Post on 04-Feb-2022
In memorial to Larry Bingham who died from cancer prior to the publication of1
this paper.
THE EFFECTS OF FOREBRAIN ABLATION ON AGGRESSIVEDISPLAY IN MALE SIAMESE FIGHTING FISH (BETTA SPLENDENS)
THOMAS E. VAN CANTFORTDepartment of Psychology
Fayetteville State University
AND
LARRY R. BINGHAM1
Department of PsychologySan Francisco State University
Paper presented at The First Annual Sandhills Regional Psychology Conference,Fayetteville, NC, March 23, 2002
Please consult the authors before citing any portion of this manuscript.
2 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
The Effects of Forebrain Ablation on AggressiveDisplay in Male Siamese Fighting Fish (Betta Splendens)
ABSTRACTMany investigators have found that the telencephalon in various teleosts plays animportant role in behavior, some concluding that the major role is one of behavioralorganization and others emphasizing its function as one of arousal or facilitation. This study explores the role of the forebrain in aggressive display in male Siamesefighting fish, Betta splendens. Fourteen ablated fish were compared to 14 intact and14 sham operated fish on 10 different behaviors elicited either by a conspecific ormirror stimulus. Ablated fish had longer latencies for fin erection, opercular spreadand air gulps and showed a decrease in frequency of opercular spread comparedto intact and sham operated fish. These results support the hypothesis that theforebrain does not directly mediate specific behavior but serves rather in afacilitatory capacity of arousal and in the integration of the information required toelicit aggressive display behavior.
INTRODUCTION
For many years the early neuroanatomists had categorized the teleost (bony
skeleton fish) forebrain as an olfactory mechanism because of its close relationship with the
olfactory mucosa and its apparent isolation from other sensory systems. Aronson (1963),
however determined that the greater part of the teleost pallium is devoid of secondary
olfactory fibers. This finding has been confirmed by Nieuwenhuys (1970) and is consistent
with the conclusion of the many experimentalists who have found that the forebrain has
multiple functions other than olfaction (Frank, Flood, & Overmier, 1972; Gordon, 1979).
Many investigators (Gordon, 1979; Overmier & Savage, 1974) have found that the
telencephalon in various teleosts plays an important role in behavior, some concluding that
the major role is one of behavioral organization and others (Aronson, 1967) emphasizing
its function as one of arousal or facilitation rather than behavioral organization. Some of
3 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
the nonolfactory functions attributed to the teleost forebrain such as deficits in schooling
behavior, active and passive avoidance (Gordon, 1979; Overmier & Savage, 1974), and
interference with reproductive behavior have been reviewed by Ten Cate (1935), Healy
(1957), Segaar (1965), and Aronson (1967).
In most of the experiments reported in the literature, ablation of parts or all of the
forebrain did not result in the loss of any behaviors. Rather, it resulted in changes in the
frequency of occurrence of certain behavioral components or in a loss of efficiency, or
synchrony.
Aggressive behaviors have been implicated as having a specific forebrain mediated
function in the initiation of fighting (Noble & Borne, 1941). It was found that following
partial or complete destruction of the forebrain in the jewel fish, the swordtail, and the
danio, there was a longer latency in fight initiation but that when fighting did occur, it was
just as vigorous as in intact fish. This led Noble and Borne to conclude that actual fighting
behavior must be organized in lower brain levels while the forebrain facilitates initiation
of the behavior. Similar results were obtained by Schönherr (1955) who studied aggressive
behavior in the three-spined stickleback. Decrements in aggressive behavior in this species
were also reported by Segaar (1961) and Segaar and Nieuwenhuys (1963). Hale (1956) also
reported a marked decrease in aggressive behavior following forebrain ablation in the sun
fish.
Shapiro, Schuckman, Sussman, and Tucker (1974) observed that telencephalic lesions
in Siamese fighting fish (Betta splendens)decreased the frequency of gill cover response to
4 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
both conspecific stimulus and mirror stimulus. The mean duration of the gill cover
response was not affected by lesioning and did not decrease (habituate) with repeated
stimulus presentation. Shapiro, et al. concluded that behavioral changes may be related
to the extent of the lesion. Since Betta splendens with telencephalic lesions still showed
aggressive displays the centers that control gill cover erection may be located in the
midbrain or hindbrain.
