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Using Control Theory to Characterize Active Sensing in Weakly Electric Fishes

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Electroreception: Fundamental Insights from Comparative Approaches

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 70))

Abstract

Animals routinely use their own motor outputs to modulate the sensory information they perceive, a process termed “active sensing.” This chapter highlights the use of control theoretic approaches to reveal the functional relationships between active sensing, task-related behaviors, sensing, and motor control. Specifically, recently developed experimental systems use artificially controlled feedback loops to perturb natural reafferent feedback in freely behaving animals. Such perturbations allow quantitative and systematic descriptions of control strategies for active sensing.

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References

  • Aghajan ZM, Acharya L, Moore JJ, Cushman JD, Vuong C, Mehta MR (2015) Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality. IEEE Trans Neural Netw 18(1):121–128

    CAS  Google Scholar 

  • Ahissar E, Arieli A (2012) Seeing via miniature eye movements: a dynamic hypothesis for vision. Front Comp Neurosci 6. https://doi.org/10.3389/fncom.2012.00089

  • Ahrens MB, Li JM, Orger MB, Robson DN, Schier AF, Engert F, Portugues R (2012) Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485(7399):471–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alviña K, Sawtell NB (2014) Sensory processing and corollary discharge effects in posterior caudal lobe Purkinje cells in a weakly electric mormyrid fish. J Neurophysiol 112(2):328–339

    Article  PubMed  PubMed Central  Google Scholar 

  • Aronov D, Tank DW (2014) Engagement of neural circuits underlying 2d spatial navigation in a rodent virtual reality system. Neuron 84(2):442–456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Au WWL, Moore PWB (1986) Echolocation transmitting beam of the Atlantic bottlenose dolphin. J Acous Soc Amer 80:688–691

    Article  CAS  Google Scholar 

  • Babineau D, Longtin A, Lewis JE (2006) Modeling the electric field of weakly electric fish. J Exp Biol 209:3636–3651

    Article  PubMed  Google Scholar 

  • Babineau D, Lewis JE, Longtin A (2007) Spatial acuity and prey detection in weakly electric fish. PLoS Comput Biol 3:e38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Biswas D, Arend LA, Stamper SA, Vágvölgyi BP, Fortune ES, Cowan NJ (2018) Closed-loop control of active sensing. Curr Biol 28(24):4029–4036

    Article  CAS  PubMed  Google Scholar 

  • Blake R (1983) Swimming in the electric eels and knifefishes. Can J Zool 61(6):1432–1441

    Article  Google Scholar 

  • Caputi AA (2017) Active electroreception in weakly electric fish. Oxford University Press, Oxford

    Google Scholar 

  • Chacron MJ, Doiron B, Maler L, Longtin A, Bastian J (2003) Non-classical receptive field mediates switch in a sensory neuron’s frequency tuning. Nature 423(6935):77–81

    Article  CAS  PubMed  Google Scholar 

  • Chen G, King JA, Burgess N, O’Keefe J (2013) How vision and movement combine in the hippocampal place code. Proc Nat Acad Sci 110(1):378–383

    Article  CAS  PubMed  Google Scholar 

  • Colgate J, Lynch KM (2004) Mechanics and control of swimming: a review. IEEE J Ocean Eng 29(3):660–673

    Article  Google Scholar 

  • Cowan NJ, Fortune ES (2007) The critical role of locomotion mechanics in decoding sensory systems. J Neurosci 27(5):1123–1128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cowan NJ, Ankarali MM, Dyhr JP, Madhav MS, Roth E, Sefati S, Sponberg S, Stamper SA, Fortune ES, Daniel TL (2014) Feedback control as a framework for understanding tradeoffs in biology. Integr Comp Biol 54(2):223–237

    Article  PubMed  Google Scholar 

  • Dave AS, Margoliash D (2000) Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290(5492):812–816

    Article  CAS  PubMed  Google Scholar 

  • Dawson SM (1991) Clicks and communication: the behavioural and social contexts of hector’s dolphin vocalizations. Ethology 88(4):265–276

