Abstract
The jamming avoidance response (JAR) of the weakly electric fish Eigenmannia is characterized by upward or downward shifts in electric organ discharge (EOD) frequency that are elicited by particular combinations of sinusoidal amplitude modulation (AM) and differential phase modulation (DPM). However, non-jamming stimuli that consist of AM and/or DPM can elicit similar shifts in EOD frequency. We tested the hypothesis that these behavioral responses result from non-jamming stimuli being misperceived as jamming stimuli. Responses to non-jamming stimuli were similar to JARs as measured by modulation rate tuning, sensitivity, and temporal dynamics. There was a smooth transition between the magnitude of JARs and responses to stimuli with variable depths of AM or DPM, suggesting that frequency shifts in response to jamming and non-jamming stimuli represent different points along a continuum rather than categorically distinct behaviors. We also tested the hypothesis that non-jamming stimuli can elicit frequency shifts in natural contexts. Frequency decreases could be elicited by semi-natural AM stimuli, such as random AM, AM presented to a localized portion of the body surface, transient changes in amplitude, and movement of resistive objects through the electric field. We conclude that ‘phantom’ jamming stimuli can induce EOD frequency shifts in natural situations.
Similar content being viewed by others
Abbreviations
- AM:
-
Amplitude modulation
- Df:
-
Difference in frequency
- DPM:
-
Differential phase modulation
- EOD:
-
Electric organ discharge
- JAR:
-
Jamming avoidance response
- PM:
-
Phase modulation
References
Bastian J, Chacron MJ, Maler L (2002) Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J Neurosci 22:4577–4590
Bastian J, Yuthas J (1984) The jamming avoidance response of Eigenmannia: properties of a diencephalic link between sensory processing and motor output. J Comp Physiol A 154:895–908
Bullock TH, Hamstra RH, Scheich H (1972a) The jamming avoidance response of high frequency electric fish. I. General features. J Comp Physiol 77:1–22
Bullock TH, Scheich H, Hamstra RH (1972b) The jamming avoidance response of high frequency electric fish. II. Quantitative aspects. J Comp Physiol 77:23–48
Carlson BA (2006) A neuroethology of electrocommunication: senders, receivers, and everything in between. In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Fish communication. Science Publishers, Enfield, NH, pp 805–848
Carlson BA, Kawasaki M (2006) Ambiguous encoding of stimuli by primary sensory afferents causes a lack of independence in the perception of multiple stimulus attributes. J Neurosci 26:9173–9183
Carr CE, Heiligenberg W, Rose GJ (1986a) A time-comparison circuit in the electric fish Eigenmannia midbrain I. Behavior and physiology. J Neurosci 6:107–119
Carr CE, Maler L, Taylor B (1986b) A time-comparison circuit in the electric fish Eigenmannia midbrain II. Functional morphology. J Neurosci 6:1372–1383
Chacron M (2007) Electrolocation. Scholarpedia, p 6776
Chacron M, Doiron B, Maler L, Longtin A, Bastian J (2003) Non-classical receptive field mediates switch in a sensory neuron’s frequency tuning. Nature 423:77–81
Crampton W (1998) Electric signal design and habitat preferences in a species rich assemblage of gymnotiform fishes from the upper Amazon basin. An Acad Bras Cienc 70:805–847
Ehret G (1987) Categorical perception of sound signals: facts and hypotheses from animal studies. In: Harnad S (eds) Categorical perception: the groundwork of cognition. Cambridge University Press, New York, pp 301–331
Hagedorn M, Heiligenberg W (1985) Court and spark: electric signals in the courtship and mating of gymnotoid fish. Anim Behav 33:254–265
Heiligenberg W (1973) Electrolocation of objects in the electric fish Eigenmannia (Rhamphichthyidae, Gymnotoidei). J Comp Physiol 87:137–164
Heiligenberg W (1991) Neural nets in electric fish. MIT, Cambridge
Heiligenberg W, Baker C, Matsubara J (1978) The jamming avoidance response in Eigenmannia revisited: the structure of a neuronal democracy. J Comp Physiol 127:267–286
Heiligenberg W, Bastian J (1980) The control of Eigenmannia’s pacemaker by distributed evaluation of electroreceptive afferences. J Comp Physiol 136:113–133
