Tuning movement for sensing in an uncertain world

While animals track or search for targets, sensory organs make small unexplained movements on top of the primary task-related motions. While multiple theories for these movements exist—in that they support infotaxis, gain adaptation, spectral whitening, and high-pass filtering—predicted trajectories show poor fit to measured trajectories. We propose a new theory for these movements called energy-constrained proportional betting, where the probability of moving to a location is proportional to an expectation of how informative it will be balanced against the movement’s predicted energetic cost. Trajectories generated in this way show good agreement with measured trajectories of fish tracking an object using electrosense, a mammal and an insect localizing an odor source, and a moth tracking a flower using vision. Our theory unifies the metabolic cost of motion with information theory. It predicts sense organ movements in animals and can prescribe sensor motion for robots to enhance performance.

[1]  A. Ijspeert,et al.  Reverse-engineering the locomotion of a stem amniote , 2019, Nature.

[2]  Jessica Porter,et al.  Mechanisms of scent-tracking in humans , 2007, Nature Neuroscience.

[3]  P. Tyack,et al.  Biosonar performance of foraging beaked whales (Mesoplodon densirostris) , 2005, Journal of Experimental Biology.

[4]  Kenneth C Catania,et al.  Stereo and serial sniffing guide navigation to an odour source in a mammal , 2013, Nature Communications.

[5]  Surya P. N. Singh,et al.  Analyzing Bounding and Galloping Using Simple Models , 2009 .

[6]  Malcolm A. MacIver,et al.  Spatial planning with long visual range benefits escape from visual predators in complex naturalistic environments , 2020, Nature Communications.

[7]  Sigurd Skogestad,et al.  A Sensory-Motor Control Model of Animal Flight Explains Why Bats Fly Differently in Light Versus Dark , 2015, PLoS biology.

[8]  Eric S. Fortune,et al.  Effects of global electrosensory signals on motion processing in the midbrain of Eigenmannia , 2005, Journal of Comparative Physiology A.

[9]  H. Sompolinsky,et al.  Adaptation without parameter change: Dynamic gain control in motion detection , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Sherry E. Scott,et al.  Different Perspectives and Formulas for Capturing Deviation from Ergodicity , 2013, SIAM J. Appl. Dyn. Syst..

[11]  M. Mackey,et al.  Chaos, Fractals, and Noise: Stochastic Aspects of Dynamics , 1998 .

[12]  L. Maler,et al.  Speed-invariant encoding of looming object distance requires power law spike rate adaptation , 2013, Proceedings of the National Academy of Sciences.

[13]  Masashi Kawasaki,et al.  Multisensory enhancement of electromotor responses to a single moving object , 2008, Journal of Experimental Biology.

[14]  I. Mezić,et al.  Metrics for ergodicity and design of ergodic dynamics for multi-agent systems , 2011 .

[15]  Mitra J. Hartmann,et al.  c ○ 2001 Kluwer Academic Publishers. Manufactured in The Netherlands. Active Sensing Capabilities of the Rat Whisker System , 2022 .

[16]  Gary J. Rose,et al.  Longitudinal tracking responses of the weakly electric fish, Sternopygus , 2004, Journal of Comparative Physiology A.

[17]  A. Watanabe,et al.  The Change of Discharge Frequency by A.C. Stimulus in a Weak Electric Fish , 1963 .

[18]  F. Attneave Some informational aspects of visual perception. , 1954, Psychological review.

[19]  Noah J Cowan,et al.  The Critical Role of Locomotion Mechanics in Decoding Sensory Systems , 2007, The Journal of Neuroscience.

[20]  Marc J. Weissburg,et al.  Slow-moving predatory gastropods track prey odors in fast and turbulent flow , 2005, Journal of Experimental Biology.

[21]  C. Moss,et al.  The sonar beam pattern of a flying bat as it tracks tethered insects. , 2003, The Journal of the Acoustical Society of America.

