Journal of Comparative Physiology A

, Volume 192, Issue 6, pp 573–586 | Cite as

Sensory acquisition in active sensing systems

  • M. E. Nelson
  • M. A. MacIver


A defining feature of active sensing is the use of self-generated energy to probe the environment. Familiar biological examples include echolocation in bats and dolphins and active electrolocation in weakly electric fish. Organisms that utilize active sensing systems can potentially exert control over the characteristics of the probe energy, such as its intensity, direction, timing, and spectral characteristics. This is in contrast to passive sensing systems, which rely on extrinsic energy sources that are not directly controllable by the organism. The ability to control the probe energy adds a new dimension to the task of acquiring relevant information about the environment. Physical and ecological constraints confronted by active sensing systems include issues of signal propagation, attenuation, speed, energetics, and conspicuousness. These constraints influence the type of energy that organisms use to probe the environment, the amount of energy devoted to the process, and the way in which the nervous system integrates sensory and motor functions for optimizing sensory acquisition performance.


Active touch Bioluminescence Echolocation Electrolocation Sensory ecology 



Jamming avoidance response



This work was supported by a grant from the National Institute of Mental Health to M.E.N. (R01 MH49242); M.A.M. was supported in part by a grant from the Whitaker Foundation to Northwestern University. We thank Dr. Rüdiger Krahe for stimulating discussions and helpful feedback.


