1932

Abstract

Here, we review the role of control theory in modeling neural control systems through a top-down analysis approach. Specifically, we examine the role of the brain and central nervous system as the controller in the organism, connected to but isolated from the rest of the animal through insulated interfaces. Though biological and engineering control systems operate on similar principles, they differ in several critical features, which makes drawing inspiration from biology for engineering controllers challenging but worthwhile. We also outline a procedure that the control theorist can use to draw inspiration from the biological controller: starting from the intact, behaving animal; designing experiments to deconstruct and model hierarchies of feedback; modifying feedback topologies; perturbing inputs and plant dynamics; using the resultant outputs to perform system identification; and tuning and validating the resultant control-theoretic model using specially engineered robophysical models.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-control-060117-104856
2020-05-03
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/control/3/1/annurev-control-060117-104856.html?itemId=/content/journals/10.1146/annurev-control-060117-104856&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Wallace AR 1858. On the tendency of varieties to depart indefinitely from the original type. Proc. Linn. Soc. Lond. 3:53–62
    [Google Scholar]
  2. 2. 
    Gross CG 1998. Claude Bernard and the constancy of the internal environment. Neuroscientist 4:380–85
    [Google Scholar]
  3. 3. 
    Milhorn HT 1966. Application of Control Theory to Physiological Systems Philadelphia: Saunders
  4. 4. 
    Acott TS, Kelley MJ, Keller KE, Vranka JA, Abu-Hassan DW, et al 2014. Intraocular pressure homeostasis: maintaining balance in a high-pressure environment. J. Ocul. Pharmacol. Ther. 30:94–101
    [Google Scholar]
  5. 5. 
    Loeb G 1995. Control implications of musculoskeletal mechanics. Proceedings of 17th International Conference of the Engineering in Medicine and Biology Society 21393–94 Piscataway, NJ: IEEE
    [Google Scholar]
  6. 6. 
    Savage MV, Brengelmann GL 1996. Control of skin blood flow in the neutral zone of human body temperature regulation. J. Appl. Physiol. 80:1249–57
    [Google Scholar]
  7. 7. 
    Cowan NJ, Ankarali MM, Dyhr JP, Madhav MS, Roth E, et al 2014. Feedback control as a framework for understanding tradeoffs in biology. Integr. Comp. Biol. 54:223–37
    [Google Scholar]
  8. 8. 
    Roth E, Sponberg S, Cowan NJ 2014. A comparative approach to closed-loop computation. Curr. Opin. Neurobiol. 25:54–62
    [Google Scholar]
  9. 9. 
    Chiel HJ, Beer RD 1997. The brain has a body: adaptive behavior emerges from interactions of nervous system, body and environment. Trends. Neurosci. 20:553–57
    [Google Scholar]
  10. 10. 
    Hooven FJ 1978. The Wright brothers’ flight-control system. Scientific American166–85
    [Google Scholar]
  11. 11. 
    Vecchio DD, Sontag ED 2009. Engineering principles in bio-molecular systems: from retroactivity to modularity. Eur. J. Control 15:389–97
    [Google Scholar]
  12. 12. 
    Del Vecchio D, Ninfa AJ, Sontag ED 2008. Modular cell biology: retroactivity and insulation. Mol. Syst. Biol. 4:161
    [Google Scholar]
  13. 13. 
    Tytell ED, Holmes P, Cohen AH 2011. Spikes alone do not behavior make: why neuroscience needs biomechanics. Curr. Opin. Neurobiol. 21:816–22
    [Google Scholar]
  14. 14. 
    Sefati S, Neveln ID, Roth E, Mitchell T, Snyder JB, et al 2013. Mutually opposing forces during locomotion can eliminate the tradeoff between maneuverability and stability. PNAS 110:18798–803
    [Google Scholar]
  15. 15. 
    Mongeau JM, Demir A, Lee J, Cowan NJ, Full RJ 2013. Locomotion- and mechanics-mediated tactile sensing: antenna reconfiguration simplifies control during high-speed navigation in cockroaches. J. Exp. Biol. 216:4530–41
    [Google Scholar]
  16. 16. 