    Article  Google Scholar 

  • Ditchburn R, Ginsborg B (1952) Vision with a stabilized retinal image. Nature 170(4314):36–37

    Article  CAS  PubMed  Google Scholar 

  • Erickson CJ (1994) Tap-scanning and extractive foraging in aye-ayes, Daubentonia madagascariensis. Folia Primatol 62(1–3):125–135

    Article  CAS  Google Scholar 

  • Erickson CJ, Nowicki S, Dollar L, Goehring N (1998) Percussive foraging: stimuli for prey location by aye-ayes (Daubentonia madagascariensis). Int J Primatol 19(1):111–122

    Article  Google Scholar 

  • Fenton B, Ratcliffe J (2004) Animal behaviour: eavesdropping on bats. Nature 429(6992):612–613

    Article  CAS  PubMed  Google Scholar 

  • Ghose K, Moss CF (2006) Steering by hearing: a bat’s acoustic gaze is linked to its flight motor output by a delayed, adaptive linear law. J Neurosci 26(6):1704–1710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gibson JJ (1962) Observations on active touch. Psychol Rev 69:477–491

    Article  CAS  PubMed  Google Scholar 

  • Götz T, Verfuß UK, Schnitzler H-U (2006) ‘Eavesdropping’ in wild rough-toothed dolphins (Steno bredanensis)? Biol Lett 2(1):5–7

    Article  PubMed  Google Scholar 

  • Griffin DR, McCue JJG, Grinnell AD (1963) The resistance of bats to jamming. J Exp Zool A 152(3):229–250

    Article  Google Scholar 

  • Gritsenko V, Yakovenko S, Kalaska JF (2009) Integration of predictive feedforward and sensory feedback signals for online control of visually guided movement. J Neurophysiol 102(2):914–930

    Article  CAS  PubMed  Google Scholar 

  • Hassan ES (1985) Mathematical analysis of the stimulus for the lateral line organ. Biol Cybern 52(1):23–36

    Article  CAS  PubMed  Google Scholar 

  • Hassan ES (1989) Hydrodynamic imaging of the surroundings by the lateral line of the blind cave fish Anoptichthys jordani. In: The mechanosensory lateral line. Springer, New York, pp 217–227

    Chapter  Google Scholar 

  • Heiligenberg W (1991a) Neural nets in electric fish. MIT Press, Cambridge, MA

    Google Scholar 

  • Heiligenberg W (1991b) The jamming avoidance response of the electric fish Eigenmannia: computational rules and their neuronal implementation. Semin Neurosci 3:3–18

    Article  Google Scholar 

  • Heiligenberg W, Bastian J (1984) The electric sense of weakly electric fish. Annu Rev Physiol 46:561–583

    Article  CAS  PubMed  Google Scholar 

  • Hofmann V, Geurten BRH, Sanguinetti-Scheck JI, Gómez-Sena L, Engelmann J (2014) Motor patterns during active electrosensory acquisition. Font Behav Neurosci 8:186

    Google Scholar 

  • Hollins M, Risner SR (2000) Evidence for the duplex theory of tactile texture perception. Percept Psychophys 62(4):695–705

    Article  CAS  PubMed  Google Scholar 

  • Kim C, Ruberto T, Phamduy P, Porfiri M (2018) Closed-loop control of zebrafish behaviour in three dimensions using a robotic stimulus. Sci Rep 8:657

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Knill DC, Bondada A, Chhabra M (2011) Flexible, task-dependent use of sensory feedback to control hand movements. J Neurosci 31(4):1219–1237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koop K, Velimirov B (1982) Field observations on activity and feeding of bat-eared foxes Otocyon megalotis at Nxai Pan, Botswana. Afr J Ecol 20(1):23–27

    Article  Google Scholar 

  • Lannoo MJ, Lannoo SJ (1993) Why do electric fishes swim backwards? An hypothesis based on gymnotiform foraging behavior interpreted through sensory constraints. Environ Biol Fish 36(2):157–165

