C-FOS CHANGES FOLLOWING AN AGGRESSIVE ENCOUNTER IN
FEMALE CALIFORNIA MICE: A SYNTHESIS OF BEHAVIOR,
HORMONE CHANGES AND NEURAL ACTIVITY
E. S. DAVIS* AND C. A. MARLER
Department of Psychology, University of Wisconsin-Madison, Madison,
WI, USA
Abstract—Although there has been growing interest in the
neuroanatomical and physiological mechanisms underlying
aggressive behavior, little work has focused on possible
mechanisms controlling natural plasticity in aggression. In
the current study, we used naturally occurring changes in
aggression level displayed by female Peromyscus californi-
cus across the estrous cycle and parallel changes in c-fos
expression to examine possible brain regions involved in
mediating this plasticity. We found that c-fos expression was
increased in females exposed to a conspecific female in-
truder compared with control females in numerous brain
regions thought to be involved in the control of aggression.
More importantly, we found that c-fos increased in the bed
nucleus of the stria terminalis (BNST) and ventral lateral
septum (LSv) only in the more aggressive, diestrous females,
and not in the less aggressive, proestrous and estrous fe-
males. Conversely, c-fos increased in the medial amygdala
(MeA) across all stages of estrus compared with controls,
suggesting the MeA is not involved in mediating changes in
individual levels of aggression. Moreover, we found correla-
tions between several measures of aggression and c-fos
expression in the BNST and LSv but not the MeA, again
suggesting a role in mediating aggression plasticity for the
former two but not the latter brain region. We further hypoth-
esize that the BNST and the LSv may be involved more
generally in mediating natural changes in aggression, such
as increases often observed after individuals win aggressive
interactions against conspecifics. © 2004 IBRO. Published by
Elsevier Ltd. All rights reserved.
Key words: aggression, c-fos, bed nucleus of the stria
terminalis, lateral septum, plasticity, estrous cycle.
Much of the current research on aggression has con-
cerned the underlying physiological mechanisms, both
hormonal and neural, that control the expression of ag-
gression. From attempts to detail possible neural net-
works involved in aggression (e.g. Delville et al., 2000),
to research on the influence of exogenous steroid abuse
on aggression (DeLeon et al., 2002), researchers have
identified a number of peripheral hormones, neuro-
chemicals and brain regions important to aggression.
However, one important aspect of aggression control
has received little attention to date. That is, the neural
and physiological mechanisms underlying naturally oc-
curring, individual plasticity in aggression are largely
unknown. For example, winning aggressive encounters
against conspecifics often leads to increased future ag-
gression in many species (fish: McDonald et al., 1968;
Chase et al., 1994; Hsu and Wolf, 1999; birds: Ratner,
1961; Drummond and Canales, 1998; rodents: Ginsburg
and Allee, 1942; Scott and Marsden, 1953; Bevan et al.,
1960; Meisel et al., 1988; Meisel and Sterner, 1990;
Kudryavtseva, 2000); yet, no neural mechanisms ex-
plaining these changes have been identified. In addition,
females of many species exhibit predictable changes in
aggression that parallel stages of estrus (reviewed by
Floody, 1983). Although some of the hormonal changes
associated with the estrous cycle have been correlated
with changes in aggression, the neural control of these
changes remains largely unknown. In the current study,
we investigate possible brain regions involved in medi-
ating plasticity in aggression by analyzing variation in
neural activity following aggression across the estrous
cycle of female California mice, Peromyscus californi-
cus.
We previously reported differences in aggression
across the estrous cycle in female California mice (Davis
and Marier, 2003), a strictly monogamous species
(Ribble and Salvioni, 1990; Ribble, 1991), in which both
males and females exhibit high levels of aggression and
parental care (Eisenberg, 1963; Dudley, 1974; Guber-
nick and Alberts, 1987; Ribble and Salvioni, 1990;
Bester-Meredith et al.1999; Trainor and Marler, 2001;
Bester-Meredith and Marler, 2003; Davis and Marler,
2004). We found that aggression was greatest when
females were in diestrus and lower when females were
in proestrus (Pro) and estrus, with most proestrous fe-
males failing to attack an intruder (Davis and Marler,
2003). Also, we found that progesterone (P
4
) decreased
following an encounter in both the most aggressive and,
surprisingly, the least aggressive group, whereas the
ratio of P
4
to testosterone (P
4
/T) decreased only in the
more aggressive, diestrous females (Davis and Marler,
2003). A decrease in either the P
4
or P
4
/T ratio is
*Correspondence to: E. S. Davis, Biological Sciences Department,
Upham Hall, University of Wisconsin-Whitewater, Whitewater, WI,
53190, USA.
E-mail address: davise@uww.edu (E. S. Davis).
Abbreviations: AccN, nucleus accumbens; AH, anterior hypothalamus;
ANCOVA, analysis of covariance; AVP, arginine vasopressin; BNST,
bed nucleus of the stria terminalis; Cort, corticosterone; D2, diestrus
day 2; D3+, diestrus day 3 or greater; DEn, endopiriform nucleus; E
2
,
estradiol; LSv, lateral septum, ventral; MeA, medial amygdala; MPN,
medial preoptic nucleus; NGS, normal goat serum; P
4
, progesterone;
PBS-X, 2 ml Triton X-100 dissolved in 1 l PBS; Pir, piriform nucleus;
Pro, proestrus; PVN, paraventricular nucleus; SCN, suprachiasmatic
nucleus; T, testosterone; VMH-l, lateral ventromedial hypothalamus;
ZI, zona incerta.
Neuroscience 127 (2004) 611– 624
0306-4522/04$30.00+0.00 © 2004 IBRO. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuroscience.2004.05.034
611