  1. Assad C, Rasnow B, Stoddard PK (1999) Electric organ discharges and electric images during electrolocation. J Exp Biol 202:1185–1193PubMedGoogle Scholar
  2. Au WWL (1993) The sonar of dolphins. Springer, Berlin Heidelberg New YorkGoogle Scholar
  3. Au WWL (2004) A comparison of the sonar capabilities of bats and dolphins. In: Thomas JA, Moss CF, Vater M (eds) Echolocation in bats and dolphins. University of Chicago Press, Chicago, pp xiii–xxviiGoogle Scholar
  4. Au WWL, Benoit-Bird KJ (2003) Automatic gain control in the echolocation system of dolphins. Nature 423:861–863PubMedGoogle Scholar
  5. Au WWL, Snyder KJ (1980) Long-range target detection in open waters by an echolocating atlantic bottlenose dolphin (Tursiops truncatus). J Acoust Soc Am 68:1077–1084Google Scholar
  6. Au WWL, Floyd RW, Penner RH, Murchison AE (1974) Measurement of echolocation signals of the atlantic bottlenose dolphin, Tursiops truncatus Montagu, in open waters. J Acoust Soc Am 56:1280–1290PubMedGoogle Scholar
  7. Bajcsy R (1988) Active perception. Proc IEEE 76:996–1005Google Scholar
  8. Ballard DH (1991) Animate vision. Artif Intell 48:57–86Google Scholar
  9. Barrett-Lennard LG, Ford JKB, Heise KA (1996) The mixed blessing of echolocation: differences in sonar use by fish-eating and mammal-eating killer whales. Anim Behav 51:553–565Google Scholar
  10. Bass AH (1986) Electric organs revisited. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 13–70Google Scholar
  11. Bell CC, Bradbury J, Russell CJ (1976) The electric organ of a mormyrid fish as a current and voltage source. J Comp Physiol A 110:65–88Google Scholar
  12. Berg RW, Kleinfeld D (2003) Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. J Neurophysiol 89:104–117PubMedGoogle Scholar
  13. Blake A (1995) Active vision. In: Arbib MA (ed) The handbook of brain theory and neural networks. MIT Press, Cambridge/Massachusetts, pp 61–63Google Scholar
  14. Bonner JT, Suthers HB, Odell GM (1986) Ammonia orients cell masses and speeds up aggregating cells of slime molds. Nature 323:630–632Google Scholar
  15. Brecht M, Preilowski B, Merzenich MM (1997) Functional architecture of the mystacial vibrissae. Behav Brain Res 84:81–97PubMedGoogle Scholar
  16. Buck JB (1978) Functions and evolutions of bioluminescence. In: Herring PJ (ed) Bioluminescence in action. Academic, New York, pp 419–460Google Scholar
  17. Bullock TH, Heiligenberg W (1986) Electroreception. Wiley, New YorkGoogle Scholar
  18. von Campenhausen C, Riess I, Weissert R (1981) Detection of stationary objects by the blind cave fish Anoptichthys jordani (Characidae). J Comp Physiol A 143:369–374Google Scholar
  19. Carr CE, Maler L, Sas E (1982) Peripheral organization and central projections of the electrosensory nerves in gymnotiform fish. J Comp Neurol 211:139–153PubMedGoogle Scholar
  20. Carvell GE, Simons DJ (1990) Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10:2638–2648PubMedGoogle Scholar
  21. Chen L, House JH, Krahe R, Nelson ME (2005) Modeling signal and background components of electrosensory scenes. J Comp Physiol A 168:331–345Google Scholar
  22. Cranford TW, Amundin M (2004) Biosonar pulse production in odontocetes: the state of our knowledge. In: Thomas JA, Moss CF, Vater M (eds) Echolocation in bats and dolphins. University of Chicago Press, Chicago, pp 27–35Google Scholar
  23. Douglas RH, Partridge JC (1997) On the visual pigments of deep-sea fish. J Fish Biol 50:68–85Google Scholar
  24. Douglas RH, Partridge JC, Dulai K, Hunt D, Mullineaux CW, Tauber A, Hynninen PH (1998) Dragon fish see using chlorophyll. Nature 393:423–424Google Scholar
  25. Dudley R, Winter Y (2002) Hovering flight mechanics of neotropical flower bats (Phyllostomidae: Glossophaginae) in normodense and hypodense gas mixtures. J Exp Biol 205:3669–3677PubMedGoogle Scholar
  26. Dürr V, Konig Y, Kittmann R (2001) The antennal motor system of the stick insect Carausius morosus: anatomy and antennal movement pattern during walking. J Comp Physiol A 187:131–144PubMedGoogle Scholar
  27. Dusenbery DB (1992) Sensory ecology: how organisms acquire and respond to information. WH Freeman, New YorkGoogle Scholar
  28. von der Emde G (1999) Active electrolocation of objects in weakly electric fish. J Exp Biol 202:1205–1215PubMedGoogle Scholar
  29. von der Emde G (2006) Non-visual environmental imaging and object detection through active electrolocation in weakly electric fish. J Comp Physiol A (in press)Google Scholar
  30. von der Emde G, Ringer T (1992) Electrolocation of capacitive objects in four species of pulse-type weakly electric fish. I. Discrimination performance. Ethology 91:326–338CrossRefGoogle Scholar
