Sex recognition and neuronal coding of electric organ discharge waveform in the pulse-type weakly electric fish,Hypopomus occidentalis
- 47 Downloads
Hypopomus occidentalis, a weakly electric gymnotiform fish with a pulse-type discharge, has a sexually dimorphic electric organ discharge (Hagedorn 1983). The electric organ discharges (EODs) of males in the breeding season are longer in duration and have a lower peak-power frequency than the EODs of females. We tested reproductively mature fish in the field by presenting electronically generated stimuli in which the only cue for sex recognition was the waveshape of individual EOD-like pulses in a train. We found that gravid females could readily discriminate male-like from female-like EOD waveshapes, and we conclude that this feature of the electric signal is sufficient for sex recognition.
To understand the possible neural bases for discrimination of male and female EODs byH. occidentalis, we conducted a neurophysiological examination of both peripheral and central neurons. Our studies show that there are sets of neurons in this species which can discriminate male or female EODs by coding either temporal or spectral features of the EOD.
Temporal encoding of stimulus duration was observed in evoked field potential recordings from the magnocellular nucleus of the midbrain torus semicircularis. This nucleus indirectly receives pulse marker electroreceptor information. The field potentials suggest that comparison is possible between pulse marker activity on opposite sides of the body.
From standard frequency-threshold curves, spectral encoding of stimulus peak-power frequency was measured in burst duration coder electroreceptor afferents. In both male and female fish, the best frequencies of the narrow-band population of electroreceptors were lower than the peak-power frequency of the EOD. Based on this observation, and the presence of a population of wide-band receptors which can serve as a frequency-independent amplitude reference, a slope-detection model of frequency discrimination is advanced.
Spectral discrimination of EOD peak-power frequency was also shown to be possible in a more natural situation similar to that present during behavioral discrimination. As the fish's EOD mimic slowly scanned through and temporally coincided with the neighbor's EOD mimic, peak spike rate in burst duration coder afferents was measured. Spike rate at the moment of coincidence changed predictably as a function of the neighbor's EOD peak-power frequency.
Single-unit threshold measurements were made on afferents from peripheral burst duration coder receptors in the amplitude-coding pathway, and midbrain giant cells in the time-coding pathway. The amplitude-coding pathway was more sensitive to a transverse signal mimicking the EOD of a neighbor than the time-coding pathway, despite, in the latter case, increased convergence at the midbrain level.
Measurements of the sensitivity and spectral tuning characteristics of afferents from burst duration coder electroreceptors show that elements of the amplitude-coding pathway, when considered on a population level, are capable of encoding EOD peak-power frequencies to the extent necessary to account for our behavioral observations. We conclude thatH. occidentalis has the capability to discriminate male from female EOD pulse shape using both temporal and spectral cues, but that frequency discrimination based on spectral tuning of electroreceptors is the most likely neuronal mechanism.
KeywordsSpike Rate Electric Organ Discharge Frequency Discrimination Spectral Tuning Weakly Electric Fish
electric organ discharge
Unable to display preview. Download preview PDF.
- Baker CL (1980) Jamming avoidance behavior in gymnotoid electric fish with pulse-type discharges: sensory encoding for a temporal pattern discrimination. J Comp Physiol 136:165–181Google Scholar
- Bass AH (1986) A hormone-sensitive communication system in an electric fish. J Neurobiol 17:131–156Google Scholar
- Bastian J (1976) Frequency response characteristics of electroreceptors in weakly electric fish (Gymnotoidei) with a pulse discharge. J Comp Physiol 112:165–180Google Scholar
- Bastian J (1977) Variations in the frequency response of electroreceptors dependent on receptor location in weakly electric fish (Gymnotoidei) with a pulse discharge. J Comp Physiol 121:53–64Google Scholar
- Bell CC, Szabo T (1986) Electroreception in mormyrid fish: central anatomy. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 375–422Google Scholar
- Bennett MVL (1971) Electric organs. In: Hoar WS, Randall DJ (eds) Fish physiology vol 5. Academic Press, New York, pp 347–391Google Scholar
- Bullock TH (1968) Representation of information in neurons and sites for molecular participation. Proc Natl Acad Sci (Wash) 60:1058–1068Google Scholar
- Bullock TH (1969) Species differences in effect of electroreceptor input in electric organ pacemakers and other aspects of behavior in electric fish. Brain Behav Evol 2:85–118Google Scholar
- Carr CE, Heiligenberg W, Rose GJ (1986) The detection of small temporal disparities in the weakly electric fish,Eigenmannia. J Neurosci 6:107–119Google Scholar
- Carr CE, Maler L (1986) Electroreception in gymnotiform fish. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 319–375Google Scholar
- Fay RR, Ream TJ (1986) Acoustic response and tuning in saccular nerve fibers of the goldfish (Carassius auratus). J Acoust Soc Am 79:1883–1895Google Scholar