    Article  Google Scholar 

  • Lederman SJ, Klatzky RL (1987) Hand movements: a window into haptic object recognition. Cogn Psychol 19(3):342–368

    Article  CAS  PubMed  Google Scholar 

  • Lichtenberg EM, Hrncir M, Turatti IC, Nieh JC (2011) Olfactory eavesdropping between two competing stingless bee species. Behav Ecol Sociobiol 65(4):763–774

    Article  PubMed  Google Scholar 

  • MacIver MA, Sharabash NM, Nelson ME (2001) Prey-capture behavior in gymnotid electric fish: motion analysis and effects of water conductivity. J Exp Biol 204(3):543–557

    CAS  PubMed  Google Scholar 

  • Madhav MS, Stamper SA, Fortune ES, Cowan NJ (2013) Closed-loop stabilization of the jamming avoidance response reveals its locally unstable and globally nonlinear dynamics. J Exp Biol 216(22):4272–4284

    Article  PubMed  Google Scholar 

  • Madhav MS, Jayakumar RP, Demir A, Stamper SA, Fortune ES, Cowan NJ (2018) High-resolution behavioral mapping of electric fishes in Amazonian habitats. Sci Rep 8(1):5830

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maimon G, Straw AD, Dickinson MH (2010) Active flight increases the gain of visual motion processing in drosophila. Nat Neurosci 13(3):393–399

    Article  CAS  PubMed  Google Scholar 

  • Metzner W (1999) Neural circuitry for communication and jamming avoidance in gymnotiform electric fish. J Exp Biol 202(10):1365–1375

    CAS  PubMed  Google Scholar 

  • Meyer JH, Zakon HH (1982) Androgens alter the tuning of electroreceptors. Science 217(4560):635–637

    Article  CAS  PubMed  Google Scholar 

  • Mogdans J, Ostwald J, Schnitzler H-U (1988) The role of pinna movement for the localization of vertical and horizontal wire obstacles in the greater horseshoe bat, Rhinolopus ferrumequinum. J Acoust Soc Am 84(5):1676–1679

    Article  Google Scholar 

  • Mosconi T, Woolsey TA, Jacquin MF (2010) Passive vs. active touch-induced activity in the developing whisker pathway. Eur J Neurosci 32(8):1354–1363

    Article  PubMed  PubMed Central  Google Scholar 

  • Mostofi N, Boi M, Rucci M (2016) Are the visual transients from microsaccades helpful? Measuring the influences of small saccades on contrast sensitivity. Vis Res 118:60–69

    Article  PubMed  Google Scholar 

  • Nelson ME, MacIver MA (1999) Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. J Exp Biol 202(10):1195–1203

    CAS  PubMed  Google Scholar 

  • Nelson ME, MacIver MA (2006) Sensory acquisition in active sensing systems. J Comp Physiol A 192(6):573–586

    Article  CAS  Google Scholar 

  • Oestreich J, Zakon HH (2005) Species-specific differences in sensorimotor adaptation are correlated with differences in social structure. J Comp Physiol A 191(9):845–856

    Article  Google Scholar 

  • Partan S, Marler P (1999) Communication goes multimodal. Science 283(5406):1272–1273

    Article  CAS  PubMed  Google Scholar 

  • Pearson K (2008) Role of sensory feedback in the control of stance duration in walking cats. Brain Res Rev 57(1):222–227

    Article  CAS  PubMed  Google Scholar 

  • Phillips KA, Goodchild LMS, Haas ME, Ulyan MJ, Petro S (2004) Use of visual, acoustic, and olfactory information during embedded invertebrate foraging in brown capuchins (Cebus apella). J Comp Physiol 118(2):200–205

    Google Scholar 

  • Populin LC, Yin TC (1998) Pinna movements of the cat during sound localization. J Neurosci 18(11):4233–4243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pye J, Roberts L (1970) Ear movements in a hipposiderid bat. Nature 225(5229):285–286