[22]  Todd D. Murphey,et al.  Real-Time Area Coverage and Target Localization Using Receding-Horizon Ergodic Exploration , 2017, IEEE Transactions on Robotics.

[23]  Massimo Vergassola,et al.  ‘Infotaxis’ as a strategy for searching without gradients , 2007, Nature.

[24]  Dawnis M. Chow,et al.  Flies Require Bilateral Sensory Input to Track Odor Gradients in Flight , 2009, Current Biology.

[25]  S. Mitter,et al.  The conjugate gradient method for optimal control problems , 1967 .

[26]  Todd D. Murphey,et al.  Ergodic Exploration of Distributed Information , 2016, IEEE Transactions on Robotics.

[27]  H. Schnitzler,et al.  From spatial orientation to food acquisition in echolocating bats , 2003 .

[28]  Neelesh A. Patankar,et al.  Energy-Information Trade-Offs between Movement and Sensing , 2010, PLoS Comput. Biol..

[29]  Scott Cheng-Hsin Yang,et al.  Active sensing in the categorization of visual patterns , 2016, eLife.

[30]  Mark A. Frye,et al.  Drosophila Spatiotemporally Integrates Visual Signals to Control Saccades , 2017, Current Biology.

[31]  M. Willis,et al.  Odor-modulated orientation in walking male cockroaches Periplaneta americana, and the effects of odor plumes of different structure , 2005, Journal of Experimental Biology.

[32]  M. A. MacIver,et al.  Prey-capture behavior in gymnotid electric fish: motion analysis and effects of water conductivity. , 2001, The Journal of experimental biology.

[33]  Todd D. Murphey,et al.  Decentralized Ergodic Control: Distribution-Driven Sensing and Exploration for Multiagent Systems , 2018, IEEE Robotics and Automation Letters.

[34]  Leonard Maler,et al.  Feedback Synthesizes Neural Codes for Motion , 2017, Current Biology.

[35]  Richard M. Murray,et al.  Discriminating External and Internal Causes for Heading Changes in Freely Flying Drosophila , 2013, PLoS Comput. Biol..

[36]  Simon B. Laughlin,et al.  Action Potential Energy Efficiency Varies Among Neuron Types in Vertebrates and Invertebrates , 2010, PLoS Comput. Biol..

[37]  Patrick J Drew,et al.  Models and properties of power-law adaptation in neural systems. , 2006, Journal of neurophysiology.

[38]  Rob R. de Ruyter van Steveninck,et al.  The metabolic cost of neural information , 1998, Nature Neuroscience.

[39]  Jacob Engelmann,et al.  Motor patterns during active electrosensory acquisition , 2014, Front. Behav. Neurosci..

[40]  Constantin A. Rothkopf,et al.  Multi-step planning of eye movements in visual search , 2019, Scientific Reports.

[41]  Noah J. Cowan,et al.  Recovering Observability via Active Sensing , 2018, 2018 Annual American Control Conference (ACC).

[42]  Marina E. Wosniack,et al.  The evolutionary origins of Lévy walk foraging , 2017, PLoS Comput. Biol..

[43]  Robert J. Full,et al.  Templates and Anchors for Antenna-Based Wall Following in Cockroaches and Robots , 2008, IEEE Transactions on Robotics.

[44]  Benjamin Van Roy,et al.  A Tutorial on Thompson Sampling , 2017, Found. Trends Mach. Learn..

[45]  C. Gilbert Visual control of cursorial prey pursuit by tiger beetles (Cicindelidae) , 1997, Journal of Comparative Physiology A.

[46]  A. Reynolds,et al.  Free-Flight Odor Tracking in Drosophila Is Consistent with an Optimal Intermittent Scale-Free Search , 2007, PloS one.

[47]  Dario Floreano,et al.  Climbing favours the tripod gait over alternative faster insect gaits , 2017, Nature Communications.

[48]  Jonathan P. Dyhr,et al.  Luminance-dependent visual processing enables moth flight in low light , 2015, Science.

