Envelope Coding and Processing: Implications for Perception and Behavior

  • Michael G. MetzenEmail author
  • Maurice J. Chacron
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 70)


How envelopes are processed in the electrosensory system and how this gives rise to behavioral responses has been the focus of extensive research. This chapter provides a comprehensive review on the mechanisms the brain exploits at different stages of sensory processing to extract meaningful information about these stimulus attributes and how this mediates behavioral responses. After a brief review of the relevant anatomy and circuitry, the natural statistics of envelopes in the electrosensory system are discussed in detail. This is followed by a review of the current state of knowledge as to the cellular and network mechanisms that give rise to envelope responses in the electrosensory system. In particular, it is highlighted how electrosensory neurons can optimally encode envelopes by matching their tuning properties to natural statistics. There is an emphasis throughout the chapter on the important parallels with the mammalian auditory and other systems, along with interesting future avenues of research.


Envelope Information theory Neural coding Neuromodulation Parallel processing Second-order statistics Sensory processing Wave type Weakly electric fish 


Compliance with Ethics Requirements

Michael G. Metzen declares that he has no conflict of interest.

Maurice J. Chacron declares that he has no conflict of interest.


  1. Baker CL Jr (1999) Central neural mechanisms for detecting second-order motion. Curr Opin Neurobiol 9(4):461–466. Scholar
  2. Baker CL Jr, Mareschal I (2001) Processing of second-order stimuli in the visual cortex. Prog Brain Res 134:171–191CrossRefGoogle Scholar
  3. Bastian J, Nguyenkim J (2001) Dendritic modulation of burst-like firing in sensory neurons. J Neurophysiol 85(1):10–22CrossRefGoogle Scholar
  4. Bastian J, Courtright J, Crawford J (1993) Commissural neurons of the electrosensory lateral line lobe of Apteronotus leptorhynchus: morphological and physiological characteristics. J Comp Physiol A 173(3):257–274CrossRefGoogle Scholar
  5. Berman NJ, Maler L (1999) Neural architecture of the electrosensory lateral line lobe: adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering. J Exp Biol 202(10):1243–1253PubMedGoogle Scholar
  6. Bullock T, Hamstra R, Scheich H (1972) The jamming avoidance response of high frequency electric fish. J Comp Physiol A 77(1):1–22CrossRefGoogle Scholar
  7. Carr CE (2004) Timing is everything: organization of timing circuits in auditory and electrical sensory systems. J Comp Neurol 472(2):131–133. Scholar
  8. Carr CE, Maler L (1985) A Golgi study of the cell types of the dorsal torus semicircularis of the electric fish Eigenmannia: functional and morphological diversity in the midbrain. J Comp Neurol 235(2):207–240CrossRefGoogle Scholar
  9. Carr CE, Maler L, Heiligenberg W, Sas E (1981) Laminar organization of the afferent and efferent systems of the torus semicircularis of Gymnotiform fish: morphological substrates for parallel processing in the electrosensory system. J Comp Neurol 203(4):649–670CrossRefGoogle Scholar
  10. Chacron MJ, Maler L, Bastian J (2005) Electroreceptor neuron dynamics shape information transmission. Nat Neurosci 8:673–678CrossRefGoogle Scholar
  11. Clarke SE, Longtin A, Maler L (2015) Contrast coding in the electrosensory system: parallels with visual computation. Net Rev Neurosci 16(12):733–744. Scholar
  12. Crawford JD (1992) Comparative analysis of electrosensory and auditory function in a mormyrid fish. In: Webster DB, Popper AN, Fay RR (eds) The evolutionary biology of hearing. Springer New York, New York, pp 457–457CrossRefGoogle Scholar
  13. Duncan JS, Fritzsch B (2012) Evolution of sound and balance perception: innovations that aggregate single hair cells into the ear and transform a gravistatic sensor into the organ of corti. Anat Rec (Hoboken) 295(11):1760–1774. Scholar
  14. Ellis LD, Mehaffey WH, Harvey-Girard E, Turner RW, Maler L, Dunn RJ (2007) SK channels provide a novel mechanism for the control of frequency tuning in electrosensory neurons. J Neurosci 27(35):9491–9502. Scholar
  15. Ellis LD, Maler L, Dunn RJ (2008) Differential distribution of SK channel subtypes in the brain of the weakly electric fish Apteronotus leptorhynchus. J Comp Neurol 507(6):1964–1978. Scholar
