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Electric organ discharge frequency modulation evoked by water vibration in Gymnotus carapo
Camp. Biochem. Physiol. Vol. IOOA, No. 3, pp. 555562,
0300-9629/91$3.00+ 0.00 0 1991Pergamon Press plc
1991
Printed in Great Britain
ELECTRIC ORGAN DISCHARGE FREQUENCY MODULATION EVOKED BY WATER VIBRATION IN GYMNOTUS CARAPO L. C. BARRIO,* A. CAPuTr,t L. CRISPINO~ and W. Btio*$ *Unidad de Neurobiologia Funcional, Neurofisiologia, Instituto Cajal, CSIC, Av. Doctor Arce 37, 28002 Madrid, Spain, Fax: (91) 5854154; thleurofisiologia, Instituto “C. Estable”, Av. Italia 3318; $Dpto. de Fisiologia, Facultad de Medicina, Av. General Flores 2125, Montevideo, Uruguay (Received 2 January 1991)
Abstract-l. The electric organ discharge (EOD) frequency modulations evoked by brief water vibration were analysed in the pulse-type fish Gymnorus carapo. 2. The response consisted of a transient increase of the EOD frequency at short latency (30msec). Response profiles were characteristic of the specimen and relatively independent on stimulus intensity. 3. Conversely, they were dependent on stimulation sequence, showing a rapid decrement along successive stimuli and high temporal discrimination. 4. The brief latencies indicate a relatively simple neural circuit. 5. The response may be an electrolocation enhancement strategy for the detection of moving objects based on “sampling” the periphery at a higher frequency.
This investigation describes and quantifies, in the South American pulse-type species Gymnotus carapo, the transient EOD accelerations evoked by brief, low amplitude, vibrations transmitted through the water. Stimuli such as water drops and small objects falling into the aquarium or fast movements of a small glass rod close to the fish elicited the response. This “reflex” may also be an electrolocation enhancement strategy for detection of rapidly moving objects or may be used to signal novel stimuli to animals of the same species.
INTRODUCTION Much evidence is available on the behavioral meaning of short-term modulations of the electric organ discharge (EOD) frequency in wave-type weakly elec-
tric fish species, but less is known about pulse-type fish (for reviews, see, e.g. Heihgenberg, 1986; Hopkins, 1988). Short-term EOD modulations are either used to enhance the fish’s ability to electrolocate, or as social communication signal (e.g. Baker, 1980; Bastian, 1981, 1986~; Bell and Szabo, 1986; Black-Cleworth, 1970; Bullock et nl., 1961, 1972; Heiligenberg, 1973, 1974, 1986; Hopkins, 1988; Westby, 1974, 1975). Electrolocation consists in object detection by actively sensing distortions of the electric field of the fish’s own EOD (e.g. Bastian, 1986~; Bullock et al., 1961; Carr and Maler, 1986; Fessard and Szabo, 1961; Heiligenberg, 1987). Electrolocation ability may be enhanced by changing the EOD frequency. The best understood electrolocation enhancement strategy is the jamming avoidance response which occurs when two fish emitting similar EODs interfere (e.g. Baker, 1980, 1981; Bullock et al., 1972; Dye, 1987; Heiligenberg, 1974, 1986). Less understood are EOD accelerations occurring in certain species when they begin to swim, or when presented with unexpected stimuli in the form of “startle or novelty responses” (e.g. Dye, 1987; Hagedorn, 1986; Hopkins, 1988; Grau and Bastian, 1986). More stereotyped, transient, EOD accelerations, with unknown functional meaning, are evoked by vibration and sound (e.g. Kramer et al., 1981; Lissman, 1958). SAddress all correspondence to: Dr Washington
MATERIALS AND
Buxio, Unidad de Neurobiologia Funcional, Neurofisiologia, Instituto Cajal, Av. Dr. Arce 37, 28002 Madrid, Spain. Telephone: (341) 585-4115, Fax: (341) 585-4154.
METHODS
Animals (7-12-cm long) were gathered the same day in late May from a lake in the south-east of Uruguay (Laguna de1 Sauce, Departamento de Maldonado). They were classified as Gymnotus carapo both by their external phenotypic characteristics and head-to-tail multiphasic EOD waveform (e.g. Trujillo-Cenoz et al., 1984; Caputi et al. 1989). Each animal (N = 5) was placed in a cylindrical 10-l aquarium at room temperature (19-21°C) for l-3 weeks before experiments. Figure 1 shows a diagram of the recording-stimulating set-up. A small 20 x 30 cm opaque plastic tank, filled to about 7cm high was used. The fish was placed inside a 2.5 cm diameter nylon mesh tube (mesh size about 2.5 mm) which was adjusted in length to about 1 cm longer than the fish to restrain its movements. The tube had carbon electrodes (from 1.5 V batteries) at both ends connected to a capacity-coupled (0.1 set time constant) preamplifier to record the EOD (P9 in Fig. 1). Recordings were of constant amplitude and waveform (Fig. 2Al). The EOD was displayed on an oscilloscope (CR0 in Fig. 1) and recorded on a stereo audio cassette tape (30 Hz to 12 kHz bandwidth) together with synchronization pulses from a pulse generator. Regular single or barrages of brief (I-1Omsec) pulses (Fig. 2A3) from the generator were fed at different rates to a small speaker which had a glass pipette (I .6 mm diameter) glued to the center of its diaphragm (Fig. 1). The pipette tip
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EXPERIMENTAL t
SETUP
.--. LOUDSPEAKER
Fig. 1. Diagram of stimulating and recording set-up. was occluded with wax. Water displacement stimulus waveforms were monitored (Fig. 2A2), but not tape recorded, with an uncalibrated home-made hydrophone placed inside the mesh tube.. They usually consisted of several rapidly decaying waves, at frequencies between about 125.0 and 250.0 Hz, with overall stimulus durations which lasted up to 20 msec, but usually ended with about 10 mscc. The delay from stimulus pulse on to water displacement onset was variable (2-10 msec) and depended on pulse waveform and polarity. The glass pipette moved vertically about 200 to IMO~m, as measured with long duration pulses under a dissecting microscope. Its tip was placed about 2-4cm above the animal’s head (Fig. 1). Stimuli were also delivered locked 1 to 1 at a fixed delay or phase (4) from EODs by synchronizing the pulse generator with the EOD at different delays (FIXED 4 in Fig. 1). Phase was calculated by adding the pulse generator to the water displacement delays. Animals were left to adapt to the experimental environment in
