Literature DB >> 29367237

The complexity of high-frequency electric fields degrades electrosensory inputs: implications for the jamming avoidance response in weakly electric fish.

Aaron R Shifman1,2,3, John E Lewis4,2,3.   

Abstract

Sensory systems encode environmental information that is necessary for adaptive behavioural choices, and thus greatly influence the evolution of animal behaviour and the underlying neural circuits. Here, we evaluate how the quality of sensory information impacts the jamming avoidance response (JAR) in weakly electric fish. To sense their environment, these fish generate an oscillating electric field: the electric organ discharge (EOD). Nearby fish with similar EOD frequencies perform the JAR to increase the difference between their EOD frequencies, i.e. their difference frequency (DF). The fish determines the sign of the DF: when it has a lower frequency (DF > 0), EOD frequency is decreased and vice versa. We study the sensory basis of the JAR in two species: Apteronotus leptorhynchus have a high frequency (ca 1000 Hz), spatio-temporally heterogeneous electric field, whereas Eigenmannia sp. have a low frequency (ca 300 Hz), spatially uniform field. We show that the increased complexity of the Apteronotus field decreases the reliability of sensory cues used to determine the DF. Interestingly, Apteronotus responds to all JAR stimuli by increasing EOD frequency, having lost the neural pathway that produces JAR-related decreases in EOD frequency. Our results suggest that electric field complexity may have influenced the evolution of the JAR by degrading the related sensory information.
© 2018 The Author(s).

Entities:  

Keywords:  Apteronotus; Eigenmannia; amplitude modulation; electrocommunication; signal interference

Mesh:

Year:  2018        PMID: 29367237      PMCID: PMC5805966          DOI: 10.1098/rsif.2017.0633

Source DB:  PubMed          Journal:  J R Soc Interface        ISSN: 1742-5662            Impact factor:   4.118


  36 in total

1.  Model-based total evidence phylogeny of Neotropical electric knifefishes (Teleostei, Gymnotiformes).

Authors:  Victor A Tagliacollo; Maxwell J Bernt; Jack M Craig; Claudio Oliveira; James S Albert
Journal:  Mol Phylogenet Evol       Date:  2015-11-23       Impact factor: 4.286

2.  Ambiguous encoding of stimuli by primary sensory afferents causes a lack of independence in the perception of multiple stimulus attributes.

Authors:  Bruce A Carlson; Masashi Kawasaki
Journal:  J Neurosci       Date:  2006-09-06       Impact factor: 6.167

3.  Phylogenetic comparative analysis of electric communication signals in ghost knifefishes (Gymnotiformes: Apteronotidae).

Authors:  Cameron R Turner; Maksymilian Derylo; C David de Santana; José A Alves-Gomes; G Troy Smith
Journal:  J Exp Biol       Date:  2007-12       Impact factor: 3.312

Review 4.  The energetics of electric organ discharge generation in gymnotiform weakly electric fish.

Authors:  Vielka L Salazar; Rüdiger Krahe; John E Lewis
Journal:  J Exp Biol       Date:  2013-07-01       Impact factor: 3.312

5.  Signal Cloaking by Electric Fish.

Authors:  Philip K Stoddard; Michael R Markham
Journal:  Bioscience       Date:  2008       Impact factor: 8.589

6.  Evolution of electric communication signals in the South American ghost knifefishes (Gymnotiformes: Apteronotidae): A phylogenetic comparative study using a sequence-based phylogeny.

Authors:  Adam R Smith; Melissa R Proffitt; Winnie W Ho; Claire B Mullaney; Javier A Maldonado-Ocampo; Nathan R Lovejoy; José A Alves-Gomes; G Troy Smith
Journal:  J Physiol Paris       Date:  2016-10-18

7.  Phase and amplitude computations in the midbrain of an electric fish: intracellular studies of neurons participating in the jamming avoidance response of Eigenmannia.

Authors:  W Heiligenberg; G Rose
Journal:  J Neurosci       Date:  1985-02       Impact factor: 6.167

8.  Phylogenetic analysis of the South American electric fishes (order Gymnotiformes) and the evolution of their electrogenic system: a synthesis based on morphology, electrophysiology, and mitochondrial sequence data.

Authors:  J A Alves-Gomes; G Ortí; M Haygood; W Heiligenberg; A Meyer
Journal:  Mol Biol Evol       Date:  1995-03       Impact factor: 16.240

9.  Sex differences in the electrocommunication signals of the electric fish Apteronotus bonapartii.

Authors:  Winnie W Ho; Cristina Cox Fernandes; José A Alves-Gomes; G Troy Smith
Journal:  Ethology       Date:  2010-11       Impact factor: 1.897

10.  Beyond the Jamming Avoidance Response: weakly electric fish respond to the envelope of social electrosensory signals.

Authors:  Sarah A Stamper; Manu S Madhav; Noah J Cowan; Eric S Fortune
Journal:  J Exp Biol       Date:  2012-12-01       Impact factor: 3.312

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  5 in total

1.  Chirping and asymmetric jamming avoidance responses in the electric fish Distocyclus conirostris.

Authors:  Jacquelyn M Petzold; José A Alves-Gomes; G Troy Smith
Journal:  J Exp Biol       Date:  2018-09-10       Impact factor: 3.312

2.  Modeling the Sequential Pattern Variability of the Electromotor Command System of Pulse Electric Fish.

Authors:  Angel Lareo; Pablo Varona; Francisco B Rodriguez
Journal:  Front Neuroinform       Date:  2022-06-28       Impact factor: 3.739

3.  A model for studying the energetics of sustained high frequency firing.

Authors:  Bela Joos; Michael R Markham; John E Lewis; Catherine E Morris
Journal:  PLoS One       Date:  2018-04-30       Impact factor: 3.240

4.  Electrosensory Contrast Signals for Interacting Weakly Electric Fish.

Authors:  Na Yu; Ginette Hupe; André Longtin; John E Lewis
Journal:  Front Integr Neurosci       Date:  2019-07-31

5.  Dynamics of a neuronal pacemaker in the weakly electric fish Apteronotus.

Authors:  Aaron R Shifman; Yiren Sun; Chloé M Benoit; John E Lewis
Journal:  Sci Rep       Date:  2020-10-07       Impact factor: 4.379

  5 in total

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