  31. Erwin H, Wilson WW, Moss CF (2001) A computational model of sensorimotor integration in bat echolocation. J Acoust Soc Am 110:1176–1187PubMedGoogle Scholar
  32. Evans WE (1973) Echolocation by marine delphinids and one species of freshwater dolphin. J Acoust Soc Am 54:191–199Google Scholar
  33. Fenton MB (2004) Aerial-feeding bats: getting the most out of echolocation. In: Thomas JA, Moss CF, Vater M (eds) Echolocation in bats and dolphins. University of Chicago Press, Chicago, pp 350–355Google Scholar
  34. Fernald RD (1997) The evolution of eyes. Brain Behav Evol 50:253–259PubMedGoogle Scholar
  35. Franchina CR, Stoddard PK (1998) Plasticity of the electric organ discharge waveform of the electric fish Brachyhypopomus pinnicaudatus. I. Quantification of day–night changes. J Comp Physiol A 183:759–768PubMedGoogle Scholar
  36. Fuzessery ZM, Hartley DJ, Wenstrup JJ (1992) Spatial processing within the moustache bat echolocation system: possible mechanisms for optimization. J Comp Physiol A 170:57–71PubMedGoogle Scholar
  37. Gao P, Bermejo R, Zeigler HP (2001) Vibrissa deafferentation and rodent whisking patterns: behavioral evidence for a central pattern generator. J Neurosci 21:5374–5380PubMedGoogle Scholar
  38. Ghose K, Moss CF (2003) The sonar beam pattern of a flying bat as it tracks tethered insects. J Acoust Soc Am 114:1120–1131PubMedGoogle Scholar
  39. Hartley DJ (1992) Stabilization of perceived echo amplitudes in echolocating bats. I. Echo detection and automatic gain control in the big brown bat, Eptesicus fuscus, and the fishing bat, Noctilio leporinus. J Acoust Soc Am 91:1120–1132PubMedGoogle Scholar
  40. Hartley DJ, Suthers RA (1989) The sound emission pattern of the echolocating bat, Eptesicus fuscus. J Acoust Soc Am 85:1348–1351Google Scholar
  41. Hartmann MJ (2001) Active sensing capabilities of the rat whisker system. Auton Robot 11:249–254Google Scholar
  42. Hartmann MJ, Johnson NJ, Towal RB, Assad C (2003) Mechanical characteristics of rat vibrissae: resonant frequencies and damping in isolated whiskers and in the awake behaving animal. J Neurosci 23:6510–6519PubMedGoogle Scholar
  43. Hassan ES (1989) Hydrodynamic imaging of the surroundings by the lateral line of the blind cave fish Anoptichthys jordani. In: Coombs S, Peter G, Heinrich M (eds) The mechanosensory lateral line: neurobiology and evolution. Springer, Berlin Heidelberg New York, pp 217–227Google Scholar
  44. Haygood MG (1993) Light organ symbioses in fishes. Crit Rev Microbiol 19:191–216PubMedGoogle Scholar
  45. Heiligenberg W (1975) Theoretical and experimental approaches to spatial aspects of electrolocation. J Comp Physiol A 103:247–272Google Scholar
  46. Heiligenberg W (1991) Neural nets in electric fish. The MIT Press, Cambridge/MassachusettsGoogle Scholar
  47. Heiligenberg W, Baker C, Bastian J (1978) The jamming avoidance response in gymnotoid pulse species: a mechanism to minimize the probability of pulse train coincidence. J Comp Physiol A 124:211–224Google Scholar
  48. Henze D, O’Neill WE (1991) The emission pattern of vocalizations and directionality of the sonar system in the echolocating bat, Pteronotus parnelli. J Acoust Soc Am 89:2430–2434PubMedGoogle Scholar
  49. Herzing DL (2004) Social and nonsocial uses of echolocation in free-ranging Stenella frontalis and Tursiops truncatus. In: Thomas JA, Moss CF, Vater M (eds) Echolocation in bats and dolphins. University of Chicago Press, Chicago, pp 404–410Google Scholar
  50. Holderied MW, von Helversen O (2003) Echolocation range and wingbeat period match in aerial-hawking bats. Proc R Soc Lond B 270:2293–2299Google Scholar
  51. Holland RA, Waters DA, Rayner JMV (2004) Echolocation signal structure in the megachiropteran bat Rousettus aegyptiacus Geoffroy 1810. J Exp Biol 207:4361–4369PubMedGoogle Scholar
  52. Hopkins CD (1976) Stimulus filtering and electroreception: tuberous electroreceptors in three species of gymnotoid fish. J Comp Physiol A 111:171–207Google Scholar
  53. Hopkins CD (1986) Temporal structure of non-propagated electric communication. Brain Behav Evol 28:43–59PubMedGoogle Scholar
  54. Hopkins CD (1999) Design features for electric communication. J Exp Biol 202:1217–1228PubMedGoogle Scholar
  55. Hopkins CD, Shieh KT, McBride DW, Winslow M (1997) A quantitative analysis of passive electrolocation behavior in electric fish. Brain Behav Evol 50(suppl 1):32–59PubMedGoogle Scholar
  56. Horseman BG, Gebhardt M, Honegger HW (1997) Involvement of the suboesophageal and thoracic ganglia in the control of antennal movements in crickets. J Comp Physiol A 181:195–204Google Scholar
  57. Hudson RD (1969) Infrared system engineering. Wiley-Interscience, New York, p 144Google Scholar