    Alcocer-Cuarón C, Rivera AL, Castaño VM 2014. Hierarchical structure of biological systems: a bioengineering approach. Bioengineered 5:73–79
    [Google Scholar]
  17. 17. 
    Loeb GE, Brown IE, Cheng EJ 1999. A hierarchical foundation for models of sensorimotor control. Exp. Brain. Res. 126:1–18
    [Google Scholar]
  18. 18. 
    Mongeau JM, Sponberg SN, Miller JP, Full RJ 2015. Sensory processing within cockroach antenna enables rapid implementation of feedback control for high-speed running maneuvers. J. Exp. Biol. 218:2344–54
    [Google Scholar]
  19. 19. 
    Wolpert DM, Flanagan J 2001. Motor prediction. Curr. Biol. 11:R729–32
    [Google Scholar]
  20. 20. 
    Bajcsy R 1988. Active perception. Proc. IEEE 76:996–1005
    [Google Scholar]
  21. 21. 
    Grant RA, Mitchinson B, Fox CW, Prescott TJ 2009. Active touch sensing in the rat: anticipatory and regulatory control of whisker movements during surface exploration. J. Neurophysiol. 101:862–74
    [Google Scholar]
  22. 22. 
    Jung SN, Borst A, Haag J 2011. Flight activity alters velocity tuning of fly motion-sensitive neurons. J. Neurosci. 31:9231–37
    [Google Scholar]
  23. 23. 
    Lederman SJ, Klatzky RL 1987. Hand movements: a window into haptic object recognition. Cogn. Psychol. 19:342–68
    [Google Scholar]
  24. 24. 
    Gibson J 1962. Observations on active touch. Psychol. Rev. 69:477–91
    [Google Scholar]
  25. 25. 
    Bastian J 1982. Vision and electroreception: integration of sensory information in the optic tectum of the weakly electric fish Apteronotus albifrons. J. Comp. Physiol. A 147:287–97
    [Google Scholar]
  26. 26. 
    Rose GJ, Canfield JG 1993. Longitudinal tracking responses of Eigenmannia and Sternopygus. J. Comp. Physiol. A 173:698–700
    [Google Scholar]
  27. 27. 
    Stamper SA, Roth E, Cowan NJ, Fortune ES 2012. Active sensing via movement shapes spatiotemporal patterns of sensory feedback. J. Exp. Biol. 215:1567–74
    [Google Scholar]
  28. 28. 
    Uyanik I, Stamper SA, Cowan NJ, Fortune ES 2019. Sensory cues modulate smooth pursuit and active sensing movements. Front. Behav. Neurosci. 13:59
    [Google Scholar]
  29. 29. 
    Nelson ME, MacIver MA 1999. Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. J. Exp. Biol. 202:1195–203
    [Google Scholar]
  30. 30. 
    Hofmann V, Sanguinetti-Scheck JI, Kunzel S, Geurten B, Gomez-Sena L, Engelmann J 2013. Sensory flow shaped by active sensing: sensorimotor strategies in electric fish. J. Exp. Biol. 216:2487–500
    [Google Scholar]
  31. 31. 
    Biswas D, Arend LA, Stamper SA, Vágvölgyi BP, Fortune ES, Cowan NJ 2018. Closed-loop control of active sensing movements regulates sensory slip. Curr. Biol. 28:4029–36.e4
    [Google Scholar]
  32. 32. 
    Kunapareddy A, Cowan NJ 2018. Recovering observability via active sensing. 2018 American Control Conference2821–26 Piscataway, NJ: IEEE
    [Google Scholar]
  33. 33. 
    Liu D, Todorov E 2007. Evidence for the flexible sensorimotor strategies predicted by optimal feedback control. J. Neurosci. 27:9354–68
    [Google Scholar]
  34. 34. 
    Todorov E, Jordan MI 2002. Optimal feedback control as a theory of motor coordination. Nat. Neurosci. 5:1226–35
    [Google Scholar]
  35. 35. 
    Jun JJ, Longtin A, Maler L 2016. Active sensing associated with spatial learning reveals memory-based attention in an electric fish. J. Neurophysiol. 115:2577–92
    [Google Scholar]
  36. 36. 
    McNamee D, Wolpert DM 2019. Internal models in biological control. Annu. Rev. Control Robot. Auton. Syst. 2:339–64
    [Google Scholar]
  37. 37. 