- Fay RR, Popper AN (1980) Structure and function in teleost auditory systems. In: Popper AN, Fay RR (eds) Comparative studies of hearing in vertebrates. Springer, Berlin Heidelberg New York, pp 3–42Google Scholar
- Hagedorn M (1983) Social signals in electric fish. PhD dissertation, University of California, San DiegoGoogle Scholar
- Hagedorn M (1986) The ecology, courtship, and mating of gymnotiform electric fish. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 497–525Google Scholar
- Hagedorn M (1988) Ecology and behavior of a pulse type electric fish,Hypopomus occidentalis (Gymnotiformes, Hypopomidae), in a fresh water stream in Panama. Copeia 1988:324–335Google Scholar
- Hagedorn M, Carr CE (1985) Single electrocytes produce a sexually dimorphic signal in South American electric fish,Hypopomus occidentalis (Gymnotiformes, Hypopomidae). J Comp Physiol A 156:511–523Google Scholar
- Hagiwara S, Morita H (1963) Coding mechanisms of electroreceptor fibers in some electric fish. J Neurophysiol 26:551–567Google Scholar
- Hagiwara S, Kusano K, Negishi K (1962) Physiological properties of electroreceptors of some gymnotids. J Neurophysiol 28:784–799Google Scholar
- Heiligenberg W (1974) Electrolocation and jamming avoidance in aHypopygus (Rhamphichthyidae, Gymnotoidei), an electric fish with pulse-type discharges. J Comp Physiol 91:223–240Google Scholar
- Heiligenberg W (1977) Principles of electrolocation and jamming avoidance in electric fish. In: Braitenberg V (ed) Studies of brain function, vol 1. Springer, Berlin Heidelberg New York, p 7Google Scholar
- Heiligenberg W, Altes RA (1978) Phase sensitivity in electroreception. Science 199:1001–1003Google Scholar
- 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 124:211–224Google Scholar
- Hopkins CD (1972) Sex differences in electric signalling in an electric fish. Science 176:1035–1037Google Scholar
- Hopkins CD (1974a) Electric communication in the reproductive behavior ofSternopygus macrums (Gymnotoidei). Z Tierpsychol 35:518–535Google Scholar
- Hopkins CD 61974b) Electric communication in fish. Am Sci 62:426–437Google Scholar
- Hopkins CD (1977) Electric communication. In: Sebeok TA (ed) How animals communicate. Indiana University Press, Bloomington, pp 263–289Google Scholar
- Hopkins CD (1986a) Behavior of Mormyridae. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 527–576Google Scholar
- Hopkins CD (1986b) Temporal structure of non-propagated electric communication signals. Brain Behav Evol 28:43–59Google Scholar
- Hopkins CD, Bass AH (1981) Temporal coding of species recognition in an electric fish. Science 212:85–87Google Scholar
- Hopkins CD, Heiligenberg W (1978) Evolutionary designs for electric signals and electroreceptors in gymnotoid fishes of Surinam. Behav Ecol Sociobiol 3:113–134Google Scholar
- Hopkins CD, Westby GWM (1986) Time-domain processing of electric organ discharges by pulse-type electric fish. Brain Behav Evol 29:77–104Google Scholar
- Kalmijn AJ (1988) Hydrodynamic and acoustic field detection. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, Berlin Heidelberg New York, pp 83–130Google Scholar
- Knudsen EI (1975) Spatial aspects of the electric fields generated by weakly electric fish. J Comp Physiol 99:103–118Google Scholar
- Kramer B, Zupanc GKH (1986) Conditioned discrimination of electric waves differing only in form and harmonic content in the electric fish,Eigenmannia. Naturwissenschaften 73:679–681Google Scholar
- Schlegel PA (1977) Electroreceptive single units in the mesencephalic magnocellular nucleus of the weakly electric fishGymnotus carapo. Exp Brain Res 29:201–218Google Scholar
- Schwassmann HO (1978) Activity rhythms in gymnotoid electric fishes. In: Thorpe JE (ed) Rhythmic activity of fishes. Academic Press, London, pp 235–241Google Scholar
- Szabo T (1974) Central processing of messages from tuberous electroreceptors in teleosts. In: Fessard A (ed) Electroreceptors and other specialized receptors in lower vertebrates (Handbook of sensory physiology, vol 3). Springer, Berlin Heidelberg New York, pp 95–124Google Scholar
- Szabo T, Fessard A (1974) Physiology of electroreceptors (Handbook of sensory physiology, vol 5). Springer, Berlin Heidelberg New York, pp 59–124Google Scholar
- Watson D, Bastian J (1979) Frequency response characteristics of electroreceptors in the weakly electric fish,Gymnotus carapo. J Comp Physiol 134:191–202Google Scholar
- Westby GWM (1974) Assessment of the signal value of certain discharge patterns in the electric fish,Gymnotus carapo, by means of playback. J Comp Physiol 92:327–341Google Scholar
- Westby GWM (1975 a) Comparative studies of the aggressive behavior of two gymnotid electric fish (Gymnotus carapo andHypopomus artedi). Anim Behav 23:192–213Google Scholar
- Westby GWM (1975b) Has the latency dependent response ofGymnotus carapo to discharge-triggered stimuli a bearing on electric fish communication? J Comp Physiol 96:307–341Google Scholar
- Westby GWM (1979) Electrical communication and jamming avoidance between restingGymnotus carapo. Behav Ecol Sociobiol 4:381–393Google Scholar
- Westby GWM, Kirschbaum F (1981) Sex differences in the electric organ discharge ofEigenmannia virescens and the effect of gonadal maturation. In: Szabo T, Czeh G (eds) Sensory physiology of aquatic lower vertebrates. Adv Physiol Sci vol 31. Pergamon Press, New York, pp 179–194Google Scholar
- Wilczynski W, Zakon H, Brenowitz EA (1984) Acoustic communication in spring peepers. J Comp Physiol A 155:577–584Google Scholar
- Zakon HH (1986) The electroreceptive periphery. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 103–156Google Scholar