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Lactation does not alter the long-term stability of individual differences in behavior of laboratory mice on the elevated plus maze

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  • Université Sorbonne Paris Nord

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Individual consistency over time in behavioral responses to challenging situations is usually regarded as an indication of the existence of animal personality types. Although such consistency has been found in a variety of species, information about long-term stability is scanty, in particular across different life history stages, for example reproductive and non-reproductive periods, which have the potential to affect substantially the behavioral responses of animals. In our study of adult female laboratory mice, we explored the stability of behavioral responses across a 43-day period by successively testing the animals on an elevated plus maze. We tested two groups, one group that had offspring during the first two tests but not during the last test, and another group that only had offspring during the last test. We found clear evidence of individual consistency over time by means of positive significant correlations across the different tests: animals that spent more time in the closed arms and those that entered the open arms more often during the first test also tended to do so during the second test—when still in the same reproductive state, and also during the third test—when in a different reproductive state. In addition, females of the two groups did not differ overall in their responses, although we found a significant increase in the frequency and duration of presumed anxiety-related behavior during the course of the experiment, contradicting the notion that habituation effects should attenuate the challenge of the test situation. In conclusion, our study strongly suggests the existence of stable personality types in female laboratory mice, even across different reproductive stages.
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ARTICLE
Lactation does not alter the long-term stability of individual
differences in behavior of laboratory mice on the elevated
plus maze
Heiko G. Ro
¨
del
Robyn Hudson
Lena Rammler
Nina Sa
¨
nger
Lisa Schwarz
Peter Machnik
Received: 14 October 2011 / Accepted: 22 November 2011 / Published online: 10 December 2011
Ó Japan Ethological Society and Springer 2011
Abstract Individual consistency over time in behavioral
responses to challenging situations is usually regarded as
an indication of the existence of animal personality types.
Although such consistency has been found in a variety of
species, information about long-term stability is scanty, in
particular across different life history stages, for example
reproductive and non-reproductive periods, which have the
potential to affect substantially the behavioral responses of
animals. In our study of adult female laboratory mice, we
explored the stability of behavioral responses across a
43-day period by successively testing the animals on an
elevated plus maze. We tested two groups, one group that
had offspring during the first two tests but not during the
last test, and another group that only had offspring during
the last test. We found clear evidence of individual con-
sistency over time by means of positive significant corre-
lations across the different tests: animals that spent more
time in the closed arms and those that entered the open
arms more often during the first test also tended to do so
during the second test—when still in the same reproductive
state, and also during the third test—when in a different
reproductive state. In addition, females of the two groups
did not differ overall in their responses, although we found
a significant increase in the frequency and duration of
presumed anxiety-related behavior during the course of the
experiment, contradicting the notion that habituation
effects should attenuate the challenge of the test situation.
In conclusion, our study strongly suggests the existence of
stable personality types in female laboratory mice, even
across different reproductive stages.
Keywords Animal personality Anxiety
Mus musculus Temperament Reproduction
Introduction
Interest has been growing recently in the study of consis-
tent individual differences in the behavior of animals, a
phenomenon that has been variously termed animal per-
sonality, temperament, behavioral style, behavioral syn-
drome, or coping style (Wilson et al. 1994; Koolhaas et al.
1999; Sih et al. 2004). An increasing number of studies of a
wide range of vertebrate and invertebrate species have
demonstrated the stability of such differences over long
time spans and in different contexts (Gosling and John
1999; Dingemanse et al. 2002; Bell 2007; Freeman and
Gosling 2010; Gracceva et al. 2011; Reyes-Meza et al.