    Brooks JX, Carriot J, Cullen KE 2015. Learning to expect the unexpected: rapid updating in primate cerebellum during voluntary self-motion. Nat. Neurosci. 18:1310–17
    [Google Scholar]
  38. 38. 
    Miall R, Wolpert D 1996. Forward models for physiological motor control. Neural Netw. 9:1265–79
    [Google Scholar]
  39. 39. 
    Wolpert DM, Miall R, Kawato M 1998. Internal models in the cerebellum. Trends. Neurosci. 2:338–47
    [Google Scholar]
  40. 40. 
    Baumann O, Borra RJ, Bower JM, Cullen KE, Habas C, et al 2015. Consensus paper: the role of the cerebellum in perceptual processes. Cerebellum 14:197–220
    [Google Scholar]
  41. 41. 
    Bhanpuri NH, Okamura AM, Bastian AJ 2014. Predicting and correcting ataxia using a model of cerebellar function. Brain 137:1931–44
    [Google Scholar]
  42. 42. 
    Körding KP, Ku Sp, Wolpert DM 2004. Bayesian integration in force estimation. J. Neurophysiol. 92:3161–65
    [Google Scholar]
  43. 43. 
    Körding KP, Wolpert DM 2004. Bayesian integration in sensorimotor learning. Nature 427:244–7
    [Google Scholar]
  44. 44. 
    Aström KJ, Wittenmark B 2013. Adaptive Control North Chelmsford, MA: Courier
  45. 45. 
    Sun J 2014. Model reference adaptive control. Encyclopedia of Systems and Control London: Springer https://doi.org/10.1007/978-1-4471-5102-9_116-1
    [Crossref] [Google Scholar]
  46. 46. 
    Conant RC, Ross Ashby W 1970. Every good regulator of a system must be a model of that system. Int. J. Syst. Sci. 1:89–97
    [Google Scholar]
  47. 47. 
    Tin C, Poon CS 2005. Internal models in sensorimotor integration: perspectives from adaptive control theory. J. Neural Eng. 2:1–37
    [Google Scholar]
  48. 48. 
    Full RJ, Koditschek DE 1999. Templates and anchors: neuromechanical hypotheses of legged locomotion on land. J. Exp. Biol. 202:3325–32
    [Google Scholar]
  49. 49. 
    Clarke D, Mohtadi C, Tuffs P 1987. Generalized predictive control—part I. The basic algorithm. Automatica 23:137–48
    [Google Scholar]
  50. 50. 
    Johansson RS, Cole KJ 1992. Sensory-motor coordination during grasping and manipulative actions. Curr. Opin. Neurobiol. 2:815–23
    [Google Scholar]
  51. 51. 
    Collins CJS, Barnes GR 2009. Predicting the unpredictable: Weighted averaging of past stimulus timing facilitates ocular pursuit of randomly timed stimuli. J. Neurosci. 29:13302–14
    [Google Scholar]
  52. 52. 
    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. 214:1170–80
    [Google Scholar]
  53. 53. 
    Cutlip S, Freudenberg J, Cowan N, Gillespie RB 2019. Haptic feedback and the internal model principle. 2019 IEEE World Haptics Conference568–73 Piscataway, NJ: IEEE
    [Google Scholar]
  54. 54. 
    Huang J, Isidori A, Marconi L, Mischiati M, Sontag E, Wonham W 2018. Internal models in control, biology and neuroscience. 2018 IEEE Conference on Decision and Control5370–90 Piscataway, NJ: IEEE
    [Google Scholar]
  55. 55. 
    Francis BA, Wonham WM 1976. The internal model principle of control theory. Automatica 12:457–65
    [Google Scholar]
  56. 56. 
    Tolman EC 1948. Cognitive maps in rats and men. Psychol. Rev. 55:189–208
    [Google Scholar]
  57. 57. 
    O'Keefe J, Dostrovsky J 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34:171–75
    [Google Scholar]
  58. 58. 
    Taube JS, Muller RU, Ranck JB 1990. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10:420–35
    [Google Scholar]
  59. 59. 
    Hafting T, Fyhn M, Molden S, Moser MB, Moser EI 2005. Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–6
    [Google Scholar]
  60. 60. 