  16. Fee MS, Mitra PP, Kleinfeld D (1997) Central versus peripheral determinants of patterned spike activity in rat vibrissa cortex during whisking. J Neurophysiol 78(2):1144–1149CrossRefGoogle Scholar
  17. Fotowat H, Harrison RR, Krahe R (2013) Statistics of the electrosensory input in the freely swimming weakly electric fish Apteronotus leptorhynchus. J Neurosci 33(34):13758–13772. Scholar
  18. Gussin D, Benda J, Maler L (2007) Limits of linear rate coding of dynamic stimuli by electroreceptor afferents. J Neurophysiol 97(4):2917–2929. Scholar
  19. Heil P (2003) Coding of temporal onset envelope in the auditory system. Sp Comm 41:123–134CrossRefGoogle Scholar
  20. Heiligenberg W (1991) Neural nets in electric fish. MIT Press, Cambridge MAGoogle Scholar
  21. Hewitt MJ, Meddis R (1994) A computer model of amplitude-modulation sensitivity of single units in the inferior colliculus. J Acoust Soc Am 95(4):2145–2159CrossRefGoogle Scholar
  22. Huang CG, Chacron MJ (2016) Optimized parallel coding of second-order stimulus features by heterogeneous neural populations. J Neurosci 36(38):9859–9872. Scholar
  23. Huang CG, Chacron MJ (2017) SK channel subtypes enable parallel optimized coding of behaviorally relevant stimulus attributes: a review. Channels (Austin) 11(4):281–304. Scholar
  24. 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. Scholar
  25. Huang CG, Metzen MG, Chacron MJ (2018) Feedback optimizes neural coding and perception of natural stimuli. eLife 7:e38935.
  26. Hudspeth AJ (2014) Integrating the active process of hair cells with cochlear function. Nat Rev Neurosci 15(9):600–614. Scholar
  27. Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84(2):541–577. Scholar
  28. Krahe R, Maler L (2014) Neural maps in the electrosensory system of weakly electric fish. Curr Opin Neurobiol 24:13–21. Scholar
  29. Lewicki MS (2002) Efficient coding of natural sounds. Nat Neurosci 5(4):356–363. Scholar
  30. Longtin A, Middleton JW, Cieniak J, Maler L (2008) Neural dynamics of envelope coding. Math Biosci 214(1–2):87–99. Scholar
  31. Maler L (2009) Receptive field organization across multiple electrosensory maps. I. Columnar organization and estimation of receptive field size. J Comp Neurol 516(5):376–393. Scholar
  32. Mante V, Frazor RA, Bonin V, Geisler WS, Carandini M (2005) Independence of luminance and contrast in natural scenes and in the early visual system. Nat Neurosci 8(12):1690–1697. Scholar
  33. Marsat G, Longtin A, Maler L (2012) Cellular and circuit properties supporting different sensory coding strategies in electric fish and other systems. Curr Opin Neurobiol 22(4):686–692. Scholar
  34. Martinez D, Metzen MG, Chacron MJ (2016) Electrosensory processing in Apteronotus albifrons: implications for general and specific neural coding strategies across wave-type weakly electric fish species. J Neurophysiol 116(6):2909–2921. Scholar
  35. Massot C, Schneider AD, Chacron MJ, Cullen KE (2012) The vestibular system implements a linear-nonlinear transformation in order to encode self-motion. PLoS Biol 10(7):e1001365. Scholar
  36. McGillivray P, Vonderschen K, Fortune ES, Chacron MJ (2012) Parallel coding of first and second order stimulus attributes by midbrain electrosensory neurons. J Neurosci 32:5510–5524. Scholar
  37. Metzen MG, Chacron MJ (2014) Weakly electric fish display behavioral responses to envelopes naturally occurring during movement: implications for neural processing. J Exp Biol 217(8):1381–1391. Scholar
  38. Metzen MG, Chacron MJ (2015) Neural heterogeneities determine response characteristics to second-, but not first-order stimulus features. J Neurosci 35(7):3124–3138. Scholar
  39. Metzen MG, Chacron MJ (2017) Stimulus background influences phase invariant coding by correlated neural activity. eLife 6:e24482. Scholar
  40. Metzen MG, Jamali M, Carriot J et al (2015) Coding of envelopes by correlated but not single-neuron activity requires neural variability. Proc Natl Acad Sci U S A 112(15):4791–4796. Scholar
  41. Metzen MG, Hofmann V, Chacron MJ (2016) Neural correlations enable invariant coding and perception of natural stimuli in weakly electric fish. eLife 5:e12993. Scholar
  42. Metzen MG, Huang CG, Chacron MJ (2018) Descending pathways generate perception of and neural responses to weak sensory input. PLoS Biol 16(6):e2005239. Scholar