A
C
6
INTERVAL
3
constant artificial incandescent light for about 1 hr before stimulation and recording were performed. Only fish which remained relatively motionless and displayed a very regular EOD were used. This situation will be termed “control”. Stimuli never evoked overt movement reactions. Data was processed off-line by playing back cassettes in a PDP-I1 computer. The computer displayed inter-EOD interval (I) durations sequentially with 512 successive I (except in Fig. 6 where 1024 intervals were plotted) called here interval plots (IP) (Fig. 2C). It calculated instantaneous frequency vs time plots and averages (Fig. 2Dl), either with 128 or 256 successive responses, of several of these plots (FPAs) and standard deviation vs time plots for FPAs (Fig. 2D2) (e.g. Barrio and Butio, 1990). Averages were calculated after a 2-3-min stimulation period to elimlnate response variation at stimulation on (see Results). InterEOD intervals in FPs were measured with IOO~sec accuracy. EODs, stimulus pulses and water displacement
r-l
E?D
30-l
D
OI EOD NUMBER
‘zonis
Fig. 2. Stimulus and response characteristics. A: (1) Electric organ discharge EOD (head to tail) and superimposed instantaneous interval plot (IP); (2) water vibration; (3) pulse fed to stimulator. The inter-EOD interval (I) and the phase and cophase (4 and 0, respectively) are indicated. B: Single EOD, and C: IP during control and at stimulus on. Interrupted line indicates the baseline inter-EOD interval. D: (1) Average instantaneous frequency plot (AFP); (2) standard deviation. Vertical arrows indicates stimulus on, as in all other figures. Interrupted line indicates baseline in record 2.
Vibration-evoked EOD modulation waveforms were plotted on paper with a digital oscilloscope XY plotter system. RESULTS
In control conditions fish displayed regular EOD with mean frequencies which in different animals varied between 33.5 and 45.0 Hz, with coefficient of variation of inter-EOD intervals ~0.008, and peakto-peak amplitudes between about 20 and 40 mV. The response to brief water vibrations consisted of a transient increase of the EOD frequency evoked after a brief delay (about 30msec). Responses showed a rapid rising phase peaking at about 200 msec and a longer (about 1.2 set) recovery phase. They were characteristic of the specimen and were highly reproducible and relatively independent on stimulus intensity in a given fish. Conversely, they were highly dependent on stimulation sequence, showing a rapid decrement along successive stimuli and high temporal discrimination between individual stimuli. Figure 2A1, illustrates the rhythmic discharge and Fig. 2B, the filtered recording of the multiphasic head to tail EOD (cJ Trujillo-Cenoz et al., 1984). Figure 2A2 shows the water displacement waveforms, and Fig. 2A3, the stimulus pulse records. The IP superimposed on record Al, shows the characteristic response consisting of a rapid shortening of I durations (i.e. EOD acceleration) with a minimum interval (or peak response) which was reached in about six EODs (close to 125 msec). The I decrease at the peak of the response was about 4msec from the close to 24.5 msec control or baseline mean inter-EOD interval (i.e. a decrease of about 16%). The IP in Fig. 2C, shows control conditions with a baseline mean I value of about 26 msec or 37.0 Hz, and the effects of regular stimulation of 0.4/set in another fish. The on response was largest (as in all other cases), peaking at about 9 EODs (peak latency about 230msec). The I value at the peak was 18.9 msec or 53.0 Hz, a close to 73% decrease from the baseline I, or a 16.0 Hz increase (Af= 16.0 Hz) from the baseline EOD frequency. Subsequent I increased in duration (i.e. the EOD decelerated) gradually, relaxing towards the baseline (interrupted line). Baseline values were not completely recovered because successive responses occurred before the total relaxation of the preceding response. Successive responses decreased gradually in amplitude and eventually stabilized with about 10 to 15 stimuli at an amplitude which depended markedly on stimulus rate (see below). This relaxation-which will be called attenuation-also increased gradually, although control values were not completely recovered at this stimulus rate. Figure 2Dl shows the FPA obtained in response to single pulse stimulation at 0.2/set. The response consisted of a rapid EOD acceleration followed by a gradual deceleration towards the baseline (interrupted line). The brief latency to response on and to the peak should be highlighted. The gradual relaxation lasted about 1.5 sec. The baseline EOD frequency was 44.5 Hz and the peak was 54 Hz, a 9.5 Hz increase (Af= 9.5 Hz). The standard deviation vs time plot in Fig. 2D2, shows an irregular profile with small values throughout, and a small