    Savelli F, Yoganarasimha D, Knierim JJ 2008. Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18:1270–82
    [Google Scholar]
  61. 61. 
    Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI 2008. Representation of geometric borders in the entorhinal cortex. Science 322:1865–68
    [Google Scholar]
  62. 62. 
    Wang C, Chen X, Lee H, Deshmukh SS, Yoganarasimha D, et al 2018. Egocentric coding of external items in the lateral entorhinal cortex. Science 362:945–49
    [Google Scholar]
  63. 63. 
    Deshmukh SS, Knierim JJ 2013. Influence of local objects on hippocampal representations: landmark vectors and memory. Hippocampus 23:253–67
    [Google Scholar]
  64. 64. 
    Lever C, Burton S, Jeewajee A, O'Keefe J, Burgess N 2009. Boundary vector cells in the subiculum of the hippocampal formation. J. Neurosci. 29:9771–77
    [Google Scholar]
  65. 65. 
    Høydal ØA, Skytøen ER, Andersson SO, Moser MB, Moser EI 2019. Object-vector coding in the medial entorhinal cortex. Nature 568:400–4
    [Google Scholar]
  66. 66. 
    Quirk GJ, Muller RU, Kubie JL 1990. The firing of hippocampal place cells in the dark depends on the rat's recent experience. J. Neurosci. 10:2008–17
    [Google Scholar]
  67. 67. 
    Zhang S, Schönfeld F, Wiskott L, Manahan-Vaughan D 2014. Spatial representations of place cells in darkness are supported by path integration and border information. Front. Behav. Neurosci. 8:222
    [Google Scholar]
  68. 68. 
    MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H 2011. Hippocampal “time cells” bridge the gap in memory for discontiguous events. Neuron 71:737–49
    [Google Scholar]
  69. 69. 
    Aronov D, Nevers R, Tank DW 2017. Mapping of a non-spatial dimension by the hippocampalentorhinal circuit. Nature 543:719–22
    [Google Scholar]
  70. 70. 
    Yartsev MM, Ulanovsky N 2013. Representation of three-dimensional space in the hippocampus of flying bats. Science 340:367–72
    [Google Scholar]
  71. 71. 
    Danjo T, Toyoizumi T, Fujisawa S 2018. Spatial representations of self and other in the hippocampus. Science 359:213–18
    [Google Scholar]
  72. 72. 
    Omer DB, Maimon SR, Las L, Ulanovsky N 2018. Social place-cells in the bat hippocampus. Science 359:218–24
    [Google Scholar]
  73. 73. 
    Derdikman D, Knierim JJ eds 2014. Space, Time and Memory in the Hippocampal Formation New York: Springer
  74. 74. 
    Savelli F, Knierim JJ 2019. Origin and role of path integration in the cognitive representations of the hippocampus: computational insights into open questions. J. Exp. Biol. 222:jeb188912
    [Google Scholar]
  75. 75. 
    Chen G, Lu Y, King JA, Cacucci F, Burgess N 2019. Differential influences of environment and self-motion on place and grid cell firing. Nat. Commun. 10:630
    [Google Scholar]
  76. 76. 
    Jayakumar RP, Madhav MS, Savelli F, Blair HT, Cowan NJ, Knierim JJ 2019. Recalibration of path integration in hippocampal place cells. Nature 566:533–37
    [Google Scholar]
  77. 77. 
    Campbell MG, Ocko SA, Mallory CS, Low II, Ganguli S, Giocomo LM 2018. Principles governing the integration of landmark and self-motion cues in entorhinal cortical codes for navigation. Nat. Neurosci. 21:1096–106
    [Google Scholar]
  78. 78. 
    Dissanayake M, Newman P, Clark S, Durrant-Whyte H, Csorba M 2001. A solution to the simultaneous localization and map building (SLAM) problem. IEEE Trans. Robot. Automat. 17:229–41
    [Google Scholar]
  79. 79. 
    Goldberg JM, Fernandez C 1971. Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular accelerations. J. Neurophysiol. 34:635–60
    [Google Scholar]
  80. 80. 
    Robinson DA 1981. The use of control systems analysis in the neurophysiology of eye movements. Annu. Rev. Neurosci. 4:463–503
    [Google Scholar]
  81. 81. 