  43. Metzner W (1993) The jamming avoidance response in Eigenmannia is controlled by two separate motor pathways. J Neurosci 13(5):1862–1878CrossRefGoogle Scholar
  44. Middleton JW, Longtin A, Benda J, Maler L (2006) The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope. Proc Natl Acad Sci U S A 103(39):14596–14601CrossRefGoogle Scholar
  45. Middleton JW, Longtin A, Benda J, Maler L (2009) Postsynaptic receptive field size and spike threshold determine encoding of high-frequency information via sensitivity to synchronous presynaptic activity. J Neurophysiol 101(3):1160–1170. Scholar
  46. Modrell MS, Lyne M, Carr AR et al (2017) Insights into electrosensory organ development, physiology and evolution from a lateral line-enriched transcriptome. eLife 6:e24197. Scholar
  47. Olshausen BA, Field DJ (2004) Sparse coding of sensory inputs. Curr Opin Neurobiol 14(4):481–487. Scholar
  48. Partridge BL, Heiligenberg W, Matsubara J (1981) The neural basis of a sensory filter in the jamming avoidance response: no grandmother cells in sight. J Comp Physiol A 145:153–168CrossRefGoogle Scholar
  49. Rieke F, Warland D, de Ruyter van Steveninck RR, Bialek W (1996) Spikes: exploring the neural code. MIT Press, Cambridge MAGoogle Scholar
  50. Rose GJ, Call SJ (1993) Temporal filtering properties of midbrain neurons in an electric fish: implications for the function of dendritic spines. J Neurosci 13(3):1178–1189CrossRefGoogle Scholar
  51. Savard M, Krahe R, Chacron MJ (2011) Neural heterogeneities influence envelope and temporal coding at the sensory periphery. Neuroscience 172:270–284CrossRefGoogle Scholar
  52. Scheich H, Bullock TH, Hamstra RH (1973) Coding properties of two classes of afferent nerve fibers: high frequency electroreceptors in the electric fish, Eigenmania. J Neurophysiol 36:39–60CrossRefGoogle Scholar
  53. Simoncelli EP, Olshausen BA (2001) Natural image statistics and neural representation. Annu Rev Neurosci 24:1193–1216. Scholar
  54. Smith ZM, Delgutte B, Oxenham AJ (2002) Chimaeric sounds reveal dichotomies in auditory perception. Nature 416(6876):87–90. Scholar
  55. Sproule MK, Metzen MG, Chacron MJ (2015) Parallel sparse and dense information coding streams in the electrosensory midbrain. Neurosci Lett 607:1–6. Scholar
  56. Stamper SA, Carrera-G E, Tan EW et al (2010) Species differences in group size and electrosensory interference in weakly electric fishes: implications for electrosensory processing. Behav Brain Res 207(2):368–376CrossRefGoogle Scholar
  57. 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(23):4196–4207. Scholar
  58. Stamper SA, Fortune ES, Chacron MJ (2013) Perception and coding of envelopes in weakly electric fishes. J Exp Biols 216(Pt 13):2393–2402. Scholar
  59. Theunissen FE, Elie JE (2014) Neural processing of natural sounds. Nat Rev Neurosci 15(6):355–366. Scholar
  60. Thomas RA, Metzen MG, Chacron MJ (2018) Weakly electric fish distinguish between envelope stimuli arising from different behavioral contexts. J Exp Biol 221(Pt 15):jeb178244. Scholar
  61. Vonderschen K, Chacron MJ (2011) Sparse and dense coding of natural stimuli by distinct midbrain neuron subpopulations in weakly electric fish. J Neurophysiol 106(6):3102–3118. Scholar
  62. Wang X, Sachs MB (1995) Transformation of temporal discharge patterns in a ventral cochlear nucleus stellate cell model: implications for physiological mechanisms. J Neurophysiol 73(4):1600–1616. Scholar
  63. Wark B, Lundstrom BN, Fairhall A (2007) Sensory adaptation. Curr Opin Neurobiol 17(4):423–429. Scholar
  64. Watanabe A, Takeda K (1963) The change of discharge frequency by AC stimulus in a weak electric fish. J Exp Biol 40(1):57–66Google Scholar
  65. Yu N, Hupe G, Garfinkle C, Lewis JE, Longtin A (2012) Coding conspecific identity and motion in the electric sense. PLoS Comput Biol 8(7):e1002564. Scholar
  66. Zeng FG, Nie K, Stickney GS et al (2005) Speech recognition with amplitude and frequency modulations. Proc Natl Acad Sci U S A 102(7):2293–2298. Scholar
  67. Zhang ZD, Chacron MJ (2016) Adaptation to second order stimulus features by electrosensory neurons causes ambiguity. Sci Rep 6:28716. Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of PhysiologyMcGill UniversityMontrealCanada

Personalised recommendations