Heiligenberg W, Partridge BL (1981) How electroreceptors encode JAR-eliciting stimulus regimes: reading trajectories in a phase-amplitude plane. J Comp Physiol 142:295–308
Heiligenberg WF, Rose G (1985) Phase and amplitude computations in the midbrain of an electric fish: intracellular studies of neurons participating in the jamming avoidance response of Eigenmannia. J Neurosci 5:515–531
Hopkins C (1972) Sex differences in electric signaling in an electric fish. Science 176:1035–1037
Hopkins C (1974) Electric communication: functions in the social behavior of Eigenmannia virescens. Behaviour 50:270–305
Hopkins CD (1976) Stimulus filtering and electroreception: tuberous electroreceptors in three species of gymnotoid fish. J Comp Physiol 111:171–207
Hopkins CD (1999) Design features for electric communication. J Exp Biol 202:1217–1228
Kawasaki M (1997) Sensory hyperacuity in the jamming avoidance response of weakly electric fish. Curr Opin Neurobiol 7:473–479
Kramer B (1987) The sexually dimorphic jamming avoidance response in the electric fish Eigenmannia (Teleostei, Gymnotiformes). J Exp Biol 130:39–62
Kramer B (1999) Waveform discrimination, phase sensitivity and jamming avoidance in a wave-type electric fish. J Exp Biol 202:1387–1398
Nelson ME, MacIver MA (1999) Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. J Exp Biol 202:1195–1203
Nelson ME, MacIver MA, Coombs S (2002) Modeling electrosensory and mechanosensory images during the predatory behavior of weakly electric fish. Brain Behav Evol 59:199–210
Ramcharitar J, Tan E, Fortune E (2005) Effects of global electrosensory signals on motion processing in the midbrain of Eigenmannia. J Comp Physiol A 191:865–872
Rose G, Heiligenberg W (1985) Temporal hyperacuity in the electric sense of fish. Nature 318:178–180
Rose GJ, Heiligenberg W (1986) Neural coding of difference frequencies in the midbrain of the electric fish Eigenmannia: reading the sense of rotation in an amplitude-phase plane. J Comp Physiol A 158:613–624
Rose GJ, Keller C, Heiligenberg W (1987) ‘Ancestral’ neural mechanisms of electrolocation suggest a substrate for the evolution of the jamming avoidance response. J Comp Physiol A 160:491–500
Scheich H, Bullock TH, Hamstra RH (1973) Coding properties of two classes of afferent nerve fibers: high frequency electroreceptors in the electric fish, Eigenmannia. J Neurophysiol 36:39–60
Scheich J, Bullock TH (1974) The detection of fields from electric organs. In: Fessard A (ed) Handbook of sensory physiology. Springer, New York, pp 201–256
Takizawa Y, Rose GJ, Kawasaki M (1999) Resolving competing theories for control of the jamming avoidance response: the role of amplitude modulations in electric organ discharge decelerations. J Exp Biol 202:1377–1386
von der Emde G (1998) Capacitance detection in the wave-type electric fish Eigenmannia during active electrolocation. J Comp Physiol A 182:217–224
von der Emde G (1999) Active electrolocation of objects in weakly electric fish. J Exp Biol 202:1205–1215
von der Emde G, Ringer T (1992) Electrolocation of capacitive objects in four species of pulse-type weakly electric fish. I. Discrimination performance. Ethology 91:326–338
Watanabe A, Takeda K (1963) The change of discharge frequency by A.C. stimulus in a weakly electric fish. J Exp Biol 40:57–66
Wyttenbach RA, Hoy RR (1999) Categorical perception of behaviorally-relevant stimuli by crickets. In: Hauser MD, Konishi M (eds) The design of animal communication. MIT, Cambridge, MA, pp 559–576
Zakon HH (1986) The electroreceptive periphery. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 103–156
Acknowledgments
This work was supported by grants from the National Institute of Neurological Disorders and Stroke (F32 NS049788 to B.A.C.) and the National Science Foundation (IBN-0235533 to M.K.). These experiments comply with the “Principles of animal care,” publication No. 86-23, revised 1985 of the National Institutes of Health, and were approved by the University of Virginia Institutional Animal Care and Use Committee.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Carlson, B.A., Kawasaki, M. Behavioral responses to jamming and ‘phantom’ jamming stimuli in the weakly electric fish Eigenmannia . J Comp Physiol A 193, 927–941 (2007). https://doi.org/10.1007/s00359-007-0246-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-007-0246-6