    Article  Google Scholar 

  • Ravassard P, Kees A, Willers B, Ho D, Aharoni D, Cushman J, Aghajan ZM, Mehta MR (2013) Multisensory control of hippocampal spatiotemporal selectivity. Science 340(6138):1342–1346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reiser MB, Dickinson MH (2008) A modular display system for insect behavioral neuroscience. J Neurosci Methods 167(2):127–139

    Article  PubMed  Google Scholar 

  • Robinson DA (1976) Adaptive gain control of vestibuloocular reflex by the cerebellum. J Neurophysiol 39(5):954–969

    Article  CAS  PubMed  Google Scholar 

  • Robinson D (1977) Linear addition of optokinetic and vestibular signals in the vestibular nucleus. Exp Brain Res 30(2–3):447–450

    CAS  PubMed  Google Scholar 

  • Rose GJ, Canfield JG (1993) Longitudinal tracking responses of Eigenmannia and Sternopygus. J Comp Physiol A 173:698–700

    Google Scholar 

  • Roth E, Zhuang K, Stamper SA, Fortune ES, Cowan NJ (2011) Stimulus predictability mediates a switch in locomotor smooth pursuit performance for Eigenmannia virescens. J Exp Biol 214(7):1170–1180

    Article  PubMed  Google Scholar 

  • Roth E, Reiser MB, Dickinson MH, Cowan NJ (2012) A task-level model for optomotor yaw regulation in Drosophila melanogaster: a frequency-domain system identification approach. Proc IEEE Int Conf on Decision Control:3721–3726

    Google Scholar 

  • Roth E, Sponberg S, Cowan NJ (2014) A comparative approach to closed-loop computation. Curr Opin Neurobiol 25:54–62

    Article  CAS  PubMed  Google Scholar 

  • Sefati S, Neveln ID, Roth E, Mitchell T, Snyder JB, MacIver MA, Fortune ES, Cowan NJ (2013) Mutually opposing forces during locomotion can eliminate the tradeoff between maneuverability and stability. Proc Nat Acad Sci 110(47):18798–18803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snyder JB, Nelson ME, Burdick JW, MacIver MA (2007) Omnidirectional sensory and motor volumes in electric fish. PLoS Biol 5(11):1–13

    Article  CAS  Google Scholar 

  • Sofroniew NJ, Cohen JD, Lee AK, Svoboda K (2014) Natural whisker-guided behavior by head-fixed mice in tactile virtual reality. J Neurosci 34(29):9537–9550

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stamper S, Carrera-G E, Tan E, Fortune ES (2010) Species differences in group size and electrosensory interference in weakly electric fishes: implications for electrosensory processing. Behav Brain Res 207(2):368–376

    Article  PubMed  Google Scholar 

  • Stamper SA, RothE CNJ, Fortune ES (2012) Active sensing via movement shapes spatiotemporal patterns of sensory feedback. J Exp Biol 215(9):1567–1574

    Article  PubMed  Google Scholar 

  • Stowe MK, Turlings T, Loughrin JH, Lewis WJ, Tumlinson JH (1995) The chemistry of eavesdropping, alarm, and deceit. Proc Nat Acad Sci 92(1):23–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Surlykke A, Boel Pedersen S, Jakobsen L (2009a) Echolocating bats emit a highly directional sonar sound beam in the field. Proc R Soc B 276(1658):853–860

    Article  PubMed  Google Scholar 

  • Surlykke A, Ghose K, Moss CF (2009b) Acoustic scanning of natural scenes by echolocation in the big brown bat, Eptesicus fuscus. J Exp Biol 212(7):1011–1020

    Article  PubMed  PubMed Central  Google Scholar 

  • Szwed M, Bagdasarian K, Ahissar E (2003) Encoding of vibrissal active touch. Neuron 40(3):621–630