2011;Ro
¨
del and Meyer 2011;Ro
¨
del and Monclu
´
s 2011;
Schuett et al. 2011), two factors that are generally regarded
as requirements for the existence of animal personality
(Bell 2007; Bergmu
¨
ller 2010; Uher 2011). Nevertheless, in
addition to the study of consistency across time and con-
text, there is also a need for information about temporal
H. G. Ro
¨
del (&)
Laboratoire d’Ethologie Expe
´
rimentale et Compare
´
e
E.A. 4443 (LEEC), Universite
´
Paris 13, Sorbonne Paris Cite
´
,
93430 Villetaneuse, France
e-mail: heiko.rodel@leec.univ-paris13.fr
H. G. Ro
¨
del L. Rammler N. Sa
¨
nger L. Schwarz
P. Machnik (&)
Department of Animal Physiology, University of Bayreuth,
Universita
¨
tsstraße 30, 95447 Bayreuth, Germany
e-mail: Peter.Machnik@uni-bayreuth.de
R. Hudson (&)
Instituto de Investigaciones Biome
´
dicas, Universidad Nacional
Auto
´
noma de Me
´
xico, Distrito Federal, Mexico
e-mail: rhudson@biomedicas.unam.mx
123
J Ethol (2012) 30:263–270
DOI 10.1007/s10164-011-0320-y
consistency in individual differences during different
stages in the life history of an individual. Without doubt,
reproduction is one of the most prominent aspects of the
life of an adult animal, accompanied by marked changes in
its physiological and emotional state. Importantly, it is
widely accepted that mammalian females are hypo-
responsive to stressors during lactation (Lightmann et al.
2001), leading to decreased fear and anxiety and to
increased maternal aggressiveness (Ostermeier 1983;Ha
˚
rd
and Hansen 1985; Maestripieri and D’Amato 1991).
Defense of offspring against infanticidal intruders is
thought to be the main function of this (Parmigiani et al.
1988;Ro
¨
del et al. 2008). Thus, changes in emotionality
associated with animals’ reproductive stage might have the
potential to alter the consistency of a female’s behavioral
responses over long time periods, including different
reproductive stages. Typically, such changes can affect the
temporal consistency of the average score of a behavior
expressed by a group of animals tested in a given context
(mean-level consistency; Stamps and Groothuis 2010), as
has been described for great tits (Parus major) across age
or across different life history stages (Dingemanse et al.
2002; Carere et al. 2005).
Considering that the laboratory mouse (Mus musculus)
is now one of the most commonly used mammals in
behavioral and biomedical research, it was our objective in
this study to investigate the stability of individual differ-
ences in behavioral responses of females of this species
tested over an appreciable time span and when in different
reproductive states. Generally, it has recently been reported
that laboratory mice are also consistent over time in their
responses in standardized test situations, pointing towards
the existence of distinct personality types (Lewejohann
et al. 2011). We chose RjHan:NMRI mice, because these
are frequently used in behavioral studies in biomedicine
and psychopharmacology, and we chose to investigate
animals’ responses when tested on the elevated plus maze,
a standardized and commonly used test of anxiety in
laboratory rats and mice (Archer 1973; Pellow et al. 1985;
Komada et al. 2008).
We asked whether stable individual differences in
response would be observed for females on the elevated
plus maze across an appreciable time span, and also across
different reproductive states. For this, we first evaluated
the temporal consistency of lactating and non-lactating
females’ behavioral responses over a short time period of
2 days, and in particular whether these two groups of
females would be distinguishable in their overall responses.
We then tested for temporal consistencies over a longer
time period of more than 40 days, and which included
changes in the females’ reproductive state.
Methods
Animals and housing conditions
We used 23 female RjHan:NMRI mice (on average
91.5 ± 0.9 SD days old at the start of the study) obtained
from Janvier Laboratories (Le Genest-Saint-Isle, France).
Females were kept individually in standard polycarbonate
cages (26 cm 9 42 cm 9 15 cm; Macro 2808 type III;
Ehret, Germany) containing wood shavings as bedding. For
mating, only, they were housed with a stud male of the
same strain (for 7 days). Animals had ad libitum access to
mouse standard diet (Rat & Mouse Pro; Versele-Laga,
Belgium) and water, and were kept on a 12:12-h light/dark
cycle (lights off at 19:00 hours). Temperature was main-
tained at 21°C(±0.5 SD) and relative humidity at
approximately 50%. Animals were transferred to clean
cages once a week. Cages were checked daily for the
presence of litters, and the day of birth was regarded as
postnatal day 0. Mothers and litters were left undisturbed
until the mothers’ first test trial on postpartum day 6
(Fig. 1). Mean litter size was 15.9 ± 1.8 SD, and litters
were euthanized shortly after the trials on postnatal day 8.
