Neuroethology of Electroreception. Weakly Electric Fish

Transcription

1 Neuroethology of Electroreception Weakly Electric Fish

2 Evolution of Electroreception *monotremes *cetacean Electroreception has evolved in at least 10 vertebrate taxon

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4 Candiru Catfish (aka Vampire fish) Electroreceptive parasitic fish

5 Candiru Catfish Candiru (Yes, Some Say the Urban Myth is True!)

6 Ray Troll

7 Ray Troll

8 When you are in the Amazon River DO NOT urinate in the water! Ray Troll

9 If you do, be prepared! Ray Troll

10 Active vs. Passive Electroreception Active location systems: Sender: Receiver: Animal Animal Passive location systems: Sender: abiotic environment or biotic: other animals Receiver: Animal Sender = Receiver Examples: echolocating bats, electrolocating fish humans =? Ben Underwood Sender = Receiver listening bats electroreception in sharks & rays seeing in humans

11 Strong vs. Weakly Electric Fishes Capable of discharging V Up to 220V Up to 600 V, 100 A Lesser electric ray with strong & weak EODs mv to <1 V

12 Weakly Electric Fishes Two types of freshwater weakly electric fishes weakly electric = producing electric organ discharges in the range of mvs (thousandths of volts) (1) Mormyrids (Family Mormyridae) (2) Gymnotoids (Order Gymnotiformes)

13 Research on Weakly Electric Fish Science Nation Electric fish charges up research on Animal Behavior Fortune and Cowan Labs

14 Mormyrids (Family Mormyridae) common name = elephantnose fishes ~190 species - live in the tropical freshwaters of Africa Brienomyrus hopkinsi from the Ivindo River in Gabon (Photo: C. Hopkins).

15 Mormyrids (Elephantnose fishes) The electric organ discharges (EODs) are pulse type discharges Gnathonemus petersii The EOD is composed of two parts: a fixed EOD waveform, and a variable sequence of pulses intervals Pulse-type signal

16 Mormyrids (Elephantnose fishes) Pulse EODs are used during social behavior (more about function of EODs later.) Brienomyrus brachyistius Carl Hopkins Cornell University Electrical and motor activities of the electric fish, Brienomyrus brachyistius, recorded and analyzed in the Hopkins Lab

17 Waveforms of Mormyrids are species-specific Six distinctive signal types from specimens from five species of Paramormyrops from the Okano River in Gabon, Africa. (From the Hopkins Lab)

18 Some Mormyrids also produce species-specific vocalizations for acoustic communication Sounds produced by Pollimyurus isidori Pollimyrus adspersus

19 Gymnotoids (Order Gymnotiformes) common name = knifefishes ~55 species Eigenmannia virescens found in tropical freshwaters of South America electric organ discharges are a continuous wave type discharge (electric pulses are produced in a quasi-sinusoidal manner with the duration of the pulses comparable to the duration of the interpulse interval) Sternopygus macrurus

20 Gymnotoid Waveforms are Species-specific EOD shape is: Species-specific ( Hz) Sexually dimorphic Juvenile-adult Individual-specific E.g., Sternopygus EODs range from Hz Apteronotus EODs range from Hz Eigenmannia EODs range from Hz

21 How Do These Fish Generate the Weak EODs? Mormyrids Gymnotoids Electric organs derive from muscle cells or motoneurons which no longer innervate muscle

22 The Electric Organ - electric organ in found in the tail - composed of modified muscle cells called electrocytes, each of which can produce an electric discharge of some tens of mvs. Stoddard (2009) - many of the electrocytes are arranged in series for the synchronous EO discharge. Stoddard (2009)

23 How is the EOD Frequency Controlled? The rhythm or regularity of the EODs is determined by an endogenous oscillator in the fish s hindbrain known as pacemaker nucleus. Command pulses generated by the pacemaker cells which drive the discharges of the electric organ in a oneto-one fashion.

