathan R. Rediscovering the Power of Pairwise Interactions. arXiv:07124397 [q-bio]. 2007;."},{"issue":"03","key":"pcbi.1010072.ref076","doi-asserted-by":"crossref","first-page":"P03011","DOI":"10.1088\/1742-5468\/2013\/03\/P03011","article-title":"The Simplest Maximum Entropy Model for Collective Behavior in a Neural Network","volume":"2013","author":"G Tka\u010dik","year":"2013","journal-title":"J Stat Mech"},{"key":"pcbi.1010072.ref077","volume-title":"Biophysics: Searching for Principles","author":"WS Bialek","year":"2012"},{"issue":"1","key":"pcbi.1010072.ref078","doi-asserted-by":"crossref","first-page":"010901","DOI":"10.1063\/1.4923066","article-title":"Perspective: Sloppiness and Emergent Theories in Physics, Biology, and Beyond","volume":"143","author":"MK Transtrum","year":"2015","journal-title":"J Chem Phys"},{"issue":"18","key":"pcbi.1010072.ref079","doi-asserted-by":"crossref","first-page":"188104","DOI":"10.1103\/PhysRevLett.97.188104","article-title":"Eigenvalue Spectra of Random Matrices for Neural Networks","volume":"97","author":"K Rajan","year":"2006","journal-title":"Phys Rev Lett"},{"key":"pcbi.1010072.ref080","doi-asserted-by":"crossref","first-page":"313","DOI":"10.3389\/fnins.2017.00313","article-title":"Dual Coding Theory Explains Biphasic Collective Computation in Neural Decision-Making","volume":"11","author":"BC Daniels","year":"2017","journal-title":"Front Neurosci"},{"issue":"6","key":"pcbi.1010072.ref081","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1049\/piee.1969.0206","article-title":"Wmatrix and the Geometry of Model Equivalence and Reduction","volume":"116","author":"D Mitra","year":"1969","journal-title":"Proc Inst Electr Eng UK"},{"key":"pcbi.1010072.ref082","doi-asserted-by":"crossref","unstructured":"Roy P, Cela A, Hamam Y. On the Relation of FIM and Controllability Gramian. In: 2009 IEEE International Symposium on Industrial Embedded Systems. Lausanne, Switzerland: IEEE; 2009. p. 37\u201341.","DOI":"10.1109\/SIES.2009.5196189"},{"key":"pcbi.1010072.ref083","doi-asserted-by":"crossref","unstructured":"Liu J, Elia N. Convergence of Fundamental Limitations in Information, Estimation, and Control. In: Proceedings of the 45th IEEE Conference on Decision and Control. San Diego, CA, USA: IEEE; 2006. p. 5609\u20135614.","DOI":"10.1109\/CDC.2006.377694"},{"issue":"1","key":"pcbi.1010072.ref084","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1073\/pnas.0805923106","article-title":"Identification of Direct Residue Contacts in Protein-Protein Interaction by Message Passing","volume":"106","author":"M Weigt","year":"2009","journal-title":"Proc Natl Acad Sci USA"},{"issue":"6","key":"pcbi.1010072.ref085","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1007\/s10208-009-9045-5","article-title":"Exact Matrix Completion via Convex Optimization","volume":"9","author":"EJ Cand\u00e8s","year":"2009","journal-title":"Found Comput Math"},{"issue":"3","key":"pcbi.1010072.ref086","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1016\/j.neuron.2019.10.037","article-title":"Nested Neuronal Dynamics Orchestrate a Behavioral Hierarchy across Timescales","volume":"105","author":"HS Kaplan","year":"2020","journal-title":"Neuron"},{"issue":"6","key":"pcbi.1010072.ref087","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1016\/S1534-5807(01)00085-5","article-title":"A Hormonal Signaling Pathway Influencing C. Elegans Metabolism, Reproductive Development, and Life Span","volume":"1","author":"B Gerisch","year":"2001","journal-title":"Developmental Cell"},{"issue":"8","key":"pcbi.1010072.ref088","doi-asserted-by":"crossref","first-page":"1765","DOI":"10.1242\/dev.01068","article-title":"Hormonal Signals Produced by DAF-9\/Cytochrome P450 Regulate C. Elegans Dauer Diapause in Response to Environmental Cues","volume":"131","author":"B Gerisch","year":"2004","journal-title":"Development"},{"issue":"2","key":"pcbi.1010072.ref089","doi-asserted-by":"crossref","first-page":"e53","DOI":"10.1371\/journal.pbio.0030053","article-title":"Nuclear Hormone Receptor NHR-49 Controls Fat Consumption and Fatty Acid Composition in C. Elegans","volume":"3","author":"MRV