    Shapley R, Enroth-Cugell C 1984. Visual adaptation and retinal gain control. Prog. Retin. Res. 3:263–346
    [Google Scholar]
  82. 82. 
    Demb JB 2008. Functional circuitry of visual adaptation in the retina. J. Physiol. 586:4377–84
    [Google Scholar]
  83. 83. 
    Atick JJ, Redlich AN 1992. What does the retina know about natural scenes?. Neural Comput. 4:196–210
    [Google Scholar]
  84. 84. 
    Rivlin-Etzion M, Grimes WN, Rieke F 2018. Flexible neural hardware supports dynamic computations in retina. Trends Neurosci. 41:224–37
    [Google Scholar]
  85. 85. 
    Hogan N 1984. Adaptive control of mechanical impedance by coactivation of antagonist muscle. IEEE Trans. Autom. Control 29:681–90
    [Google Scholar]
  86. 86. 
    Camhi JM, Johnson EN 1999. High-frequency steering maneuvers mediated by tactile cues: antennal wall-following in the cockroach. J. Exp. Biol. 202:631–43
    [Google Scholar]
  87. 87. 
    Lee J, Sponberg SN, Loh OY, Lamperski AG, Full RJ, Cowan NJ 2008. Templates and anchors for antenna-based wall following in cockroaches and robots. IEEE Trans. Robot. 24:130–43
    [Google Scholar]
  88. 88. 
    Mongeau JM, Demir A, Dallmann CJ, Jayaram K, Cowan NJ, Full RJ 2014. Mechanical processing via passive dynamic properties of the cockroach antenna can facilitate control during rapid running. J. Exp. Biol. 217:3333–45
    [Google Scholar]
  89. 89. 
    Brandman O, Meyer T 2008. Feedback loops shape cellular signals in space and time. Science 322:390–95
    [Google Scholar]
  90. 90. 
    Shraiman BI 2005. Mechanical feedback as a possible regulator of tissue growth. PNAS 102:3318–23
    [Google Scholar]
  91. 91. 
    Röder PV, Wu B, Liu Y, Han W 2016. Pancreatic regulation of glucose homeostasis. Exp. Mol. Med. 48:e219
    [Google Scholar]
  92. 92. 
    Powers WT 1973. Feedback: beyond behaviorism. Science 179:351–56
    [Google Scholar]
  93. 93. 
    Roth E, Hall RW, Daniel TL, Sponberg S 2016. Integration of parallel mechanosensory and visual pathways resolved through sensory conflict. PNAS 113:12832–37
    [Google Scholar]
  94. 94. 
    Burridge RR, Rizzi AA, Koditschek DE 1999. Sequential composition of dynamically dexterous robot behavior. Int. J. Robot. Res. 18:534–55
    [Google Scholar]
  95. 95. 
    Kallem V, Komoroski AT, Kumar V 2011. Sequential composition for navigating a nonholonomic cart in the presence of obstacles. IEEE Trans. Robot. 27:1152–59
    [Google Scholar]
  96. 96. 
    Ballard DH 2015. Brain Computation as Hierarchical Abstraction Cambridge, MA: MIT Press
  97. 97. 
    an der Heiden U 1979. Delays in physiological systems. J. Math. Biol. 8:345–64
    [Google Scholar]
  98. 98. 
    More HL, Donelan JM 2018. Scaling of sensorimotor delays in terrestrial mammals. Proc. R. Soc. B 285:20180613
    [Google Scholar]
  99. 99. 
    Cowan NJ, Lee J, Full RJ 2006. Task-level control of rapid wall following in the American cockroach. J. Exp. Biol. 209:1617–29
    [Google Scholar]
  100. 100. 
    Liu P, Cheng B 2017. Limitations of rotational manoeuvrability in insects and hummingbirds: evaluating the effects of neuro-biomechanical delays and muscle mechanical power. J. R. Soc. Interface 14:20170068
    [Google Scholar]
  101. 101. 
    Elzinga MJ, Dickson WB, Dickinson MH 2012. The influence of sensory delay on the yaw dynamics of a flapping insect. J. R. Soc. Interface 9:1685–96
    [Google Scholar]
  102. 102. 