24 Electric organ discharges (EODs) can be recorded with electrodes close to the head and tail EODs of Eigenmannia (Movie) Assad C, Rasnow B, Stoddard PK, Bower JM. (1998) Electric fields of the gymnotiform fishes: II. Eigenmannia. Journal of Comparative Physiology A. 183(4): EODs are displayed in pseudo color for electrical potentials: + charge = green to red DC (0 V) = light blue - charge = blue to violet

25 The Electroreceptor System Weakly electric fish possess two types of electroreceptors: (1) Ampullary electroreceptors tuned to DC (constant current) and low-frequency modulated electric signals (<40 Hz) (2) Tuberous electroreceptors tuned to the animal s own EODs The two types of electroreceptor organs in the skin of Eigenmannia TU = tuberous electroreceptor organ AM = ampullary electroreceptor organ; note the reduce canal length compared to those observed in elasmobranchs (sharks, skates, and rays)

26 Electroreceptor Excitation and Inhibition Both types of electroreceptors are excited by a positive (+) electrical stimulus and inhibited by negative (-) stimulus)

27 Differential Sensitivity of Ampullary vs. Tuberous Electroreceptors mv/cm Stoddard (2009)

28 Receptors are tuned to the frequency spectrum of the species

29 Tuberous organs are specialized to detect EODs Time-code receptors are frequency tuned to match the power spectrum of the species s EOD. time-code amplitude-code gymnotids T-unit P-unit mormyrids Knollenorgan mormyromast

30 Tuberous electroreceptors: Time Coders Relative stimulus time-code gymnotids T-unit mormyrids Knollenorgan Time Coders afferents fire one spike on each cycle of the stimulus and are phase-locked to the zero crossing of the signal. (also called phase coders)

31 Tuberous electroreceptors: Amplitude Coders amplitude-code gymnotids mormyrids P-unit mormyromast Amplitude Coders afferents fire intermittently and increase their firing rate (in a probabilistic manner) with a rise in stimulus amplitude.

32 Biological Function of the Weakly Electric Fish s Electrosensory System 1. social communication between conspecifics (tuberous electroreceptors + electric organ) 2. prey detection (primarily ampullary electroreceptors) 3. electrolocation (tuberous electroreceptors + electric organ)

33 Electric Communication Studied in both gymnotoids and mormyrids Social signals used in territory defense and reproduction Aggression, courtship, appeasement Identification of sex, species, and individual

34 Court and Spark Courtship in Gymnotoids

35 Gymnotoid Complex Courtship Signals Brachyhypopomus pinnicaudatus Stoddard (2009)

36 Complex Social Signals of 3 Gymnotiform Species Stoddard (2009)

37 Biological Function of the Weakly Electric Fish s Electrosensory System 1. social communication between conspecifics (tuberous electroreceptors + electric organ) 2. prey detection (primarily ampullary electroreceptors) 3. electrolocation (tuberous electroreceptors + electric organ)

38 Chisembe Shadow Hunters of Malawi

39 Biological Function of the Weakly Electric Fish s Electrosensory System 1. social communication between conspecifics (tuberous electroreceptors + electric organ) 2. prey detection (primarily ampullary electroreceptors) 3. electrolocation (tuberous electroreceptors + electric organ)

40 Electrolocation = the ability to sense objects in the environment by emitting weak EODs and then detecting the small perturbations in the self-generated electric field due to nearby objects in the water Electrolocation capability by weakly electric fishes was first demonstrated in the 1950s by Hans Lissmann (professor at the University of Cambridge, UK). Lissmann HW and KE Machin (1958). The mechanism of object location in Gymnarchus niloticus and similar fish. J. Exp. Biol. 35:

41 Jamming Avoidance Response (JAR) JAR = a shifting of the fish s own frequency away from neighbor s EOD frequency. Eigenmannia Wave-type fish JAR behavior was first described by Watanabe and Takeda (1963) from the Tokyo Medical and Dental University. Now classic paper in JEB. WATANABE, A. & TAKEDA, K. (1963). The change of discharge frequency by a.c. stimulus in a weak electric fish. J. exp. Biol. 40,

42 History of the Neural Basis of JAR Behavior Ted Bullock (Scripps Institution of Oceanography) and colleagues were the first to thoroughly characterize the JAR. Walter Heiligenberg (also from Scripps) and his lab over a period of 20 yrs eventually revealed: (1) how the fish determines the sign of the DF, & (2) how the fish implements the JAR behavioral rules

43 Jamming Avoidance Response (JAR) Problem = when two fish with similar EOD frequencies come together the potential for EOD interference or jamming can occur! The jamming effect is most detrimental if EOD difference is approx 20 Hz or less. Solution = Jamming Avoidance Response (JAR)

44 Jamming Avoidance Response (JAR) If EOD is higher than neighbor, raise it If EOD is lower, lower it Note: these observations demonstrate that fish are able to determine the sign of the frequency difference (commonly referred to as DF )

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