without offspring without offspring with offspring
with offspring with offspring without offspring
time
T
1
n = 14 n = 14 n = 14
n = 7
n = 9n = 9
b
a
T
2
T
3
Fig. 1 Experimental design. Repeated measurements conducted with
two groups (a, b) of same-age adult female laboratory mice. Subjects
underwent three consecutive tests on an elevated plus maze during
different reproductive states. Females with offspring were tested on
postpartum day 6 (T
1
, T
3
) and on postpartum day 8 (T
2
); note that
days after the onset of the experiment are given in the figure. Females
were not pregnant when tested
264 J Ethol (2012) 30:263–270
123
Experimental design, sample sizes and behavioral
testing
At the start of the study we randomly divided the females
into two treatment groups, those mated and first tested as
mothers of young litters and later as non-mothers, and
those housed alone and first tested as non-mothers and then
mated and tested as mothers of young litters (Fig. 1).
Fourteen females formed the first group, and nine formed
the second group, although, because of failure to become
pregnant, only seven of these completed all three trials
(Fig. 1). Except for these two females, animals were given
three trials spread over 43 days (Fig. 1) on an elevated plus
maze. During the first two trials, which were conducted
within 2 days, the animals of the two groups were in the
same reproductive state, whereas the reproductive state of
the individual females changed between the first/second
trial and the third trial, representing a change in repro-
ductive history. These changes were reversed for the two
groups (Fig. 1a, b).
The elevated plus maze was made of PVC for easy
cleaning with isopropyl alcohol and water between trials. It
consisted of four arms 10 cm wide and 50 cm long,
arranged at 90° angles, and mounted 80 cm above the floor.
Two opposite arms enclosed by 40-cm high walls and two
open arms without walls were connected by a 10 9 10 cm
central platform. We tested in the light phase (between
08:00 and 10:00 hours). The luminance measured on the
surface of the plus maze was 20 cd/m
2
in the closed arms
and 70 cd/m
2
in the open arms of the plus maze. Each
female was placed on the central platform facing an open
arm and its behavior was recorded for 5 min by use of a
video camera mounted 120 cm above the center of the
maze. We scored two types of behavior: the percentage of
time an animal spent in the closed arms and the number of
times it entered the open arms, both defined as crossing the
respective thresholds with all four feet. Animals were kept
and treated according to the institutional guidelines of the
University of Bayreuth, Germany, where the experiments
were conducted.
Statistical analysis
Each video was analyzed by one of three persons unaware
of the experimental design. Videos from the different
experimental stages and from the different animals were
analyzed in a random order.
We used multivariate statistical models for analyzing
the data; the software R version 2.13.0 (R Development
Core Team 2011) was used for all statistical analysis. The
principal objective was to test for correlations of the two
different behavioral variables (% time in closed arms;
N entries to open arms) across time. Therefore, we first
correlated the behavioral responses measured during
experimental stages T
1
(predictor variable) and T
2
(response variable), and then tested for correlations between
the behavior measured at T
1
(predictor variable) and T
3
(response variable). We always included the reproductive
state/history of the animals (Fig. 3) in the statistical models
as an additional factor. In the case of correlations between
T
1
and T
2
, the females of the two groups were in different
reproductive stages, i.e. they either had offspring or did not
(factor with 2 levels). In the case of correlations between T
1
and T
3
, the two groups of females had a different repro-
ductive history, i.e. females either had offspring during the
first test and then no longer during the second or vice versa
(factor with 2 levels). We also checked for the interactions
of T
1
and the females’ reproductive state (Table 1a, c) or
reproductive history (Table 1b, d), in order to determine
whether the correlations between the different experimental
stages differed or specifically occurred in one group of
females only. However, these interactions were never sig-
nificant (Table 1), and thus the statistical models were
recalculated after omitting the interaction term. As a con-
sequence, and because the main effects of reproductive state
or history were also never significant (Table 1), the data for
the two groups of females were pooled and only one
regression line was calculated for each statistical model
(Fig. 3).
The data presented in Fig. 2 were analyzed with mixed
effects models including the individuality of the animals as
a random factor and thus allowing for repeated measure-
ments. Also here, we calculated the interactions between
the experimental stages (factor with three levels) and the
reproductive stage/history of the females. As the interac-
tions were again never significant, they were omitted from
the models and these were re-calculated. Mixed effects
models were calculated using the R-package lme4 (Bates
et al. 2011), and P values were extracted by likelihood ratio
tests (Faraway 2006).