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peak at the EOD acceleration, indicating that the responses evoked by each stimulus were similar to the mean, well defined temporally, and highly predictable in waveform. Therefore, averages were good estimates of individual responses. Figure 3 shows stabilized responses and stimulus rate effects. The IP in Fig. 3A, illustrates successive responses evoked with pulses at O.S/sec. They consisted of rapid accelerations followed by gradual relaxations. The FPAs (N = 128) show the same responses at two different sweep speeds (2 and 3, respectively). They consisted of an initial acceleration which peaked at latencies of about 80msec. The water vibration on, to averaged response latency was measured in FPAs in all fish; the lowest value was 15 msec with a mean value of 30msec. The EOD frequency at the peak in Fig. 3 was 44.0, a 4.0 Hz increase (Af = 4.0 Hz) from the mean 40.0 Hz baseline. The initial acceleration was followed by a rapid deceleration and a second smaller peak which then relaxed gradually. Responses evoked by single pulses had durations between 600msec and 2 set (mean 1200 msec), as estimated from FPAs in all the fish. Response duration was little affected by stimulus intensity (data not shown). The IP in Fig. 3Bl and the FPAs (N = 254) in Fig. 3B2 and B3, respectively show that responses were smaller than in A (Af= 2.5 Hz) with stimuli at 2.0/set, but the response profile was essentially identical. Figure 3C shows the Afreduction as a function of stimulus rate. In this specimen and for unknown reasons, there was also a reduction of the baseline from 40.0 to 38.5 Hz in A and B, respectively. Figure 4 shows responses evoked by paired pulses at l/set in the same fish used in Fig. 3. The IPs in A, illustrate the relatively constant responses evoked with pulses at 10, 20 and 40 msec delays (1, 2 and 3, respectively); IP A4 shows two clearly separate peaks with interpulse delays of 320 msec. The corresponding FPAs are shown at two different sweep speeds in Bl-4 and Cl-4, respectively. Either a single peak 1, a peak with two humps 2, or two separate peaks 3 and 4, were evoked with pulses at 10,20,40 and 320 msec, respectively (arrows indicate the second response components). Note also the longer lasting plateaux in records C2 and C3. The frequency difference between the first and second peaks (S lS2) vs interpulse delay is shown in Fig. 4D. The Sl-S2 difference first increased with increasing delays, up to delays of about 40msec, and then decreased. Results reveal that only when the stimulus became physically two different events (220 msec; see Materials and Methods) was the animal able to discriminate the difference. Figure 5A and B compares single pulse effects with those evoked by pulse barrages (rate lO/sec, duration 1.5 set), respectively, presented at about 0.6/set. The IP shows somewhat larger I reductions in Bl and Al. The mean baseline EOD frequency was 38.5 Hz. The FPAs evoked by single pulses in A2 had a more complex profile in this fish. The response consisted of a fast acceleration (1) an initial peak (Af = 5.5 Hz) at latencies of about 60 msec (2) a rapid deceleration (3) reaching a constant frequency plateau at about 40.5 Hz (4) and a gradual relaxation to baseline values (5). The response profile was essentially
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01
EOD NUMBER
0
10
20
30
STIMULUS RATE (impulses/s)
Fig. 3. Stimulus rate effects. A, B: Stimulation at 0.5 and 2 Hz, respectively. (1) IP, and (2, 3) AFPs at two different sweep speeds. C: Peak EOD frequency minus baseline (Af ) vs stimuius rate plot.
identical in B2, but response durations increased at the expense of component 3 and also of the plateau 4. Both the peak 1 and the plateau 4 were higher in B (Af = 6.5 Hz and 41 .OHz, respectively). Note also that there was no EOD frequency modulation associated with individual stimuli in B. It should be understood that response profiles were characteristic of the individual fish, and did not change much with stimulus parameters (except notably for the above described effects). Profiles were usually simple, as those in Figs 2 and 3 (three out of five fish) and sometimes complex (e.g. Figs 4 and 5). The IPs in Fig. 6 show the effects of 1 to 1 phase locked stimulation (i.e. FIXED 4; see Fig. 1 and Materials and Methods) with Cpat 6, 12 and 24 msec (A, B and C, respectively). Phase is the time elapsed between the EOD and the next water vibration on.
delay was 6 msec, and the calculated 4 are indicated by the horizontal arrows. Note that 4 briefer than 6 msec could not be explored. The baseline I was 38 msec or about 28.0Hz. The on response was essentially identical in the three records, indicating that it was 4 independent. The response had a simple profile consisting of a rapid I duration drop to about 28 msec (i.e. and EOD acceleration to close to 35.5 Hz) followed by a gradual relaxation. Since d, was fixed, the acceleration occurred at the expense of a shortening of the time elapsed from the stimulus on to the next EOD or cophase (0). The initial response did not return to baseline values (interrupted line) because in all three cases there was a second acceleration (asterisks) before complete relaxation of the initial response (there was also a third peak in B; arrow). The second acceleration was
The water vibration
Vibration-evoked
559
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Fig. 4. Paired pulse stimulation. A: (l-4) IPs with stimulation at different rates. B, C: FPAs at two different sweep speeds (arrows indicates “second” response). (l-4) as in A. D: Plot of the difference between the first and second responses (SlS2) vs interstimulus interval.
longer lasting in C. It started more gradually, stabilized at about 65% of the baseline I, lasted about 15 set, and finally relaxed gradually. Note that in C, with the acceleration the EOD tended to occur simultaneously “in synchrony” with the water vibration, We never observed off responses with phaselocked stimulation (Fig. 6) nor with long-lasting pulse barrages (data not shown).
DISCUSSION
Objectives of this investigation were to: (i) provide a quantitative de~ription of the short-term EOD modulations evoked by water vibration, (ii) compare the results with previous analysis of EOD frequency modulations evoked in other experimental conditions, (iii) suggest mechanisms,
I
EOD NUMBER
*\ 13 4 I 1.
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Fig. 5. Pulse barrage effects. A: Single pulse stimulation, and B: barrage, (1) IP and (2) FPAs. Note complex response profiles with labeled components (l-5) in records 2. Horizontal line indicates stimulus and off is shown by second arrow, as in subsequent figure.