[49]  Jennifer M. Rieser,et al.  Tail use improves performance on soft substrates in models of early vertebrate land locomotors , 2016, Science.

[50]  S. Laughlin,et al.  Energy limitation as a selective pressure on the evolution of sensory systems , 2008, Journal of Experimental Biology.

[51]  Simon Sponberg,et al.  Comparative system identification of flower tracking performance in three hawkmoth species reveals adaptations for dim light vision , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[52]  Michael C. Mackey,et al.  Chaos, Fractals, and Noise , 1994 .

[53]  A. Reynolds,et al.  Pelagic seabird flight patterns are consistent with a reliance on olfactory maps for oceanic navigation , 2015, Proceedings of the Royal Society B: Biological Sciences.

[54]  Joseph Bastian Electrolocation in the presence of jamming signals: behavior , 2004, Journal of Comparative Physiology A.

[55]  A. Caputi,et al.  Probability and amplitude of novelty responses as a function of the change in contrast of the reafferent image in G. carapo , 2003, Journal of Experimental Biology.

[56]  Jacqueline Gottlieb,et al.  Attention, Reward, and Information Seeking , 2014, The Journal of Neuroscience.

[57]  Joseph J Atick,et al.  Could information theory provide an ecological theory of sensory processing? , 2011, Network.

[58]  Russ Tedrake,et al.  Efficient Bipedal Robots Based on Passive-Dynamic Walkers , 2005, Science.

[59]  E. Charnov Optimal foraging, the marginal value theorem. , 1976, Theoretical population biology.

[60]  J. Victor,et al.  The unsteady eye: an information-processing stage, not a bug , 2015, Trends in Neurosciences.

[61]  M. Dickinson,et al.  Active flight increases the gain of visual motion processing in Drosophila , 2010, Nature Neuroscience.

[62]  Ilya E. Monosov,et al.  Neurons in the Primate Medial Basal Forebrain Signal Combined Information about Reward Uncertainty, Value, and Punishment Anticipation , 2015, The Journal of Neuroscience.

[63]  Mark E Nelson,et al.  Omnidirectional Sensory and Motor Volumes in Electric Fish , 2007, PLoS biology.

[64]  Gaby Maimon,et al.  Abolishment of Spontaneous Flight Turns in Visually Responsive Drosophila , 2018, Current Biology.

[65]  Sheryl Coombs,et al.  Dipole source localization by mottled sculpin. I. Approach strategies , 1997, Journal of Comparative Physiology A.

[66]  M. Willis,et al.  One antenna, two antennae, big antennae, small: total antennae length, not bilateral symmetry, predicts odor-tracking performance in the American cockroach Periplaneta americana , 2015, The Journal of Experimental Biology.

[67]  W. Beyer CRC Standard Probability And Statistics Tables and Formulae , 1990 .

[68]  André Longtin,et al.  A Neural Code for Looming and Receding Motion Is Distributed over a Population of Electrosensory ON and OFF Contrast Cells , 2014, The Journal of Neuroscience.

[69]  Sreekanth H. Chalasani,et al.  Maximally informative foraging by Caenorhabditis elegans , 2014, eLife.

[70]  Sara A Solla,et al.  Whisking mechanics and active sensing , 2016, Current Opinion in Neurobiology.

[71]  Sebastian Thrun,et al.  Probabilistic robotics , 2002, CACM.

[72]  Timothy E. J. Behrens,et al.  Neural Mechanisms of Foraging , 2012, Science.

[73]  Nachum Ulanovsky,et al.  Active Control of Acoustic Field-of-View in a Biosonar System , 2011, PLoS biology.

[74]  Wilson S. Geisler,et al.  Optimal eye movement strategies in visual search , 2005, Nature.

[75]  Margaret L. Brandeau,et al.  Optimal Localization by Pointing Off Axis , 2010 .