    Beaudry NJ, Renner R 2011. An intuitive proof of the data processing inequality. arXiv:1107.0740 [quant-ph]
    [Google Scholar]
  103. 103. 
    Faisal AA, Selen LPJ, Wolpert DM 2008. Noise in the nervous system. Nat. Rev. Neurosci. 9:292–303
    [Google Scholar]
  104. 104. 
    Longtin A 2003. Effects of noise on nonlinear dynamics. Nonlinear Dynamics in Physiology and Medicine149–89 New York: Springer
    [Google Scholar]
  105. 105. 
    Horsthemke W, Lefever R 1984. Noise-induced transitions in physics, chemistry, and biology. Noise-Induced Transitions: Theory and Applications in Physics, Chemistry, and Biology164–200 Berlin: Springer
    [Google Scholar]
  106. 106. 
    Todorov E 2005. Stochastic optimal control and estimation methods adapted to the noise characteristics of the sensorimotor system. Neural Comput. 17:1084–108
    [Google Scholar]
  107. 107. 
    Carver SG, Fortune ES, Cowan NJ 2013. State-estimation and cooperative control with uncertain time. 2013 American Control Conference2990–95 Piscataway, NJ: IEEE
    [Google Scholar]
  108. 108. 
    Lamperski A, Cowan NJ 2016. Optimal control with noisy time. IEEE Trans. Autom. Control 61:319–33
    [Google Scholar]
  109. 109. 
    Bulsara A, Jacobs EW, Zhou T, Moss F, Kiss L 1991. Stochastic resonance in a single neuron model: theory and analog simulation. J. Theor. Biol. 152:531–55
    [Google Scholar]
  110. 110. 
    Gluckman BJ, Netoff TI, Neel EJ, Spano WL, Spano ML, Schiff SJ 1996. Stochastic resonance in a neuronal network from mammalian brain. Phys. Rev. Lett. 77:4098–101
    [Google Scholar]
  111. 111. 
    Pozzorini C, Naud R, Mensi S, Gerstner W 2013. Temporal whitening by power-law adaptation in neocortical neurons. Nat. Neurosci. 16:942–48
    [Google Scholar]
  112. 112. 
    Huang CG, Zhang ZD, Chacron MJ 2016. Temporal decorrelation by SK channels enables efficient neural coding and perception of natural stimuli. Nat. Commun. 7:11353
    [Google Scholar]
  113. 113. 
    Heiligenberg W 1991. The neural basis of behavior: a neuroethological view. Annu. Rev. Neurosci. 14:247–67
    [Google Scholar]
  114. 114. 
    Jindrich DL, Full RJ 2002. Dynamic stabilization of rapid hexapedal locomotion. J. Exp. Biol. 205:2803–23
    [Google Scholar]
  115. 115. 
    Dyhr JP, Morgansen KA, Daniel TL, Cowan NJ 2013. Flexible strategies for flight control: an active role for the abdomen. J. Exp. Biol. 216:1523–36
    [Google Scholar]
  116. 116. 
    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. 2012 IEEE 51st IEEE Conference on Decision and Control3721–26 Piscataway, NJ: IEEE
    [Google Scholar]
  117. 117. 
    Sutton EE, Demir A, Stamper SA, Fortune ES, Cowan NJ 2016. Dynamic modulation of visual and electrosensory gains for locomotor control. J. R. Soc. Interface 13:20160057
    [Google Scholar]
  118. 118. 
    Sponberg S, Dyhr JP, Hall RW, Daniel TL 2015. Luminance-dependent visual processing enables moth flight in low light. Science 348:1245–48
    [Google Scholar]
  119. 119. 
    Stamper SA, Madhav MS, Cowan NJ, Fortune ES 2012. Beyond the jamming avoidance response: Weakly electric fish respond to the envelope of social electrosensory signals. J. Exp. Biol. 215:4196–207
    [Google Scholar]
  120. 120. 
    Sepulchre R, Drion G, Franci A 2019. Control across scales by positive and negative feedback. Annu. Rev. Control Robot. Auton. Syst. 2:89–113
    [Google Scholar]
  121. 121. 
    Anderson PW 1972. More is different. Science 177:393–96
    [Google Scholar]
  122. 122. 