L. C. BARRIOet al.
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12..* 50 ms
1
Fig. 6. Fixed phase (4) stimulation. IPs at increasing 4 values from A to C. Horizontal arrows indicate timing of individual stimuli, and asterisks the “second” response component. The open arrow in B, indicates a third response.
implications and biological relevance of the observed behaviors. The EOD frequency was transiently increased in a stereotyped and highly predictable manner by water vibrations. The response showed extremely welldefined time relationship with the stimulus. Although responses evoked by successive stimuli were highly consistent and relatively insensitive to intensity in a given specimen, three different response profiles, shown in Figs 2D, 3A3, and 5A2 were observed in different fish. Only five animals were used in the experiments, but the different response profiles in each fish suggest strongly that they were characteristic of the individual. Of interest were the brief response latencies which indicate that a relatively simple neural circuit underlies the EOD acceleration evoked by water vibration. Considering a pacemaker to EOD conduction time of about 5 msec (Caputi, Silva and Macadar, in preparation) results indicate that an extremely brief “processing” time is necessary for the response. Brief latencies revealed an efficient strategy in terms of a possible electrolocation enhancement since the frequency shift started within about one inter-EOD interval and peaked very rapidly in only 5 to 10 EODs after stimulus on. Although on responses were similar in a given fish, the modulation depth Af was highly dependent on past stimulation history. Indeed, there was attenuation along successive stimuli (Fig. 2). This attenuation effect was present at low rates of stimulation and was enhanced when the stimulation rate was increased (Fig. 3). Rapid, stimulus rate-dependent functional
response decrements suggests that the system favors the detection of unexpected stimuli. Stimulus barrages at high rate caused the EOD frequency to increase and subsequently to yield rapidly to less than 50% of the on response at the end of the barrage (Fig. 5). Attenuation was present without frequency modulation of the EOD evoked by individual stimuli in the barrage. Therefore, the reduction should reflect a neural process rather than result from mechanical summation at pre-receptor levels since the temporal resolution of the system probed with paired stimuli (Fig. 4) was about five times greater than that necessary to discriminate individual pulses in the barrage (e.g. 20 msec vs 100 msec). Another response feature that depended on past stimulation was the amplitude variation of the second response evoked by stimulus pairs. Responses first increased (up to about 50 msec) and then decreased with interpulse delay (Fig. 4). The final decrease may reflect what we have termed stimulus attenuation, and is clearly a different process than the initial increase. The functional role of the brief initial period of response enhancement could be to increase response probability with a specific timing of the stimulus thus favoring responses at short intervals (< 50 msec). As in other systems (e.g. Bufio et al., 1981) both the initial response enhancement and the subsequent attenuation may be considered as mechanisms which increase the detectability of unexpected stimuli. The novelty responses evoked by electrosensory stimuli (e.g. Westby, 1974, 1975) and other sensory modalities (Dye, 1987; Hagedorn, 1986; Hopkins,
Vibration-evoked
1988; Lissman, 1958; Zelick, personal communication) are characteristic of pulse-type gymnotids. It has been proposed that the correlation between increased motor activity and EOD acceleration which occurs in most pulse-type Gymnotiform fish (BlackCleworth, 1970; Hagedom, 1986) might be a clue to explain the ability of these fish to respond with reflex EOD accelerations to stimulations of most sensory modalities (e.g. Kramer et al., 1981). In such type of fish a connection between motor centers and the electromotor command system probably still exists, including the nucleous magnocellularis mesencephaly (e.g. Finger, 1986; Retelyi and Szabo, 1973; Sas and Maler, 1983). Therefore, any stimulus which modifies motor activation can evoke EOD acceleration via those motor command centers. Among such stimuli those that activate the lateral line mechanosensory system which conveys vibratory information are perhaps the most important. The similarities between the responses described here and those evoked by sound, light and touch (e.g. Black-Cleworth, 1970; Kramer et al., 1981; Zelick, personal communication) are in favor of the above view, despite the fact that sound stimuli show little or no attenuation (Kramer et al., 1981). The differences suggest that attenuation could take place at earlier processing stages for vibratory information, as occurs in the electrosensory system. The anatomical parallelism of electrosensory and lateral line systems (Bell and Szabo, 1986; Carr and Maler, 1986; Finger, 1986) suggest that the same mechanisms of gain control and electric novelty detection (Bastian, 1986a,b,c; Bratton and Bastian, 1990; Grau and Bastian, 1986) could also be present in the central processing of vibratory information. Pulse-type fish may actively electrolocate only within a brief time window provided by the “standing” electric wave generated by their own EOD. Therefore, vibration-dependent EOD accelerations may be interpreted as an electrolocation enhancement strategy based on “sampling” the periphery at a higher frequency. The increased EOD frequency would improve the system’s+ temporal resolution. Therefore, the vibration-evoked EOD acceleration would increase the probability of correctly electrolocating the source of vibration, and more important perhaps, of detecting its movement direction. The response may also be used to signal novel stimuli to animals of the same species. The effects of fixed phase stimulation are difficult to interpret (e.g. Westby, 1975). However, it could also represent an electrolocation enhancement strategy which function either by synchronizing the EOD with certain types of stereotyped movements and their subsequent mechanical effects, as perhaps occurs in startle and escape responses, or to synchronize the EOD with the movement of the vibrating source to emit EODs during its movement. A similar strategy has been shown in other neural pacemakers (But50 et al., 1984), where the stimulus-response synchronization may be related to the capacity to tune in and detect periodic signals buried in noise. Acknowledgements-Work supported by a Commission of European Communities grant to Division of Neurophysiology, Instituto “C. E&able” (Uruguay) and by DGICYT (Spain) grant to W.B. Many thanks are due to Drs 0.