  58. Johnson GD, Rosenblatt RH (1988) Mechanisms of light organ occlusion in flashlight fishes, family Anomalopidae (Teleostei, Beryciformes), and the evolution of the group. Zool J Linn Soc 94:65–96Google Scholar
  59. Jones G (1999) Scaling of echolocation call parameters in bats. J Exp Biol 202:3359–3367PubMedGoogle Scholar
  60. Julian D, Crampton WGR, Wolhgemuth SE, Albert JS (2003) Oxygen consumption in weakly electric neotropical fishes. Oecologia 137:502–511PubMedGoogle Scholar
  61. Kalko EK (1995) Insect pursuit, prey capture and echolocation in pipistrelle bats (Microchiroptera). Anim Behav 50:861–880Google Scholar
  62. Knudsen EI (1974) Behavioral thresholds to electric signals in high frequency electric fish. J Comp Physiol A 91:333–353Google Scholar
  63. Knudsen EI (1975) Spatial aspects of the electric fields generated by weakly electric fish. J Comp Physiol A 99:103–118Google Scholar
  64. Krause AF, Dürr V (2004) Tactile efficiency of insect antennae with two hinge joints. Biol Cybern 91:168–181PubMedGoogle Scholar
  65. Lannoo MJ, Lannoo SJ (1993) Why do electric fishes swim backwards? An hypothesis based on gymnotiform foraging behavior interpreted through sensory constraints. Env Biol Fishes 36:157–165Google Scholar
  66. Lissmann HW (1958) On the function and evolution of electric organs in fish. J Exp Biol 35:156–191Google Scholar
  67. MacIver MA, Sharabash NM, Nelson ME (2001) Prey-capture behavior in gymnotid electric fish: motion analysis and effects of water conductivity. J Exp Biol 204:543–557PubMedGoogle Scholar
  68. MacIver MA, Fontaine E, Burdick JW (2004) Designing future underwater vehicles: principles and mechanisms of the weakly electric fish. IEEE J Oceanic Eng 29:651–659Google Scholar
  69. Madsen PT, Kerr I, Payne R (2004) Echolocation clicks of two free-ranging, oceanic delphinids with different food preferences: false killer whales Pseudorca crassidens and Risso’s dolphins Grampus griseus. J Exp Biol 207:1811–1823PubMedGoogle Scholar
  70. Madsen PT, Johnson M, de Soto NA, Zimmer WMX, Tyack P (2005) Biosonar performance of foraging beaked whales (Mesoplodon densirostris). J Exp Biol 208:181–194PubMedGoogle Scholar
  71. Mann DA, Lu ZM, Hastings MC, Popper AN (1998) Detection of ultrasonic tones and simulated dolphin echolocation clicks by a teleost fish, the American shad (Alosa sapidissima). J Acoust Soc Am 104:562–568PubMedGoogle Scholar
  72. McCosker JE (1977) Flashlight fishes. Sci Am 236(3):106–114PubMedCrossRefGoogle Scholar
  73. Metzner W (1999) Neural circuitry for communication and jamming avoidance in gymnotiform electric fish. J Exp Biol 202:1365–1375PubMedGoogle Scholar
  74. Metzner W, Zhang SY, Smotherman M (2002) Doppler-shift compensation behavior in horseshoe bats revisited: auditory feedback controls both a decrease and an increase in call frequency. J Exp Biol 205:1607–1616PubMedGoogle Scholar
  75. Miller LA, Surlykke A (2001) How some insects detect and avoid being eaten by bats: tactics and countertactics of prey and predator. Bioscience 51:570–581Google Scholar
  76. Moller P (1995) Electric fishes: history and behavior. Chapman & Hall, LondonGoogle Scholar
  77. Montgomery JC, Coombs S, Baker CF (2001) The mechanosensory lateral line system of the hypogean form of Astyanax fasciatus. Env Biol Fish 62:87–96Google Scholar
  78. Moortgat KT, Keller CH, Bullock TH, Sejnowski TJ (1998) Submicrosecond pacemaker precision is behaviorally modulated: the gymnotiform electromotor pathway. Proc Natl Acad Sci USA 95:4684–4689PubMedGoogle Scholar
  79. Munk O (1999) The escal photophore of ceratioids (Pisces; Ceratioidei): a review of structure and function. Acta Zool 80:265–284Google Scholar
  80. Norberg UML (2002) Structure, form, and function of flight in engineering and the living world. J Morphol 252:52–81Google Scholar
  81. Partridge JC, Douglas RH (1995) Far red sensitivity of dragon fish Aristostomias titmanni. Nature 375:21–22Google Scholar
  82. Portfors CV, Wenstrup JJ (1999) Delay-tuned neurons in the inferior colliculus of the mustached bat: implications for analyses of target distance. J Neurophysiol 82:1326–1338PubMedGoogle Scholar
  83. Post N, von der Emde G (1999) The ‘novelty response’ in an electric fish: response properties and habituation. Physiol Behav 68:115–128PubMedGoogle Scholar
  84. Rasnow B (1996) The effects of simple objects on the electric field of Apteronotus. J Comp Physiol A 178:397–411Google Scholar
  85. Ridoux V, Guinet C, Liret C, Creton P, Steenstrup R, Beauplet G (1997) A video sonar as a new tool to study marine mammals in the wild: measurements of dolphin swimming speed. Mar Mammal Sci 13:196–206Google Scholar