    Krakauer JW, Ghazanfar AA, Gomez-Marin A, MacIver MA, Poeppel D 2017. Neuroscience needs behavior: correcting a reductionist bias. Neuron 93:480–90
    [Google Scholar]
  123. 123. 
    Cowan NJ, Fortune ES 2007. The critical role of locomotion mechanics in decoding sensory systems. J. Neurosci. 27:1123–8
    [Google Scholar]
  124. 124. 
    Amari S 1977. Dynamics of pattern formation in lateral-inhibition type neural fields. Biol. Cybern. 27:77–87
    [Google Scholar]
  125. 125. 
    Amit DJ, Tsodyks M 1991. Quantitative study of attractor neural network retrieving at low spike rates: I. Substrate—spikes, rates and neuronal gain. Netw. Comput. Neural. Syst. 2:259–73
    [Google Scholar]
  126. 126. 
    Samsonovich A, McNaughton BL 1997. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17:5900–20
    [Google Scholar]
  127. 127. 
    Burak Y, Fiete IR 2009. Accurate path integration in continuous attractor network models of grid cells. PLOS Comput. Biol. 5:e1000291
    [Google Scholar]
  128. 128. 
    Megías M, Emri Z, Freund T, Gulyás A 2001. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102:527–40
    [Google Scholar]
  129. 129. 
    Metzner W 1993. The jamming avoidance response in Eigenmannia is controlled by two separate motor pathways. J. Neurosci. 13:1862–78
    [Google Scholar]
  130. 130. 
    Kirschbaum F 1983. Myogenic electric organ precedes the neurogenic organ in apteronotid fish. Naturwissenschaften 70:205–7
    [Google Scholar]
  131. 131. 
    Dickinson MH, Muijres FT 2016. The aerodynamics and control of free flight manoeuvres in Drosophila. Philos. Trans. R. Soc. B 371:20150388
    [Google Scholar]
  132. 132. 
    Zhang C, Hedrick TL, Mittal R 2018. An integrated study of the aeromechanics of hovering flight in perturbed flows. AIAA J. 57:3753–64
    [Google Scholar]
  133. 133. 
    Sane SP, Dieudonne A, Willis Ma, Daniel TL 2007. Antennal mechanosensors mediate flight control in moths. Science 315:863–66
    [Google Scholar]
  134. 134. 
    Bhushan N, Shadmehr R 1999. Computational nature of human adaptive control during learning of reaching movements in force fields. Biol. Cybern. 81:39–60
    [Google Scholar]
  135. 135. 
    Kiemel T, Zhang Y, Jeka JJ 2011. Identification of neural feedback for upright stance in humans: stabilization rather than sway minimization. J. Neurosci. 31:15144–53
    [Google Scholar]
  136. 136. 
    van der Kooij H, van Asseldonk E, van der Helm FCT 2005. Comparison of different methods to identify and quantify balance control. J. Neurosci. Methods 145:175–203
    [Google Scholar]
  137. 137. 
    Theobald JC, Ringach DL, Frye MA 2010. Dynamics of optomotor responses in Drosophila to perturbations in optic flow. J. Exp. Biol. 213:1366–75
    [Google Scholar]
  138. 138. 
    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. 216:4272–84
    [Google Scholar]
  139. 139. 
    Fussmann GF, Ellner SP, Shertzer KW, Hairston NG Jr 2000. Crossing the Hopf bifurcation in a live predator-prey system. Science 290:1358–60
    [Google Scholar]
  140. 140. 
    O'Connor SM, Donelan JM 2012. Fast visual prediction and slow optimization of preferred walking speed. J. Neurophysiol. 107:2549–59
    [Google Scholar]
  141. 141. 
    Reiser MB, Dickinson MH 2008. A modular display system for insect behavioral neuroscience. J. Neurosci. Methods 167:127–39
    [Google Scholar]
  142. 142. 
    Maimon G, Straw AD, Dickinson MH 2008. A simple vision-based algorithm for decision making in flying Drosophila. Curr. Biol. 18:464–70
    [Google Scholar]
  143. 143. 