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Macadar, 0. Trujillo-Cenoz and E. Garcia-Austt for their suggestions. REFERENCES
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0300-9629/91$3.00+ 0.00 0 1991Pergamon Press plc
1991
Printed in Great Britain
ELECTRIC ORGAN DISCHARGE FREQUENCY MODULATION EVOKED BY WATER VIBRATION IN GYMNOTUS CARAPO L. C. BARRIO,* A. CAPuTr,t L. CRISPINO~ and W. Btio*$ *Unidad de Neurobiologia Funcional, Neurofisiologia, Instituto Cajal, CSIC, Av. Doctor Arce 37, 28002 Madrid, Spain, Fax: (91) 5854154; thleurofisiologia, Instituto “C. Estable”, Av. Italia 3318; $Dpto. de Fisiologia, Facultad de Medicina, Av. General Flores 2125, Montevideo, Uruguay (Received 2 January 1991)
Abstract-l. The electric organ discharge (EOD) frequency modulations evoked by brief water vibration were analysed in the pulse-type fish Gymnorus carapo. 2. The response consisted of a transient increase of the EOD frequency at short latency (30msec). Response profiles were characteristic of the specimen and relatively independent on stimulus intensity. 3. Conversely, they were dependent on stimulation sequence, showing a rapid decrement along successive stimuli and high temporal discrimination. 4. The brief latencies indicate a relatively simple neural circuit. 5. The response may be an electrolocation enhancement strategy for the detection of moving objects based on “sampling” the periphery at a higher frequency.
This investigation describes and quantifies, in the South American pulse-type species Gymnotus carapo, the transient EOD accelerations evoked by brief, low amplitude, vibrations transmitted through the water. Stimuli such as water drops and small objects falling into the aquarium or fast movements of a small glass rod close to the fish elicited the response. This “reflex” may also be an electrolocation enhancement strategy for detection of rapidly moving objects or may be used to signal novel stimuli to animals of the same species.
INTRODUCTION Much evidence is available on the behavioral meaning of short-term modulations of the electric organ discharge (EOD) frequency in wave-type weakly elec-
tric fish species, but less is known about pulse-type fish (for reviews, see, e.g. Heihgenberg, 1986; Hopkins, 1988). Short-term EOD modulations are either used to enhance the fish’s ability to electrolocate, or as social communication signal (e.g. Baker, 1980; Bastian, 1981, 1986~; Bell and Szabo, 1986; Black-Cleworth, 1970; Bullock et nl., 1961, 1972; Heiligenberg, 1973, 1974, 1986; Hopkins, 1988; Westby, 1974, 1975). Electrolocation consists in object detection by actively sensing distortions of the electric field of the fish’s own EOD (e.g. Bastian, 1986~; Bullock et al., 1961; Carr and Maler, 1986; Fessard and Szabo, 1961; Heiligenberg, 1987). Electrolocation ability may be enhanced by changing the EOD frequency. The best understood electrolocation enhancement strategy is the jamming avoidance response which occurs when two fish emitting similar EODs interfere (e.g. Baker, 1980, 1981; Bullock et al., 1972; Dye, 1987; Heiligenberg, 1974, 1986). Less understood are EOD accelerations occurring in certain species when they begin to swim, or when presented with unexpected stimuli in the form of “startle or novelty responses” (e.g. Dye, 1987; Hagedorn, 1986; Hopkins, 1988; Grau and Bastian, 1986). More stereotyped, transient, EOD accelerations, with unknown functional meaning, are evoked by vibration and sound (e.g. Kramer et al., 1981; Lissman, 1958). SAddress all correspondence to: Dr Washington
MATERIALS AND
Buxio, Unidad de Neurobiologia Funcional, Neurofisiologia, Instituto Cajal, Av. Dr. Arce 37, 28002 Madrid, Spain. Telephone: (341) 585-4115, Fax: (341) 585-4154.
METHODS
Animals (7-12-cm long) were gathered the same day in late May from a lake in the south-east of Uruguay (Laguna de1 Sauce, Departamento de Maldonado). They were classified as Gymnotus carapo both by their external phenotypic characteristics and head-to-tail multiphasic EOD waveform (e.g. Trujillo-Cenoz et al., 1984; Caputi et al. 1989). Each animal (N = 5) was placed in a cylindrical 10-l aquarium at room temperature (19-21°C) for l-3 weeks before experiments. Figure 1 shows a diagram of the recording-stimulating set-up. A small 20 x 30 cm opaque plastic tank, filled to about 7cm high was used. The fish was placed inside a 2.5 cm diameter nylon mesh tube (mesh size about 2.5 mm) which was adjusted in length to about 1 cm longer than the fish to restrain its movements. The tube had carbon electrodes (from 1.5 V batteries) at both ends connected to a capacity-coupled (0.1 set time constant) preamplifier to record the EOD (P9 in Fig. 1). Recordings were of constant amplitude and waveform (Fig. 2Al). The EOD was displayed on an oscilloscope (CR0 in Fig. 1) and recorded on a stereo audio cassette tape (30 Hz to 12 kHz bandwidth) together with synchronization pulses from a pulse generator. Regular single or barrages of brief (I-1Omsec) pulses (Fig. 2A3) from the generator were fed at different rates to a small speaker which had a glass pipette (I .6 mm diameter) glued to the center of its diaphragm (Fig. 1). The pipette tip
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EXPERIMENTAL t
SETUP
.--. LOUDSPEAKER
Fig. 1. Diagram of stimulating and recording set-up. was occluded with wax. Water displacement stimulus waveforms were monitored (Fig. 2A2), but not tape recorded, with an uncalibrated home-made hydrophone placed inside the mesh tube.. They usually consisted of several rapidly decaying waves, at frequencies between about 125.0 and 250.0 Hz, with overall stimulus durations which lasted up to 20 msec, but usually ended with about 10 mscc. The delay from stimulus pulse on to water displacement onset was variable (2-10 msec) and depended on pulse waveform and polarity. The glass pipette moved vertically about 200 to IMO~m, as measured with long duration pulses under a dissecting microscope. Its tip was placed about 2-4cm above the animal’s head (Fig. 1). Stimuli were also delivered locked 1 to 1 at a fixed delay or phase (4) from EODs by synchronizing the pulse generator with the EOD at different delays (FIXED 4 in Fig. 1). Phase was calculated by adding the pulse generator to the water displacement delays. Animals were left to adapt to the experimental environment in