[76]  Andrew M. Hein,et al.  Natural search algorithms as a bridge between organisms, evolution, and ecology , 2016, Proceedings of the National Academy of Sciences.

[77]  Noah J. Cowan,et al.  Closed-Loop Control of Active Sensing Movements Regulates Sensory Slip , 2018, Current Biology.

[78]  Lena Osterhagen,et al.  Data analysis for scientists and engineers , 1975 .

[79]  Noah J. Cowan,et al.  Active sensing via movement shapes spatiotemporal patterns of sensory feedback , 2012, Journal of Experimental Biology.

[80]  Howie Choset,et al.  A review on locomotion robophysics: the study of movement at the intersection of robotics, soft matter and dynamical systems , 2016, Reports on progress in physics. Physical Society.

[81]  H. Martin Osmotropotaxis in the Honey-Bee , 1965, Nature.

[82]  U. Bhalla,et al.  Rats track odour trails accurately using a multi-layered strategy with near-optimal sampling , 2012, Nature Communications.

[83]  Manoj Srinivasan,et al.  Computer optimization of a minimal biped model discovers walking and running , 2006, Nature.

[84]  Konrad Paul Kording,et al.  Bayesian integration in sensorimotor learning , 2004, Nature.

[85]  Todd D. Murphey,et al.  Tuning movement for sensing in an uncertain world , 2019, eLife.

[86]  M. A. MacIver,et al.  Sensory acquisition in active sensing systems , 2006, Journal of Comparative Physiology A.

[87]  Claire M Postlethwaite,et al.  Optimal movement in the prey strikes of weakly electric fish: a case study of the interplay of body plan and movement capability , 2009, Journal of The Royal Society Interface.

[88]  M. Botvinick,et al.  The hippocampus as a predictive map , 2016 .

[89]  C. Moss,et al.  Steering by Hearing: A Bat’s Acoustic Gaze Is Linked to Its Flight Motor Output by a Delayed, Adaptive Linear Law , 2006, The Journal of Neuroscience.

[90]  Sreekanth H. Chalasani,et al.  Neural Mechanisms for Evaluating Environmental Variability in Caenorhabditis elegans , 2015, Neuron.

[91]  Jonathan D Victor,et al.  Elementary sensory-motor transformations underlying olfactory navigation in walking fruit-flies , 2018, bioRxiv.

[92]  B. Webb,et al.  Sensorimotor control of navigation in arthropod and artificial systems. , 2004, Arthropod structure & development.

[93]  Pete C. Trimmer,et al.  Foraging for foundations in decision neuroscience: insights from ethology , 2018, Nature Reviews Neuroscience.

[94]  Ben Mitchinson,et al.  Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact , 2007, Proceedings of the Royal Society B: Biological Sciences.

[95]  L. Vosshall,et al.  Bilateral olfactory sensory input enhances chemotaxis behavior , 2008, Nature Neuroscience.

[96]  J Atema,et al.  Three-dimensional odor tracking by Nautilus pompilius. , 2000, The Journal of experimental biology.

[97]  Shahin Sefati,et al.  Mutually opposing forces during locomotion can eliminate the tradeoff between maneuverability and stability , 2013, Proceedings of the National Academy of Sciences.

[98]  Marshall G. Hussain Shuler,et al.  Rationalizing spatial exploration patterns of wild animals and humans through a temporal discounting framework , 2016, Proceedings of the National Academy of Sciences.

[99]  Ninad B Kothari,et al.  Adaptive sonar call timing supports target tracking in echolocating bats , 2018, Journal of Experimental Biology.

[100]  K. Aihara,et al.  Echolocating bats use future-target information for optimal foraging , 2016, Proceedings of the National Academy of Sciences.

[101]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[102]  Thomas L Daniel,et al.  Flower tracking in hawkmoths: behavior and energetics , 2007, Journal of Experimental Biology.

[103]  Kathrin Flaßkamp,et al.  Ergodic exploration with stochastic sensor dynamics , 2016, 2016 American Control Conference (ACC).