The percentage time that the two groups of animals
spent in the closed arms was analyzed with linear mixed
models (data plotted in Fig. 2a, b) or linear models (data
plotted in Fig. 3a, b). We ensured the model residuals
approximated a normal distribution by checking normal
probability plots and by using the Shapiro–Wilk test. The
number of entries into the open arms was analyzed with
generalized linear models (data plotted in Fig. 2c, d) or
general linear mixed models (data plotted in Fig. 3c, d) for
Poisson-distributed data using a log-link function. For
all models, we checked for homogeneity of variances
by plotting the model residuals versus fitted values
(Faraway 2006). For the Poisson regressions (as shown in
Fig. 3c, d) we calculated Nagelkerke’s pseudo-R
2
to assess
the explained variance of the significant correlations
(Nagelkerke 1991).
J Ethol (2012) 30:263–270 265
123
Results
Anxiety-related behavior of females during successive
tests
The percentage time that the animals spent in the closed
arms of the elevated plus maze increased (within subjects:
v
2
2
= 40.57, P \0.001; Fig. 2a, b) and the number of
entries into the open arms decreased (within subjects:
v
2
2
= 45.37, P \ 0.001; Fig. 2c, d) across the three con-
secutive experimental stages. Post-hoc comparisons with
regard to both response variables indicated significant
differences (increase: Fig. 2a, b; decrease: Fig. 2c, d)
between T
1
and T
2
and between T
1
and T
3
; P \0.001 in all
cases), but not between T
2
and T
3
(P [ 0.10). There were,
however, no general differences among individual females
in different reproductive states (P [ 0.10), and also no
specific differences between the two groups of females
during the different stages of the experiment—as indicated
by the non-significant interaction terms (group 9 experi-
mental stage: P [ 0.10), either with regard to the per-
centage time spent in the closed arms or to the number of
entries into the open arms.
Consistency across time
The time that individual females spent in the closed arms
and the number of entries into the open arms were signif-
icantly correlated across time (Fig. 3). There were signifi-
cant positive correlations between the responses during the
first and second tests, when individual females of the two
groups were in the same reproductive state (Table 1a, c;
Fig. 3a, c), and there were also positive, although weaker,
correlations between the first and the third period of the
experiment, i.e. across two periods when the reproductive
state within the two groups of females had changed
(Table 1b, d; Fig. 3b, d).
As shown above, the results indicate that there were no
general differences in this anxiety-related behavior
between the females of the two groups; that is, the corre-
lations of the two groups did not differ in the intercepts, as
indicated by the non-significant effects of reproductive
state (Table 1). In addition, there were no differences in
slopes, as indicated by the non-significant interaction terms
(Table 1a, b), and thus the four correlations were best
explained by single regression lines for the two groups of
females (Fig. 3a–d).
Discussion
Overall, individual behavioral responses of female mice in
a standardized test considered to test fearfulness were
markedly different. We found correlational evidence for
short-term temporal consistency across individuals (dif-
ferential consistency: Stamps and Groothuis 2010) for
animals in the same reproductive state. The repeatability
was quite high, with explained variances of 33 and 50%
(values of R
2
in Fig. 3a, c, respectively). In addition, the
two measures of anxiety-related behavior used here were
also indicative of high long-term temporal consistency over
the 43-day experimental period, an appreciable time span
in the life of an adult mouse. Here, the repeatability was
moderate with explained variances of 22 and 43% (Fig. 3b, d).
Table 1 Consistency across time
Response variable Predictor variables F/v
2
df P
(a) T
2
time spent in closed arms T
1
time spent in closed arms 10.31 1,21 0.004
Reproductive state 1.32 1,20 0.26
Interaction 0.83 1,19 0.37
(b) T
3
time spent in closed arms T
1
time spent in closed arms 5.43 1,19 0.031
Reproductive history 3.50 1,18 0.078
Interaction 0.95 1,17 0.34
(c) T
2
entries into open arms T
1
entries into open arms 15.89 1,21 \0.001
Reproductive state \0.01 1,20 0.98
Interaction 1.53 1,19 0.22
(d) T
3
entries into open arms T
1
entries into open arms 12.72 1,19 \0.001
Reproductive history 0.35 1,18 0.56
Interaction 0.05 1,17 0.82
Multivariate models on the correlations between the percentage time that female laboratory mice spent in the closed arms of an elevated plus
maze (a, b: calculated with linear models) and between the numbers of entries into the open arms (c, d: calculated with generalized linear models
for Poisson-distributed data) during three consecutive tests. In addition, the effects of the animals’ reproductive state/history were tested (Fig. 1).