A
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constant artificial incandescent light for about 1 hr before stimulation and recording were performed. Only fish which remained relatively motionless and displayed a very regular EOD were used. This situation will be termed “control”. Stimuli never evoked overt movement reactions. Data was processed off-line by playing back cassettes in a PDP-I1 computer. The computer displayed inter-EOD interval (I) durations sequentially with 512 successive I (except in Fig. 6 where 1024 intervals were plotted) called here interval plots (IP) (Fig. 2C). It calculated instantaneous frequency vs time plots and averages (Fig. 2Dl), either with 128 or 256 successive responses, of several of these plots (FPAs) and standard deviation vs time plots for FPAs (Fig. 2D2) (e.g. Barrio and Butio, 1990). Averages were calculated after a 2-3-min stimulation period to elimlnate response variation at stimulation on (see Results). InterEOD intervals in FPs were measured with IOO~sec accuracy. EODs, stimulus pulses and water displacement
r-l
E?D
30-l
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OI EOD NUMBER
‘zonis
Fig. 2. Stimulus and response characteristics. A: (1) Electric organ discharge EOD (head to tail) and superimposed instantaneous interval plot (IP); (2) water vibration; (3) pulse fed to stimulator. The inter-EOD interval (I) and the phase and cophase (4 and 0, respectively) are indicated. B: Single EOD, and C: IP during control and at stimulus on. Interrupted line indicates the baseline inter-EOD interval. D: (1) Average instantaneous frequency plot (AFP); (2) standard deviation. Vertical arrows indicates stimulus on, as in all other figures. Interrupted line indicates baseline in record 2.
Vibration-evoked EOD modulation waveforms were plotted on paper with a digital oscilloscope XY plotter system. RESULTS
In control conditions fish displayed regular EOD with mean frequencies which in different animals varied between 33.5 and 45.0 Hz, with coefficient of variation of inter-EOD intervals ~0.008, and peakto-peak amplitudes between about 20 and 40 mV. The response to brief water vibrations consisted of a transient increase of the EOD frequency evoked after a brief delay (about 30msec). Responses showed a rapid rising phase peaking at about 200 msec and a longer (about 1.2 set) recovery phase. They were characteristic of the specimen and were highly reproducible and relatively independent on stimulus intensity in a given fish. Conversely, they were highly dependent on stimulation sequence, showing a rapid decrement along successive stimuli and high temporal discrimination between individual stimuli. Figure 2A1, illustrates the rhythmic discharge and Fig. 2B, the filtered recording of the multiphasic head to tail EOD (cJ Trujillo-Cenoz et al., 1984). Figure 2A2 shows the water displacement waveforms, and Fig. 2A3, the stimulus pulse records. The IP superimposed on record Al, shows the characteristic response consisting of a rapid shortening of I durations (i.e. EOD acceleration) with a minimum interval (or peak response) which was reached in about six EODs (close to 125 msec). The I decrease at the peak of the response was about 4msec from the close to 24.5 msec control or baseline mean inter-EOD interval (i.e. a decrease of about 16%). The IP in Fig. 2C, shows control conditions with a baseline mean I value of about 26 msec or 37.0 Hz, and the effects of regular stimulation of 0.4/set in another fish. The on response was largest (as in all other cases), peaking at about 9 EODs (peak latency about 230msec). The I value at the peak was 18.9 msec or 53.0 Hz, a close to 73% decrease from the baseline I, or a 16.0 Hz increase (Af= 16.0 Hz) from the baseline EOD frequency. Subsequent I increased in duration (i.e. the EOD decelerated) gradually, relaxing towards the baseline (interrupted line). Baseline values were not completely recovered because successive responses occurred before the total relaxation of the preceding response. Successive responses decreased gradually in amplitude and eventually stabilized with about 10 to 15 stimuli at an amplitude which depended markedly on stimulus rate (see below). This relaxation-which will be called attenuation-also increased gradually, although control values were not completely recovered at this stimulus rate. Figure 2Dl shows the FPA obtained in response to single pulse stimulation at 0.2/set. The response consisted of a rapid EOD acceleration followed by a gradual deceleration towards the baseline (interrupted line). The brief latency to response on and to the peak should be highlighted. The gradual relaxation lasted about 1.5 sec. The baseline EOD frequency was 44.5 Hz and the peak was 54 Hz, a 9.5 Hz increase (Af= 9.5 Hz). The standard deviation vs time plot in Fig. 2D2, shows an irregular profile with small values throughout, and a small