    Reiser MB, Dickinson MH 2010. Drosophila fly straight by fixating objects in the face of expanding optic flow. J. Exp. Biol. 213:1771–81
    [Google Scholar]
  144. 144. 
    Beatus T, Guckenheimer JM, Cohen I 2015. Controlling roll perturbations in fruit flies. J. R. Soc. Interface 12:20150075
    [Google Scholar]
  145. 145. 
    Seelig JD, Chiappe ME, Lott GK, Dutta A, Osborne JE, et al 2010. Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior. Nat. Methods 7:535–40
    [Google Scholar]
  146. 146. 
    Seelig JD, Jayaraman V 2015. Neural dynamics for landmark orientation and angular path integration. Nature 521:186–91
    [Google Scholar]
  147. 147. 
    Green J, Adachi A, Shah KK, Hirokawa JD, Magani PS, Maimon G 2017. A neural circuit architecture for angular integration in Drosophila. Nature 546:101–6
    [Google Scholar]
  148. 148. 
    Heiligenberg W 1991. The jamming avoidance response of the electric fish, Eigenmannia: computational rules and their neuronal implementation. Semin. Neurosci. 3:3–18
    [Google Scholar]
  149. 149. 
    Zimmermann JB, Jackson A 2014. Closed-loop control of spinal cord stimulation to restore hand function after paralysis. Front. Neurosci. 8:87
    [Google Scholar]
  150. 150. 
    Srinivasan SS, Maimon BE, Diaz M, Song H, Herr HM 2018. Closed-loop functional optogenetic stimulation. Nat. Commun. 9:5303
    [Google Scholar]
  151. 151. 
    Rutishauser U, Kotowicz A, Laurent G 2013. A method for closed-loop presentation of sensory stimuli conditional on the internal brain-state of awake animals. J. Neurosci. Methods 215:139–55
    [Google Scholar]
  152. 152. 
    Schiff SJ 2012. Neural Control Engineering: The Emerging Intersection Between Control Theory and Neuroscience Cambridge, MA: MIT Press
  153. 153. 
    Ljung L 1978. Convergence analysis of parametric identification methods. IEEE Trans. Autom. Control 23:770–83
    [Google Scholar]
  154. 154. 
    Marmarelis PZ, Marmarelis VZ 1978. The white-noise method in system identification. Analysis of Physiological Systems131–80 Boston: Springer
    [Google Scholar]
  155. 155. 
    Nickl RW, Ankarali MM, Cowan NJ 2019. Complementary spatial and timing control in rhythmic arm movements. J. Neurophysiol. 121:1543–60
    [Google Scholar]
  156. 156. 
    Ljung L 2006. Frequency domain versus time domain methods in system identification—revisited. Control of Uncertain Systems: Modelling, Approximation, and Design BA Francis, MC Smith, JC Willems 277–91 Berlin: Springer
    [Google Scholar]
  157. 157. 
    Aström K, Eykhoff P 1971. System identification—a survey. Automatica 7:123–62
    [Google Scholar]
  158. 158. 
    Aguilar J, Zhang T, Qian F, Kingsbury M, McInroe B, et al 2016. A review on locomotion robophysics: the study of movement at the intersection of robotics, soft matter and dynamical systems. Rep. Prog. Phys. 79:110001
    [Google Scholar]
  159. 159. 
    Demir A, Samson EW, Cowan NJ 2010. A tunable physical model of arthropod antennae. 2010 IEEE International Conference on Robotics and Automation3793–98 Piscataway, NJ: IEEE
    [Google Scholar]
  160. 160. 
    Holmes P, Full RJ, Koditschek D, Guckenheimer J 2006. The dynamics of legged locomotion: models, analyses, and challenges. SIAM Rev. 48:207–304
    [Google Scholar]
  161. 161. 
    Pellis SM, Bell HC 2011. Closing the circle between perceptions and behavior: a cybernetic view of behavior and its consequences for studying motivation and development. Dev. Cogn. Neurosci 1:404–13
    [Google Scholar]
  162. 162. 
    Marken RS, Mansell W, Khatib Z 2013. Motor control as the control of perception. Percept. Motor Skills 117:236–47
    [Google Scholar]
/content/journals/10.1146/annurev-control-060117-104856
Loading
/content/journals/10.1146/annurev-control-060117-104856
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error