    Article  CAS  PubMed  Google Scholar 

  • Tan EW, Nizar JM, Carrera-G E, Fortune ES (2005) Electrosensory interference in naturally occurring aggregates of a species of weakly electric fish, Eigenmannia virescens. Behav Brain Res 164(1):83–92

    Article  PubMed  Google Scholar 

  • Teyke T (1988) Flow field, swimming velocity and boundary layer: parameters which affect the stimulus for the lateral line organ in blind fish. J Comp Physiol A 163(1):53–61

    Article  CAS  PubMed  Google Scholar 

  • Toerring M-J, Møller P (1984) Locomotor and electric displays associated with electrolocation during exploratory behavior in mormyrid fish. Behav Brain Res 12(3):291–306

    Article  CAS  PubMed  Google Scholar 

  • Von Campenhausen C, Riess I, Weissert R (1981) Detection of stationary objects by the blind cave fish Anoptichthys jordani (Characidae). J Comp Physiol 143(3):369–374

    Article  Google Scholar 

  • Windsor SP, Tan D, Montgomery JC (2008) Swimming kinematics and hydrodynamic imaging in the blind mexican cave fish (Astyanax fasciatus). J Exp Biol 211(18):2950–2959

    Article  PubMed  Google Scholar 

  • Windsor SP, Norris SE, Cameron SM, Mallison GD, Montogmery JC (2010) The flow fields involved in hydrodynamic imaging by blind Mexican cave fish (Astyanax fasciatus). Part II: gliding parallel to a wall. J Exp Biol 213:3832–3842

    Article  PubMed  Google Scholar 

  • Yang SC-H, Wolpert DM, Lengyel M (2016) Theoretical perspectives on active sensing. Curr Opin Behav Sci 11:100–108

    Article  CAS  Google Scholar 

  • Yarbus AL (1967) Eye movements and vision. Plenum Press, New York

    Book  Google Scholar 

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Acknowledgments

This material is based on work supported by a Complex Systems Scholar Award from the James McDonnell Foundation under Grant 112836 to Noah J. Cowan and Grants 1557858 and 1557895 from the National Science Foundation to Noah J. Cowan and Eric S. Fortune.

Compliance with Ethics Requirements

Sarah A. Stamper declares that she has no conflict of interest.

Manu S. Madhav declares that he has no conflict of interest.

Noah J. Cowan declares that he has no conflict of interest.

Eric S. Fortune declares that he has no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Mechanical Engineering, The Johns Hopkins University, Baltimore, MD, USA

    Sarah A. Stamper & Noah J. Cowan

  2. Zanvyl Krieger Mind/Brain Institute, The Johns Hopkins University, Baltimore, MD, USA

    Manu S. Madhav

  3. Federated Department of Biological Sciences, New Jersey Institute of Technology, Newark, NJ, USA

    Eric S. Fortune

Authors
  1. Sarah A. Stamper
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  2. Manu S. Madhav
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  3. Noah J. Cowan
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  4. Eric S. Fortune
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Corresponding author

Correspondence to Eric S. Fortune .

Editor information

Editors and Affiliations

  1. Department of Biology, Washington University in St. Louis, St. Louis, MO, USA

    Bruce A. Carlson

  2. Department of Psychology, University of Washington, Seattle, WA, USA

    Joseph A. Sisneros

  3. Department of Biology, University of Maryland, College Park, MD, USA

    Arthur N. Popper

  4. Department of Psychology, Loyola University Chicago, Chicago, IL, USA

    Richard R. Fay

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Stamper, S.A., Madhav, M.S., Cowan, N.J., Fortune, E.S. (2019). Using Control Theory to Characterize Active Sensing in Weakly Electric Fishes. In: Carlson, B., Sisneros, J., Popper, A., Fay, R. (eds) Electroreception: Fundamental Insights from Comparative Approaches. Springer Handbook of Auditory Research, vol 70. Springer, Cham. https://doi.org/10.1007/978-3-030-29105-1_8

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