Statistics were calculated using a backward elimination of non-significant predictor variables and interaction terms
266 J Ethol (2012) 30:263–270
123
Most importantly, the changes in reproductive state (from
non-lactating to lactating in one group and vice versa in the
other) did not nullify this consistency.
Our results are therefore, on the one hand, consistent
with the proposition that mice show stable individual dif-
ferences in anxiety-related behavior, commonly used as
indicators of animal personality (Lewejohann et al. 2011).
On the other hand, our failure to find a general effect on
fearfulness of the females’ reproductive state or of their
reproductive history was surprising. Overall, females were
no less fearful when they had young, and, irrespective of
their reproductive state, in relation to the sequence of
conditions in which they were tested. This was the case
even though we tested mothers early postpartum when
changes in the physiological and emotional state of a
female are thought to be particularly strong (Ostermeier
1983). Although this finding contrasts with a number of
reports of reduced fearfulness of lactating rats and mice
(Fleming and Luebke 1981;Ha
˚
rd and Hansen 1985;
Ferreira et al. 1989; Maestripieri and D’Amato 1991), it is
consistent with other reports failing to find such an effect
(Lonstein 2005). Various explanations for this inconsis-
tency have been suggested: possible bias because of
elimination of ‘non-responders’ from study samples
(Maestripieri and D’Amato 1991); that different behavioral
tests measure different aspects of anxiety; that females’
levels of fearfulness vary during different stages of lacta-
tion; strain differences; and whether or not mothers had
recently had contact with their young before testing
(Lonstein 2005).
Fig. 2 Differences in the
responses over time.
Comparison of the percentage
time that female laboratory
mice spent in the closed arms of
an elevated plus maze (a, b) and
between the numbers of entries
into the open arms (c, d) during
three consecutive tests. Data
(repeated measurements) are
shown separately for the two
sets of females with different
consecutive reproductive stages:
grey boxes indicate that the
females had offspring whereas
white boxes indicate that
females did not have offspring
during the respective trials. See
text for statistics; sample sizes
are given in the graph
J Ethol (2012) 30:263–270 267
123
For animals of both groups an increase in fearfulness
was actually observed from the first compared with the
subsequent two trials, expressed as an increase in the time
spent on the closed arms and a decrease in the number of
entries into the open arms (Fig. 2). This is in contrast with
the assumption that the animals might habituate to the
maze, i.e. show an overall reduction in fearfulness as a
result of increasing familiarity with the test situation across
the three trials (Calvo-Torrent et al. 1999). However, such
an increase in anxiety-related behavior in successive plus-
maze tests seems to be not unusual and similar results have
been reported previously (File et al. 1993; McIlwain et al.
2001;Vo
˜
ikar et al. 2003; Lewejohann et al. 2011). Possi-
bly, in the first trial, motivation to explore the novel situ-
ation presented by the maze counteracted to some extent
the more fearful response (or reduced curiosity) seen in
later trials after the animals had learned the configuration
of the maze and their various response options. Alterna-
tively, it might be assumed that the better illumination of
the surface of the open arms (70 cd/m
2
) than of the closed
arms (20 cd/m
2
) might have led to an increased aversion to
the former parts of the elevated plus maze across the dif-
ferent trials (Miller et al. 2011). Nevertheless, important for
the purpose of our study, these changes in the absolute
levels in the animals’ behavioral responses over time tested
on an individual basis were again decoupled from the
females’ initial reproductive stage along T
1
and T
2
, and
from the changes in the females’ reproductive state along
T
2
and T
3
(Figs. 1, 2).
