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L20. The Jamming Avoidance Response (J.A.R.) of Electric Fish (1: Behavior)

September 28, 2011

Carl D. Hopkins

e-fish e-receptor

e-organ October 3

Please email Wikipedia Project title to Carl Hopkins by Monday AM

Outline

1) Electroreception and electrogenesis. – Electroreception arose as a 6th sense in aquatic vertebrates as a means for

detecting bioelectric current arising from muscles and epithelial tissues of prey.

– Several clades of fishes generate weak electric discharges from e-organs; the e-organs are used for communication or object detection.

– Powerful electric discharges evolved later for predation or defense.

2) Independently, 2 large clades of e-fish evolved elaborate e-communication. – Some species have pulse discharges others have wave discharges.

3) Wave fish jam each other when the discharges have the same frequency. – Can’t e-locate when jammed.

4) The jamming avoidance response (JAR) shifts the discharge frequency away from the jamming frequency – JAR restores electrolocation

5) The JAR is an ideal sensory/motor system for tracing out the entire neural circuit for a complex behavior.

?

“Passive” electroreception is electrical listening

Kalmijn, A. (1971) J. Exp. Biol. (see Hopkins, 2010)

Ampullae of Lorenzini

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Electroreception is present in many aquatic vertebrates Electroreception arose early in vertebrates and was lost and re-grained. Electric organs: a model system for study of parallel evolution of novelty

electroreception

© Hopkins. In Lavoué et al, in preparation

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Electric Fishes

Actinopterygii (ray-finned fishes) – Mormyroids

• Gymnarchus (1 family, 1 species)

• Mormyridae (1 family, 200+ species)

– Siluriformes: • Malapteruridae (1 family, 3-10 species ?)

– Gymnotiformes (7 families, 150+ species)

– Perciformes: Uranoscopidae (stargazers)

Electric organs arose independently in 6 lineages of fishes. Elasmobranchs Torpedo rays Skates (Raja)

Two independent lineages of teleosts fishes speciated rapidly at about the same time (after independent evolution of electroreception). Horizontal timescale is in million years before present (Mya). Horizontal bars at nodes are 95% age credibility intervals. Last temporal stages of the separation of Africa and South America are indicated with three inserts.

** Lavoué, Sébastien, Miya, Masaki, Arnegard, M. E. , Sullivan, J. P., Hopkins, C. D. and Nishida, M. (in preparation). Simultaneous origins of electrogenesis in teleost fishes.

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Sternarchorhynchus roseni

Sternopygus macrurus

Adontosternarchus sachsi

Eigenmannia virescens

Gymnotiformes

C.D. Hopkins 10

Mormyriformes

ISICHTHYS

HIPPOPOTAMYRUS

PETROCEPHALUS

BOULENGEROMYRUS

BRIENOMYRUS

2 FAMILIES 198 SPECIES 18 GENERA

CAMPYLOMORMYRUS

C.D. Hopkins

C.D. Hopkins

C.D. Hopkins

C.D. Hopkins C.D. Hopkins

C.D. Hopkins

Electric fish produce either “pulse” discharges or “wave” discharges

** Lavoué, Sébastien, Miya, Masaki, Arnegard, M. E. , Sullivan, J. P., Hopkins, C. D. and Nishida, M. (in preparation). Simultaneous origins of electrogenesis in teleost fishes.

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“Active” Electrolocation

Resistive object (glass rod).

Discovered using training paradigm (Lissmann, 1958).

glass rod inside clay pot

recorder (detects hit)

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ELECTRIC COMMUNICATION

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EIGENMANNIA VIRESCENS

10 ms

300 Hz

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Swinging fish quantifies electrolocation performance

swinging rods plastic rod inside electrically-‘transparent’ agar

Rods swing, fish follows rod diameter = 15.6 mm

Rods swing, fish bumps into them. diameter = 3.7 mm

Heiligenberg, 1974

rods

fish

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F=400; S = F+/- 40 Hz Ft= fish frequency (400 Hz); S= external sine wave stimulus

Electrolocation GAIN gain = out/in PHASE

i - o

S-F

Conclusion: Eigenmannia is unable to electrolocate when external stimulus is similar in frequency to its own discharge.