Gorlick (1990) identified parts of the presumptive neural pathway for gill cover
erection in Siamese fighting fish. Motor, motor integration, and sensory areas were
identified in the medulla and mesencephalon. Dilator opericuli motor neurons appeared
to receive all three types of inputs. Gorlick, concluded that connections between motor
areas, and between parts of the reticular formation, may coordinate the performance of gill
cover erection with other behavioral patterns used during aggressive display. Ma (1995)
reported that the opercular dilator muscle consists of three parts: a deep belly and two
superficial bellies. Innervation of this muscle is derived from the maxillary division of the
trigeminal nerve; all three portions are innervated by axons from the same fascicle. Direct
stimulation demonstrates that all bellies can mediate opercular extension. In addition,
Hollis and Overmier (1982) explored the effects of telencephalon ablation on instrumental
learning and Pavlovian conditioning in Betta splendens. They reported that unconditioned
fin erection, gill erection and tail beating to mirror UCS were less frequent in ablates than
in normals or shams. In summary, these various studies seem to show that aggressive
behavior in teleost fish is organized in lower centers, while the forebrain facilitates
5 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
responses to the stimuli and integrates the information required to elicit the behavior.
Hale (1956) reported that forebrain ablation reduces aggressive behavior in some
teleost no one has studied the effects of forebrain ablation on aggressive behaviors in
Siamese fighting fish (Betta splendens) towards it’s conspecific (another male Siamese
fighting fish). Aggressive display responses in the male Betta splendens have been
extensively described (Braddock & Braddock, 1955; Simpson, 1968) and include approach;
extension of the gill covers and gill membranes; erection of the dorsal, ventral, medial, and
caudal fins; intense deepening of body and fin color; and the characteristic orientation and
undulatory movements. The aggressive display can be elicited by a conspecific male or
one’s own mirror image ( Figler 1972; Johnson & Johnson, 1973; Lissman, 1933 Meliska,
Meliska & Peeks, 1980).
A variety of factors appears to influence aggressive display response in the male
Betta splendens. Siamese fighting fish shown a facing posture model (used mainly in
aggressive contexts) are more aggressive than Siamese fighting fish shown a broadside
posture model (used in many social context) (Halperin, Giri, & Dunham, 1997). Social
isolation also plays a role in aggressive display response of male Betta splendens. Socially
isolated Siamese fighting fish showed weaker aggressive display to the first model seen
after social isolation in a series of novel models than nonisolate. The aggressive display
was progressively weaker the longer the social isolation. Whereas, isolates displayed more
strongly than nonisolates to the last model of the series, and display intensity became
monotonically stronger with longer social isolation (Halperin, Dunham & Ye, 1992).
6 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
Halperin and Dunham (1994) have also demonstrated that social overstimulation reduces
subsequent aggression in male Betta splendens.
There has been some question about the strengths of conspecific versus mirror
eliciting stimuli. For example, Johnson and Johnson (1973) found that a mirror stimulus
elicited greater responses than did a conspecific stimulus. Figler (1972) reported that
unhabituated male Betta splendens was the strongest releaser of aggressive display in
Siamese fighting fish, followed successively by mirror, habituated male, and model.
Meliska, Meliska, and Peeks (1980) identified two groups of Betta splendens, those that
responded with high levels of reactivity to a mirror or those that responded with low
reactivity to a mirror. Subjects that displayed at the mirror for short durations (low
reactivity) were matched for combat with either other short-duration displayers (the Short-
Short group), or long-duration (high reactivity) displayers (the Long-Short group). In
combat, Short-Short pairs fought less intensely than Long-Short pairs; but within Long-
Short pairs, Short- and Long-duration displayers did not differ in combat vigor.
Correlations between combat behavior and precombat mirror display measures
tended to be positive, but were mostly small and nonsignificant. Correlations with
postcombat mirror displays were greater. These results imply that mirror-elicited threat
behaviors provide a partial predictor of actual combat aggression in Siamese fighting fish
(Meliska, Meliska, & Peeks, 1980). Some of the differences found in the above studies may
have been due to the different experimental paradigm or utilization of different response
measures.
7 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
The purpose of this study was to examine the effects of forebrain ablation on the
aggressive display in male Siamese fighting fish. A mirror and conspecific stimuli were
utilized, and the effects of ablation on several different measures of aggressive display
involving latency, frequency, and duration of behavior were compared.
METHODSSubjects
Sixty adult male Betta splendens were used. The subjects had color variation as was
expected and is common even within the same brood. Figler (1972) reported color
variation is not a factor in the elicitation of aggressive responses. Subjects were housed in
specially constructed plexiglass aquaria such that each fish was chemically and visually
isolated from all other fishes. The room that housed these aquaria had a controlled light-
dark cycle, lights on from 08:00 hours to 20:00 hours.