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peak at the EOD acceleration, indicating that the responses evoked by each stimulus were similar to the mean, well defined temporally, and highly predictable in waveform. Therefore, averages were good estimates of individual responses. Figure 3 shows stabilized responses and stimulus rate effects. The IP in Fig. 3A, illustrates successive responses evoked with pulses at O.S/sec. They consisted of rapid accelerations followed by gradual relaxations. The FPAs (N = 128) show the same responses at two different sweep speeds (2 and 3, respectively). They consisted of an initial acceleration which peaked at latencies of about 80msec. The water vibration on, to averaged response latency was measured in FPAs in all fish; the lowest value was 15 msec with a mean value of 30msec. The EOD frequency at the peak in Fig. 3 was 44.0, a 4.0 Hz increase (Af = 4.0 Hz) from the mean 40.0 Hz baseline. The initial acceleration was followed by a rapid deceleration and a second smaller peak which then relaxed gradually. Responses evoked by single pulses had durations between 600msec and 2 set (mean 1200 msec), as estimated from FPAs in all the fish. Response duration was little affected by stimulus intensity (data not shown). The IP in Fig. 3Bl and the FPAs (N = 254) in Fig. 3B2 and B3, respectively show that responses were smaller than in A (Af= 2.5 Hz) with stimuli at 2.0/set, but the response profile was essentially identical. Figure 3C shows the Afreduction as a function of stimulus rate. In this specimen and for unknown reasons, there was also a reduction of the baseline from 40.0 to 38.5 Hz in A and B, respectively. Figure 4 shows responses evoked by paired pulses at l/set in the same fish used in Fig. 3. The IPs in A, illustrate the relatively constant responses evoked with pulses at 10, 20 and 40 msec delays (1, 2 and 3, respectively); IP A4 shows two clearly separate peaks with interpulse delays of 320 msec. The corresponding FPAs are shown at two different sweep speeds in Bl-4 and Cl-4, respectively. Either a single peak 1, a peak with two humps 2, or two separate peaks 3 and 4, were evoked with pulses at 10,20,40 and 320 msec, respectively (arrows indicate the second response components). Note also the longer lasting plateaux in records C2 and C3. The frequency difference between the first and second peaks (S lS2) vs interpulse delay is shown in Fig. 4D. The Sl-S2 difference first increased with increasing delays, up to delays of about 40msec, and then decreased. Results reveal that only when the stimulus became physically two different events (220 msec; see Materials and Methods) was the animal able to discriminate the difference. Figure 5A and B compares single pulse effects with those evoked by pulse barrages (rate lO/sec, duration 1.5 set), respectively, presented at about 0.6/set. The IP shows somewhat larger I reductions in Bl and Al. The mean baseline EOD frequency was 38.5 Hz. The FPAs evoked by single pulses in A2 had a more complex profile in this fish. The response consisted of a fast acceleration (1) an initial peak (Af = 5.5 Hz) at latencies of about 60 msec (2) a rapid deceleration (3) reaching a constant frequency plateau at about 40.5 Hz (4) and a gradual relaxation to baseline values (5). The response profile was essentially
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01
EOD NUMBER
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STIMULUS RATE (impulses/s)
Fig. 3. Stimulus rate effects. A, B: Stimulation at 0.5 and 2 Hz, respectively. (1) IP, and (2, 3) AFPs at two different sweep speeds. C: Peak EOD frequency minus baseline (Af ) vs stimuius rate plot.
identical in B2, but response durations increased at the expense of component 3 and also of the plateau 4. Both the peak 1 and the plateau 4 were higher in B (Af = 6.5 Hz and 41 .OHz, respectively). Note also that there was no EOD frequency modulation associated with individual stimuli in B. It should be understood that response profiles were characteristic of the individual fish, and did not change much with stimulus parameters (except notably for the above described effects). Profiles were usually simple, as those in Figs 2 and 3 (three out of five fish) and sometimes complex (e.g. Figs 4 and 5). The IPs in Fig. 6 show the effects of 1 to 1 phase locked stimulation (i.e. FIXED 4; see Fig. 1 and Materials and Methods) with Cpat 6, 12 and 24 msec (A, B and C, respectively). Phase is the time elapsed between the EOD and the next water vibration on.
delay was 6 msec, and the calculated 4 are indicated by the horizontal arrows. Note that 4 briefer than 6 msec could not be explored. The baseline I was 38 msec or about 28.0Hz. The on response was essentially identical in the three records, indicating that it was 4 independent. The response had a simple profile consisting of a rapid I duration drop to about 28 msec (i.e. and EOD acceleration to close to 35.5 Hz) followed by a gradual relaxation. Since d, was fixed, the acceleration occurred at the expense of a shortening of the time elapsed from the stimulus on to the next EOD or cophase (0). The initial response did not return to baseline values (interrupted line) because in all three cases there was a second acceleration (asterisks) before complete relaxation of the initial response (there was also a third peak in B; arrow). The second acceleration was
The water vibration
Vibration-evoked
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Fig. 4. Paired pulse stimulation. A: (l-4) IPs with stimulation at different rates. B, C: FPAs at two different sweep speeds (arrows indicates “second” response). (l-4) as in A. D: Plot of the difference between the first and second responses (SlS2) vs interstimulus interval.
longer lasting in C. It started more gradually, stabilized at about 65% of the baseline I, lasted about 15 set, and finally relaxed gradually. Note that in C, with the acceleration the EOD tended to occur simultaneously “in synchrony” with the water vibration, We never observed off responses with phaselocked stimulation (Fig. 6) nor with long-lasting pulse barrages (data not shown).
DISCUSSION
Objectives of this investigation were to: (i) provide a quantitative de~ription of the short-term EOD modulations evoked by water vibration, (ii) compare the results with previous analysis of EOD frequency modulations evoked in other experimental conditions, (iii) suggest mechanisms,
I
EOD NUMBER
*\ 13 4 I 1.
i5
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Fig. 5. Pulse barrage effects. A: Single pulse stimulation, and B: barrage, (1) IP and (2) FPAs. Note complex response profiles with labeled components (l-5) in records 2. Horizontal line indicates stimulus and off is shown by second arrow, as in subsequent figure.