Overall, the findings of this study add to the growing
evidence of individual differences among conspecifics in
behavior that can be considered to reflect an animal’s
personality by demonstrating that individual differences in
the fearfulness (or curiosity) of female mice persist across
time and physiological (reproductive) state. This then rai-
ses questions about the origin of such differences, partic-
ularly during development (Stamps and Groothuis 2010;
Trillmich and Groothuis 2011; Trillmich and Hudson
2011). This is important, given the efforts made in
behavioral and biomedical research to reduce or ideally to
eliminate such differences by using inbred stains or clones,
and by raising and maintaining animals under highly con-
trolled, standardized conditions. These results (although
conducted with an outbred strain) provide support for a
growing understanding that eliminating such variance is
not possible, and for the proposition that stable individual
Fig. 3 Consistency across time.
Significant correlations between
the time spent in the closed
arms and between the number of
entries into the open arms of the
elevated plus maze during the
first test T
1
and (a, c) the second
test T
2
, conducted 2 days later
and (b, d) the third test T
3
,
conducted 43 days later. Data
from the females of
experimental group A are given
by filled circles, and data from
females of group B are given by
open circles (Fig. 1). The
explained variations (R
2
for
linear regressions and R
Nagelkerke
2
for Poisson regressions) are
given in the graphs; details of
the statistics are given in
Table 1. Note the differences in
the scaling of the y-axes
268 J Ethol (2012) 30:263–270
123
differences in behavior (and so in underlying physiology)
are an inherent part of animal populations (Wu
¨
rbel 2000;
Macrı
`
and Wu
¨
rbel 2006; Hudson et al. 2011; Lewejohann
et al. 2011; Schuett et al. 2011). It is now widely accepted
that variation in animal personality and the maintenance of
this within populations is because of fitness trade-offs (Dall
et al. 2004;Re
´
ale 2007; Wolf et al. 2007). Accordingly, it
would be useful to investigate the consequences for
reproductive fitness in maternal mice with indicators of
different personality types of the kind found here (Biro and
Stamps 2008; Boon et al. 2008; Smith and Blumstein
2008).
Acknowledgments We thank Stefan Schuster, Wolfram Schulze,
and Hans Distel for stimulating discussions, Carolina Rojas for bib-
liographical assistance, and Karl-Heinz Po
¨
hner and Achim Schmidt
for excellent animal care. Financial support to RH was provided by
the Mexican funding agencies CONACYT (48692-Q) and PAPIIT
(IN223910).
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... In addition, divergent results found in different traits and testing setups might be due to differences in relative importance of changes in brain and physiology [116]. Good evidence for individual stability in performance comes from [117], who found female outbred mice (strain RjHan:NMR1) to remain stable in their anxiety-related behaviour measured in an elevated plus-maze at PND 90 and PND 135, regardless of changes in their reproductive state. In inbred mice behavioural stability was demonstrated in a study [6] by showing that male mice (strain C57BL/6N) were stable in their anxietyrelated behaviour measured in an elevated plus-maze around PND 60 and PND 90. ...
... Interestingly, both studies report behavioural consistencies despite considerable inter-individual variability. Possibly some of the variability was experimentally induced by either including two groups of females with different breeding experiences [117] or different subgroups of mice that were housed in either stable or instable social groups [6]. ...
... Additionally, there was no effect on long term stability of behaviour in lactating compared to non-lactating females in an elevated plus maze. This suggests that the reproductive state may not influence the stability of these behavioural traits [117]. Hence, except for minor (and possibly temporary) variations, behaviour remains relatively stable during the phase of adulthood. ...
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... They also potentially contribute to our further understanding of the development of individual differences in the behavior of the domestic cat and other mammals in several ways: by pointing to the need for longer term and comparative studies, where possible using naturalistic stimuli and species-relevant contexts, and to the importance of taking individuals' motivational state into account. This is indeed something which may change across the lifespan and with the changing circumstances of an individual; e.g., a lactating female with high nutritional requirements (review in Martínez-Gómez et al. 2004) might be more motivated to compete for food than a non-lactating female (but see Rödel et al. 2012 for evidence of stable individual differences in the behavior of lactating and non-lactating laboratory mice Mus musculus), posing a challenge for personality research and for the definition of "personality" as individual differences in behavior stable over context and time (see Trillmich et al. 2015). Nevertheless, it remains possible that early experience of something as fundamental as nutritional stress and associated physiological and behavioral processes might have long-term effects on an individual's behavior, its "personality," in later life (Bateson et al. 2004). ...