Surgery
Subjects were anesthetized in Sandos MS 222 (m-Aminobenzoic acid ethyl ester-
Methansulfate salt), 1 part to 4 parts water, and then placed in the stereotaxic apparatus,
the scales were scrapped away and a medial incision approximately 2 mm corresponding
with the cranial and caudal limits of the eye was made. A transverse incision was made
approximately 3 mm corresponding with the caudal limits of the eye and at 15 degrees to
the coronal plane of the subjects and about 2 mm deep to sever the forebrain from the
midbrain. The forebrain was then aspirated by means of positively applied suction from
a water aspirator. Sham operated fish were treated in the same fashion except their brains
8 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
were left intact, only the skull incisions were made.
Apparatus
The test aquaria had a clear plexiglass partition in which one compartment housed
the stimulus and the other compartment housed the experimental fish. Recording of
latencies, frequencies and durations of behaviors was accomplished with a Rustrack-4-
channel event recorder.
Procedures
Subjects were randomly assigned to one of three experimental groups; ablated
(N=30), sham operated (N=15), and intact (N=15). The subjects from each experimental
group were randomly assigned to one of two stimulus group; mirror stimulus or
conspecific stimulus and observed for 10 minutes.
Table 1 lists the behavioral components of the subject’s threat display that were
simultaneously recorded during the ten minute observation period. Also included in these
Table 1. Measurement and definition of behaviors
Latency of fin erection (LFE) latency in seconds to caudal fin erectionLatency of opercular spread (LOS) latency in seconds to opercular spreadLatency of air gulps (LAG) latency in seconds to air gulpsFrequency of fin erection (FFE) number of times the caudal fin was erect during the sessionFrequency of opercular spread (FOS) number of times the operculum was spread during
the sessionFrequency of air gulps (FAG) number of times the fish gulped air during the sessionDuration of fin erection (DFE) total time in seconds that the caudal fin was erect during the
sessionDuration of opercular spread (DOS) total time in seconds that the operculum was spread
during the session
measurements were two derived scores. Mean duration of fin erection, mean time in
seconds that the caudal fin was erected during each occurrence in a session. The mean time
9 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
was obtained by dividing total duration by frequency of occurrence in a session. And
mean duration of opecular spread, mean time in seconds that the operculum was during
each occurrence in a session. The mean time was obtained by dividing total duration by
frequency of occurrence in a session.
At the end of testing the subjects were sacrificed in the anesthesia solution for
approximately thirty minutes and then placed in a 10 percent formalin solution for 48
hours. The fish were then placed in the stereotaxic apparatus, their skulls opened and the
brains photographed to determine the extent of ablation.
RESULTS
After the surgery, 14 ablated Betta splendens in their home aquaria exhibited
behaviors that were indistinguishable from the behaviors of the control fish. That is, their
fleeing from the net, location and consumption of food, and general locomotor activity
were equal to the intact and sham operated fish. Those ablated fish that showed any gross
sensory or motor impairment were excluded from this study. The results from this study
were obtained from those 14 ablated fish, 14 randomly selected sham operated, and 14
randomly selected intact fish.
A two-way analysis of variance (see Table 2) was used to determine the effects of
surgery (ablation, sham operated, and intact) and eliciting stimuli (conspecific vs mirror)
between the groups. Removal of the telencephalon in male Siamese fighting fish resulted
in significantly greater latencies to respond as compared with intact and sham operated
control groups on fin erection, opercular spread, and air gulps (figures 1 - 3).
10 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
Table 2. Summary table for two-way analysis of variance.
Effect LFE LOS LAG FFE FOSSurgery df 2/36 2/36 2/36 2/36 2/36
F 5.04 3.90 10.77 1.47 10.71 p .05 .05 .01 NS .01
Stimulus df 1/36 1/36 1/36 1/36 1/36 F 1.44 9.61 0.25 0.18 3.23 p NS .01 NS NS NS
Surgery df 2/36 2/36 2/36 2/36 2/36 X F 0.17 1.12 0.81 0.86 1.09Stimulus p NS NS NS NS NS
Effect FAG DFE DOS MDFE MDOSSurgery df 2/36 2/36 2/36 2/36 2/36
F 11.81 17.69 6.10 10.02 0.08 p .01 .01 .05 .01 NS
Stimulus df 1/36 1/36 1/36 1/36 1/36 F 0.65 1.77 2.73 4.80 0.43 p NS NS NS .05 NS
Surgery df 2/36 2/36 2/36 2/36 2/36 X F 0.10 0.11 0.14 0.91 0.22Stimulus p NS NS NS NS NS
F .05 (2/36) = 3.26 F .05 (1/36) = 4.11F .01 (2/36) = 5.25 F .01 (1/36) = 7.40
11 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
Figure 1. Mean latency to fin erection.
Figure 2. Mean latency to opercular spread.
12 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
Figure 3. Mean latency to air gulp
Frequency of air gulp and frequency of opercular spread was significantly greater
in the intact and sham group as compared to the ablated group (figures 4 & 5). The
decrease in the frequency of opercular spread for the ablated group is consistent with the
findings of Shapiro et al. (1974). A two-way analysis of variance shows no significant
difference between ablated and the two other groups on frequency of fin erection (figure
6).