L. C. BARRIOet al.
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12..* 50 ms
1
Fig. 6. Fixed phase (4) stimulation. IPs at increasing 4 values from A to C. Horizontal arrows indicate timing of individual stimuli, and asterisks the “second” response component. The open arrow in B, indicates a third response.
implications and biological relevance of the observed behaviors. The EOD frequency was transiently increased in a stereotyped and highly predictable manner by water vibrations. The response showed extremely welldefined time relationship with the stimulus. Although responses evoked by successive stimuli were highly consistent and relatively insensitive to intensity in a given specimen, three different response profiles, shown in Figs 2D, 3A3, and 5A2 were observed in different fish. Only five animals were used in the experiments, but the different response profiles in each fish suggest strongly that they were characteristic of the individual. Of interest were the brief response latencies which indicate that a relatively simple neural circuit underlies the EOD acceleration evoked by water vibration. Considering a pacemaker to EOD conduction time of about 5 msec (Caputi, Silva and Macadar, in preparation) results indicate that an extremely brief “processing” time is necessary for the response. Brief latencies revealed an efficient strategy in terms of a possible electrolocation enhancement since the frequency shift started within about one inter-EOD interval and peaked very rapidly in only 5 to 10 EODs after stimulus on. Although on responses were similar in a given fish, the modulation depth Af was highly dependent on past stimulation history. Indeed, there was attenuation along successive stimuli (Fig. 2). This attenuation effect was present at low rates of stimulation and was enhanced when the stimulation rate was increased (Fig. 3). Rapid, stimulus rate-dependent functional
response decrements suggests that the system favors the detection of unexpected stimuli. Stimulus barrages at high rate caused the EOD frequency to increase and subsequently to yield rapidly to less than 50% of the on response at the end of the barrage (Fig. 5). Attenuation was present without frequency modulation of the EOD evoked by individual stimuli in the barrage. Therefore, the reduction should reflect a neural process rather than result from mechanical summation at pre-receptor levels since the temporal resolution of the system probed with paired stimuli (Fig. 4) was about five times greater than that necessary to discriminate individual pulses in the barrage (e.g. 20 msec vs 100 msec). Another response feature that depended on past stimulation was the amplitude variation of the second response evoked by stimulus pairs. Responses first increased (up to about 50 msec) and then decreased with interpulse delay (Fig. 4). The final decrease may reflect what we have termed stimulus attenuation, and is clearly a different process than the initial increase. The functional role of the brief initial period of response enhancement could be to increase response probability with a specific timing of the stimulus thus favoring responses at short intervals (< 50 msec). As in other systems (e.g. Bufio et al., 1981) both the initial response enhancement and the subsequent attenuation may be considered as mechanisms which increase the detectability of unexpected stimuli. The novelty responses evoked by electrosensory stimuli (e.g. Westby, 1974, 1975) and other sensory modalities (Dye, 1987; Hagedorn, 1986; Hopkins,
Vibration-evoked
1988; Lissman, 1958; Zelick, personal communication) are characteristic of pulse-type gymnotids. It has been proposed that the correlation between increased motor activity and EOD acceleration which occurs in most pulse-type Gymnotiform fish (BlackCleworth, 1970; Hagedom, 1986) might be a clue to explain the ability of these fish to respond with reflex EOD accelerations to stimulations of most sensory modalities (e.g. Kramer et al., 1981). In such type of fish a connection between motor centers and the electromotor command system probably still exists, including the nucleous magnocellularis mesencephaly (e.g. Finger, 1986; Retelyi and Szabo, 1973; Sas and Maler, 1983). Therefore, any stimulus which modifies motor activation can evoke EOD acceleration via those motor command centers. Among such stimuli those that activate the lateral line mechanosensory system which conveys vibratory information are perhaps the most important. The similarities between the responses described here and those evoked by sound, light and touch (e.g. Black-Cleworth, 1970; Kramer et al., 1981; Zelick, personal communication) are in favor of the above view, despite the fact that sound stimuli show little or no attenuation (Kramer et al., 1981). The differences suggest that attenuation could take place at earlier processing stages for vibratory information, as occurs in the electrosensory system. The anatomical parallelism of electrosensory and lateral line systems (Bell and Szabo, 1986; Carr and Maler, 1986; Finger, 1986) suggest that the same mechanisms of gain control and electric novelty detection (Bastian, 1986a,b,c; Bratton and Bastian, 1990; Grau and Bastian, 1986) could also be present in the central processing of vibratory information. Pulse-type fish may actively electrolocate only within a brief time window provided by the “standing” electric wave generated by their own EOD. Therefore, vibration-dependent EOD accelerations may be interpreted as an electrolocation enhancement strategy based on “sampling” the periphery at a higher frequency. The increased EOD frequency would improve the system’s+ temporal resolution. Therefore, the vibration-evoked EOD acceleration would increase the probability of correctly electrolocating the source of vibration, and more important perhaps, of detecting its movement direction. The response may also be used to signal novel stimuli to animals of the same species. The effects of fixed phase stimulation are difficult to interpret (e.g. Westby, 1975). However, it could also represent an electrolocation enhancement strategy which function either by synchronizing the EOD with certain types of stereotyped movements and their subsequent mechanical effects, as perhaps occurs in startle and escape responses, or to synchronize the EOD with the movement of the vibrating source to emit EODs during its movement. A similar strategy has been shown in other neural pacemakers (But50 et al., 1984), where the stimulus-response synchronization may be related to the capacity to tune in and detect periodic signals buried in noise. Acknowledgements-Work supported by a Commission of European Communities grant to Division of Neurophysiology, Instituto “C. E&able” (Uruguay) and by DGICYT (Spain) grant to W.B. Many thanks are due to Drs 0.
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Macadar, 0. Trujillo-Cenoz and E. Garcia-Austt for their suggestions. REFERENCES
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