Gilst","year":"2005","journal-title":"PLoS Biol"},{"issue":"5537","key":"pcbi.1010072.ref090","doi-asserted-by":"crossref","first-page":"2087","DOI":"10.1126\/science.1061603","article-title":"A Gene Expression Map for Caenorhabditis Elegans","volume":"293","author":"SK Kim","year":"2001","journal-title":"Science"},{"issue":"9","key":"pcbi.1010072.ref091","doi-asserted-by":"crossref","first-page":"e237","DOI":"10.1371\/journal.pbio.0050237","article-title":"High-Throughput In Vivo Analysis of Gene Expression in Caenorhabditis Elegans","volume":"5","author":"R Hunt-Newbury","year":"2007","journal-title":"PLoS Biol"},{"issue":"1","key":"pcbi.1010072.ref092","doi-asserted-by":"crossref","first-page":"103663","DOI":"10.1016\/j.isci.2021.103663","article-title":"Gene Regulatory Network Inference in Long-Lived C. Elegans Reveals Modular Properties That Are Predictive of Novel Aging Genes","volume":"25","author":"M Suriyalaksh","year":"2022","journal-title":"iScience"},{"issue":"1","key":"pcbi.1010072.ref093","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/1471-2156-6-5","article-title":"An Automated System for Measuring Parameters of Nematode Sinusoidal Movement","volume":"6","author":"CJ Cronin","year":"2005","journal-title":"BMC Genet"},{"issue":"3","key":"pcbi.1010072.ref094","doi-asserted-by":"crossref","first-page":"1117","DOI":"10.1093\/genetics\/165.3.1117","article-title":"Quantitative Classification and Natural Clustering of Caenorhabditis Elegans Behavioral Phenotypes","volume":"165","author":"W Geng","year":"2003","journal-title":"Genetics"},{"issue":"121","key":"pcbi.1010072.ref095","doi-asserted-by":"crossref","first-page":"20160466","DOI":"10.1098\/rsif.2016.0466","article-title":"Hierarchical Compression of Caenorhabditis Elegans Locomotion Reveals Phenotypic Differences in the Organization of Behaviour","volume":"13","author":"A Gomez-Marin","year":"2016","journal-title":"J R Soc Interface"},{"key":"pcbi.1010072.ref096","doi-asserted-by":"crossref","unstructured":"Costa AC, Ahamed T, Jordan D, Stephens G. Maximally Predictive Ensemble Dynamics from Data. arXiv:210512811 [physics, q-bio]. 2021;.","DOI":"10.1101\/2021.05.26.445816"},{"issue":"11","key":"pcbi.1010072.ref097","doi-asserted-by":"crossref","first-page":"4820","DOI":"10.1073\/pnas.1000615107","article-title":"Discovering the Flight Autostabilizer of Fruit Flies by Inducing Aerial Stumbles","volume":"107","author":"L Ristroph","year":"2010","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"3","key":"pcbi.1010072.ref098","doi-asserted-by":"crossref","first-page":"036701","DOI":"10.1103\/PhysRevE.83.036701","article-title":"Geometry of Nonlinear Least Squares with Applications to Sloppy Models and Optimization","volume":"83","author":"MK Transtrum","year":"2011","journal-title":"Phys Rev E"},{"issue":"6","key":"pcbi.1010072.ref099","doi-asserted-by":"crossref","first-page":"060201","DOI":"10.1103\/PhysRevLett.104.060201","article-title":"Why Are Nonlinear Fits to Data so Challenging?","volume":"104","author":"MK Transtrum","year":"2010","journal-title":"Phys Rev Lett"},{"key":"pcbi.1010072.ref100","first-page":"271","volume-title":"Quantitative Biology: Theory, Computational Methods, and Models","author":"BC Daniels","year":"2018"},{"issue":"9","key":"pcbi.1010072.ref101","doi-asserted-by":"crossref","first-page":"098701","DOI":"10.1103\/PhysRevLett.113.098701","article-title":"Model Reduction by Manifold Boundaries","volume":"113","author":"MK Transtrum","year":"2014","journal-title":"Phys Rev Lett"}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010072","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,5,27]],"date-time":"2022-05-27T17:23:56Z","timestamp":1653672236000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010072"}},"subtitle":[],"editor":[{"given":"Matthieu","family":"Louis","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2022,5,27]]},"references-count":101,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2022,5,27]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1010072","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,27]]}}}