2412
Introduction
Agonistic behaviors that regulate conflict situations between
conspecifics have shaped sociality across evolution (Lorenz, 1963;
King, 1973). Conflicts arise because animals compete for different
resources (territory, food, mates, breeding sites, etc.) and they are
solved when one individual keeps the resource in struggle
(dominant) and the other loses it (subordinate). Though the
resources individuals compete for may be different and the
behavioral patterns involved may be extremely diverse, agonistic
encounters always follow the same phases (evaluation, contest and
post-conflict resolution). Conflicts may be solved without escalated
contests, but animals usually have to fight to elucidate which will
become the winner or the loser. Therefore, aggression, defined as
an overt behavior that leads to displacing, dominating or harming
another individual (Nelson, 2006), is part of the contest phase of
agonistic encounters. Given the diversity of aggressive behaviors
and the variety of contexts in which aggression is expressed, it has
not been possible to reach a general consensus in the definition of
aggression and its classification, though several authors have
provided useful theoretical frameworks in this concern (Moyer,
1968; Brain, 1979; Wingfield et al., 2006). Within the agonistic
context, individuals can aggressively compete either for space or
for a mate, or aggressively establish hierarchies in a flock. Thus,
depending on the resources individuals compete for and the
motivation towards combat, at least three distinctive types of
aggression can be observed during agonistic encounters: territorial
aggression, reproduction-related aggression and rank-related
aggression (Wingfield et al., 2006). The type or types of aggression
displayed by one species are correlated with its social structure. For
example, it is not likely for gregarious species to display exclusive
territorial aggression, nor for solitary species to display rank-related
aggression. However, it is not always easy to discern between types
of aggression, and to obtain model systems to test clear-cut
examples of a distinctive type of aggression. Besides, both in
natural performing animals and in laboratory settings, different
types of aggression often intermingle, resulting, for example, in
territorial aggression only observed between males during breeding
while they are competing for mates, or rank-related aggression
established by territory defense (Brown, 1964).
Several brain areas are known to control aggression, though it
has not been possible to dissect a fixed neural circuit responsible
for aggressive behavior. Rather, following Newman’s hypothesis
(Newman, 1999), we interpret aggressive behaviors as emergent
properties of a complex social behavior network (SBN) that
includes the medial preoptic area, lateral septum, anterior
hypothalamus, ventromedial hypothalamus, periaqueductal gray,
Summary
Agonistic behavior has shaped sociality across evolution. Though extremely diverse in types of displays and timing, agonistic
encounters always follow the same conserved phases (evaluation, contest and post-resolution) and depend on homologous
neural circuits modulated by the same neuroendocrine mediators across vertebrates. Among neuromodulators, serotonin (5-HT)
is the main inhibitor of aggression, and arginine vasotocin (AVT) underlies sexual, individual and social context differences in
behavior across vertebrate taxa. We aim to demonstrate that a distinct spatio-temporal pattern of activation of the social behavior
network characterizes each type of aggression by exploring its modulation by both the 5-HT and AVT systems. We analyze the
neuromodulation of aggression between the intermale reproduction-related aggression displayed by the gregarious
Brachyhypopomus gauderio and the non-breeding intrasexual and intersexual territorial aggression displayed by the solitary
Gymnotus omarorum. Differences in the telencephalic activity of 5-HT between species were paralleled by a differential
serotonergic modulation through 1A receptors that inhibited aggression in the territorial aggression of G. omarorum but not in the
reproduction-related aggression of B. gauderio. AVT injection increased the motivation towards aggression in the territorial
aggression of G. omarorum but not in the reproduction-related aggression of B. gauderio, whereas the electric submission and
dominance observed in G. omarorum and B. gauderio, respectively, were both AVT-dependent in a distinctive way. The
advantages of our model species allowed us to identify precise target areas and mechanisms of the neuromodulation of two types
of aggression that may represent more general and conserved strategies of the control of social behavior among vertebrates.
Key words: territorial aggression, reproduction-related aggression, serotonin, AVT, social behavior network, Gymnotus omarorum,
Brachyhypopomus gauderio.
Received 25 October 2012; Accepted 31 January 2013
The Journal of Experimental Biology 216, 2412-2420
© 2013. Published by The Company of Biologists Ltd
doi:10.1242/jeb.082180
REVIEW
Neuromodulation of the agonistic behavior in two species of weakly electric fish that
display different types of aggression
Ana C. Silva
1,2,
*, Rossana Perrone
1
, Lucía Zubizarreta
1
, Gervasio Batista
1
and Philip K. Stoddard
3
1
Unidad Bases Neurales de la Conducta, Instituto de Investigaciones Biológicas Clemente Estable, Montevideo 11600, Uruguay,
2
Laboratorio de Neurociencias, Facultad de Ciencias, Universidad de la Republica, Montevideo 11400, Uruguay and
3
Department of
Biological Sciences, Florida International University, Miami, FL 33199, USA
*Author for correspondence (asilva@iibce.edu.uy)
THE JOURNAL OF EXPERIMENTAL BIOLOGY