  86. Russell CJ, Myers JP, Bell CC (1974) The echo response in Gnathonemus petersii Mormyridae. J Comp Physiol A 92:181–200Google Scholar
  87. Schnitzler HU (1973) Control of Doppler shift compensation in the greater horseshoe bat, Rhinolophus ferrumequinum. J Comp Physiol A 82:79–92Google Scholar
  88. Schnitzler HU, Kalko EK (2001) Echolocation by insect-eating bats. Bioscience 51:557–569Google Scholar
  89. Schnitzler H, Moss CF, Denzinger A (2003) From spatial orientation to food acquisition in echolocating bats. Trends Ecol Evol 18:386–394Google Scholar
  90. Schotten M, Au WWL, Lammers MO, Aubauer R (2004) Echolocation recordings and localization of wild spinner dolphins (Stenella longirostris) and pantropical spotted dolphins (S. attenuata) using a four-hydrophone array. In: Thomas JA, Moss CF, Vater M (eds) Echolocation in bats and dolphins. University of Chicago Press, Chicago, pp 393–400Google Scholar
  91. Schuller G, Pollak G (1979) Disproportionate frequency representation in the inferior colliculus of Doppler-compensating greater horseshoe bats, Rhinolophus ferrumequinum. J Comp Physiol A 132:47–54Google Scholar
  92. Simmons JA, Moffat AJM, Masters WM (1992) Sonar gain control and echo detection thresholds in the echolocating bat, Eptesicus fuscus. J Acoust Soc Am 91:1150–1163PubMedGoogle Scholar
  93. Speakman JR, Racey PA (1991) No cost of echolocation for bats in flight. Nature 350:421–423PubMedGoogle Scholar
  94. Stoddard PK (1999) Predation enhances complexity in the evolution of electric fish signals. Nature 400:254–256PubMedGoogle Scholar
  95. Stoddard PK (2002) Electric signals: predation, sex, and environmental constraints. Adv Stud Behav 31:201–242CrossRefGoogle Scholar
  96. Surlykke A, Moss CF (2000) Echolocation behavior of the big brown bat, Eptesicus fuscus, in the field and the laboratory. J Acoust Soc Am 108:2419–2429PubMedGoogle Scholar
  97. 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 163:53–61PubMedGoogle Scholar
  98. Tian B, Schnitzler HU (1997) Echolocation signals of the greater horseshoe bat (Rhinolophus ferrumequinum) in transfer flight and during landing. J Acoust Soc Am 101:2347–2364PubMedGoogle Scholar
  99. Thomas JA, Moss CF, Vater M (2004) Echolocation in bats and dolphins. University of Chicago Press, ChicagoGoogle Scholar
  100. Toerring MJ, Moller P (1984) Locomotor and electric displays associated with electrolocation during exploratory behavior in mormyrid fish. Behav Brain Res 12:291–306PubMedGoogle Scholar
  101. Trappe M, Schnitzler HU (1982) Doppler-shift compensation in insect-catching horseshoe bats. Naturwissenschaften 69:193–196Google Scholar
  102. Ulanovsky N, Fenton MB, Tsoar A, Korine C (2004) Dynamics of jamming avoidance in echolocating bats. Proc R Soc Lond B 271:1467–1475Google Scholar
  103. Wanzenbock J, Scheimer F (1989) Prey detection in cyprinids during early development. Can J Fish Aquat Sci 46:995–1001Google Scholar
  104. Weihs D (2004) The hydrodynamics of dolphin drafting. J Biol 3:801–816Google Scholar
  105. Weissert R, von Campenhausen C (1981) Discrimination between stationary objects by the blind cave fish Anoptichthys jordani (Characidae). J Comp Physiol A 143:375–381Google Scholar
  106. Wenstrup JJ (1999) Frequency organization and responses to complex sounds in the medial geniculate body of the mustached bat. J Neurophysiol 82:2528–2544PubMedGoogle Scholar
  107. Westby GWM (1988) The ecology, discharge diversity and predatory behavior of gymnotiform electric fish in the coastal streams of French Guiana. Behav Ecol Soc 22:341–354Google Scholar
  108. Widder EA, Latz MF, Herring PJ, Case JF (1984) Far-red bioluminescence from two deep-sea fishes. Science 225:512–514PubMedGoogle Scholar
  109. Wotton JM, Jenison RL, Hartley DJ (1997) The combination of echolocation emission and ear reception enhances directional spectral cues of the big brown bat, Eptesicus fuscus. J Acoust Soc Am 101:1723–1733PubMedGoogle Scholar
  110. Xitco MJ, Roitblat HL (1996) Object recognition through eavesdropping: passive echolocation in bottlenose dolphins. Anim Learn Behav 24:355–365Google Scholar
  111. Zakon HH (1987) Hormone-mediated plasticity in the electrosensory system of weakly electric fish. Trends Neurosci 10:416–421Google Scholar

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© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of Molecular and Integrative Physiology and The Beckman Institute for Advanced Science and TechnologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  2. 2.Department of Mechanical Engineering and Department of Biomedical EngineeringNorthwestern UniversityEvanstonUSA

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