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THE JAR = jamming avoidance response

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Jamming Avoidance Response

Theodore H. Bullock and H. Scheich

Walter Heiligenberg

Eigenmannia

Watanabe A and Takeda K (1963) The change of discharge frequency by A.C. stimulus in a weakly electric fish. J Exp Biol 40:57-66.

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Frequency Clamp

Stimulus frequency ‘tracks’ the fish’s EOD frequency.

Moves up or down until asymptote (takes 20 seconds).

Switch stimulus from +deltaF to –deltaF.

315

330

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Key Stimuli

Q? What are the essential conditions needed to evoke a JAR?

Thus: NO apparent connection between pacemaker and sensory areas. (No corollary discharge)

PM

S

PM

S2 S1 (substitute EOD)

JAR JAR

F

S

F

S

EOD

Fre

qu

ency

? ?

F = fish frequency, S = stimulus

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“Key” Stimuli for JAR

1. |S-F| < 4 Hz. 2. Two signals: S (stimulus) + F(fish). or S1 (artificial EOD + S2 (artificial jamming stimulus)

F is silenced with curare + Fish’s pacemaker is monitored in tail. S1 (F substitute) delivered between gut and tail. S2 delivered through external electrodes

3. Geometry for two signals. Condition Response Silence F. Stimulus = S1 + S2 (same geometry) no JAR

Stimulus= S1+ S2 (differential geometry) JAR S1 (tail only) + S2 (head only) JAR

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The Stimulus

sine wave 1 sine wave 2 amplitude envelope is identical for +df and -df Interval between zero crossings phase of S1+S2 relative to S1 alone

400 404 400 + 404

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What is the stimulus?

both fish generate EODs FIsh 1, senses self plus fish 2

strong S1 moderate S2 beat Strong S1 zero S2 very small beat

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What is the nature of the real stimulus?

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Mixing of Two Signals

The mixing of two signals is modulated both in amplitude and in phase.

Summed signals

phase, plotted against amplitude.

delay advance

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What differs between + F and - F?

400 +402 demo

400 +398 demo

Heiligenberg’s algorithm:

Determine the sign of rotation of circle

advance delay advance delay

JAR Video

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Clever Experiment Shows Need for both phase and amplitude information

compartment A gets both phase and amplitude modulated signal, B gets pure sine wave

A gets amplitude modulated,

B gets phase modulated.

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Electroreceptors

AMPULLARY TUBEROUS

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Ampullary Electroreceptors Code for D.C. stimuli.

Tonic activity in absence of stimulus Increase firing rate on D.C. +ve outside. Decrease firing rate on D.C. –ve outside. ‘Frequency code’

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Peripheral Receptors

T-unit: fires on zero-crossing (every cycle) of stim.

P-unit: probability codes amplitude of stimulus; P(spike) ~ amplitude of stimulus.

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Neuronal responses are close match to phase/amplitude plots

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Neuroanatomy of JAR

Overview of entire pathway.

Torus semicircularis

Electrosensory Lateral Line Lobe (ELL)

3 ‘redundant’ maps of skin

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Lessons from JAR

1. Electric fish use EOD for electrolocation of objects: active location of objects.

2. Eigenmannia (a wave species) is jammed by sinusoidal stimuli near their own frequency (electrolocation performance deteriorates when ΔF < 4 Hz).

3. Eigenmannia performs JAR to avoid jamming. Both F and F . JAR is a model for understanding decision making.

4. JAR depends on two inputs, S1 + S2 (no reference to pacemaker)

5. JAR depends on differential geometry.

6. Two cues: amplitude modulation + phase modulation

7. counter clockwise rotation if +ΔF, clockwise rotation if -ΔF

8. Two sensory cues: AM, PM

9. Two receptor types: amplitude coder (P), phase coder (T)

References

Watanabe, A., Takeda, K. (1963) The change of discharge frequency by A.C. stimulus in a weak electric fish. J. Exp. Biol. 40: 57-66.

Bullock, T.H., Hamstra Jr., R., Scheich, H. (1972) The jamming avoidance response of high frequency electric fish. J. comp. Physiol. 77: 1-22.

Heiligenberg, W. (1991). Neural nets in electric fish. Cambridge, Massachusetts: MIT Press.

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Pulse Discharges Wave Discharges

1 s 1 ms

1 ms

pulse discharge

wave discharge

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Electroreception