13 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
Figure 4. Mean frequency of opercular spread.
Figure 5. Mean Frequency of air gulp.
14 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
Figure 6. Mean frequency of fin erection.
Duration of fin erection and opercular spread were significantly greater in the intact
and sham groups as compared to the ablated group (figures 7 & 8).
Figure 7. Total duration of fin erection.
15 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
Figure 8. Total duration of opercular spread.
Removal of the forebrain resulted in a significant decrease in mean duration of fin
erection per occurrence and the conspecific stimulus elicited a significantly higher mean
duration of fin erection than that exhibited to the mirror stimulus (figure 9). No significant
difference was found between groups on mean duration of opercular spread (figure 10).
Again the results on mean duration of opercular spread for the ablated group are similar
to the results found in Shapiro et al. (1974) study.
16 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
Figure 9. Mean duration of fin erection per occurrence.
Figure 10. Mean duration of opercular spread per occurrence.
Finally, there was no significant difference on eight of the 10 dependent measures
for the effect of the eliciting stimuli. Latency to opercular spread was consistently longer
for mirror stimulus as compared to conspecific stimulus across ablated, intact and sham
17 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
operated fish.
DISCUSSION
In agreement with other studies, no obvious sensory or motor impairment was
observed in the ablated fish in their home aquaria, and their behavior was
indistinguishable from the behavior of the control fish. That is, fleeing from the net,
location and consumption of food, and general locomotor activity were equal to the intact
and sham operated fish. Therefore, deficits in the ablated fish to be described below could
not be attributed to any gross sensory or motor impairment.
The latency data from this study indicates that the forebrain plays a role in the
initiation of aggressive display, since the ablated group showed significantly higher
latencies on all three dependent measures. The forebrain also seems to facilitate aggressive
display as revealed by the low frequency of opercular spread and low frequency of air gulp
in the ablated group when compared to the intact and sham control groups. This
facilitation is also supported by the duration scores since the ablated fish showed a shorter
total duration on all of the measured components of aggressive display. Interestingly, the
ablated group showed a shorter duration of fin erection despite their somewhat higher
frequencies.
Of the eight dependent measures involving latency, frequency, and duration, the
ablated group differed significantly in seven of these eight comparisons. This strong
concordance among the various responses would indicate a basic underlying deficit
resulting from forebrain lesion, rather than a discrete response impairment. It should also
18 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
be noted that these behaviors, although disrupted, were not eliminated and this is
consistent with earlier findings (Hosch, 1936; Kamrian & Aronson, 1954; Hale, 1956).
Furthermore, the results support the hypothesis of Aronson (1967) that the forebrain
does not directly mediate specific behavior but serves rather in a facilitatory capacity of
arousal and integrates the information required to elicit aggressive display behaviors. This
hypothesis would also fit in with the parallels drawn by many authors between the
anatomical make-up of the teleost forebrain and the limbic system of mammals. In general
terms, the limbic system in mammals is thought of as a nonspecific modulator of behavior
patterns organized in other parts of the brain (Gloor, 1960) and as a regulator of awareness
(Douglas & Pribram, 1966).
Gloor (1960) wrote that the limbic system provides “motivational mechanisms
which normally allow selection of behavior appropriate to a given situation.” Aronson
continues this line of thinking by postulating a neural mechanism whereby reverberating
circuits in the lower centers deteriorate when no longer primed by the forebrain
descending influences.
Deterioration of behavior as a result of forebrain ablation might also be the result
of depletion of a biogenic substance which is normally secreted by the forebrain and which
impinges on lower brain centers. For example, Schildkraut and Kety (1967) suggest that
norepinephrine is a mediator of a nonspecific state of arousal. In addition Kusunoki and
Masai (1966) have found substantial quantities of monoamine oxidase in the olfactory
bulbs, and in certain pallia and subpallial portions of the goldfish brain. The monoamine
19 FOREBRAIN ABLATION IN SIAMESE FIGHT FISH
oxidase in the forebrain may indicate the presence of norepinephrine or other
catecholamines, and ablating the forebrain may disrupt a feedback system involved in a
neurohumoral arousal process.
Ablation studies, in general, remove large portions of the brain to learn what
function that particular part of the brain regulates. In the present study the entire frontal
lobes were removed and we found disruption in the aggressive display of male Siamese
fight fish. It is important to note that there was no loss of any aggressive display behavior,
but the behavior was disorganized. By using discrete lesioning technique we may better
understand the nature of the role that the forebrain plays in the regulation of aggressive
display in the male Siamese fighting fish.
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