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... Our results on the existence of consistent individual differences in exploration confirm the findings of previous studies in laboratory mice Mus musculus (Brust et al. 2015;Lewejohann et al. 2011;Rödel et al. 2012) and other rodent species of wild origin (mound-building mouse Mus spicilegus: Duparcq et al. 2019;Rangassamy et al. 2015;common Schuster et al. 2017). To the best of our knowledge, our study is the first to demonstrate consistent individual differences in exploration in house mice of wild origin. ...
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... Attempts to reduce such unwanted individual differences include the use of inbred and transgen- ic strains and efforts of high standardization of housing and rearing. However, it has been increasingly noted during the recent years that in- dividual differences in behavior and physiology of laboratory animals, with respect to their behavioral profiles [93,94], due to differences in early environmental conditions [95], and even in genetically identical individuals [96] cannot be fully suppressed. However, making sense of such individual differences can be considered an essential step towards the understanding of inter-individual variation in disease susceptibility or treatment responses [27,28,41,43]. ...
... Without this move toward the middle, the subpopulation of dams that are especially low in anxiety may be under-aroused and neglectful of cues coming from the litter and other aspects of their environment, while dams that are especially high in anxiety may be over-aroused and unnecessarily responsive. It is unknown how long females' premating trait-like anxiety can predict their anxiety-related behaviors after reproducing, but anxiety in mice tested during the first week postpartum is highly correlated with their anxiety tested again after weaning the pups (Rodel et al., 2012). Even more suggestive of very long-term predictive value of a females' traitlike anxiety is that female rhesus monkeys show stable anxiety-related behavior across series of births that span years (Maestripieri, 2000). ...
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... Anxiety-related behavior in nulliparous female laboratory rodents is stable across many months (Leibsch et al., 1998;Henniger et al., 2000;Curley et al., 2012), suggesting the existence of an ongoing ''trait'' anxiety (Gosling, 2001). It is unknown whether or not anxiety-related behavior in our least-anxious and most-anxious rats continues to be predictable after the first week postpartum, but this may be likely because there is a significant correlation between the anxiety of randomly selected female mice tested during the first postpartum week and again several days post-weaning (Ro¨del et al., 2012). Furthermore, mother rhesus monkeys show stable anxiety across multiple births spanning years (Maestripieri, 2000). ...
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In female mammals, the postpartum period involves dramatic shifts in many socioemotional behaviors. This includes a suppression of anxiety-related behaviors that requires recent physical contact with offspring. Factors contributing to differences among females in their susceptibility to the anxiety-modulating effect of offspring contact are unknown, but could include their innate anxiety and brain monoaminergic activity. Anxiety was assessed in a large group of nulliparous female rats and the least-anxious and most-anxious tertiles were mated. Anxiety was assessed again postpartum after females were permitted or prevented from contacting their offspring 4 hr before testing. Levels of dopamine β-hydroxylase (DBH, norepinephrine synthesizing enzyme) and tryptophan hydroxylase 2 (TPH2, serotonin synthesizing enzyme) were measured in the brainstem and dorsal raphe, respectively. It was found that anxiety-related behavior in the two groups did not differ when dams were permitted contact with offspring before testing. Removal of the offspring before testing, however, differentially affected anxiety based on dams' innate anxiety. Specifically, dams reverted back to their pre-mating levels of anxiety such that offspring removal slightly increased anxiety in the most-anxious females but greatly lowered anxiety in the least-anxious females. This reduction in anxiety in the least-anxious females after litter removal was associated with lower brainstem DBH. There was no relationship between females' anxiety and dorsal raphe TPH2. Thus, a primary effect of recent contact with offspring on anxiety-related behavior in postpartum rats is to shift females away from their innate anxiety to a more moderate level of responding. This is particularly true for females with the lowest anxiety, which may be mediated by central noradrenergic systems, and has implications for their ability to attend to their offspring.
Thesis
Cette thèse comprend cinq manuscrits d'articles. Deux de ces manuscrits sont publiés, l’un est actuellement en révision et deux sont en préparation pour soumission.Les animaux diffèrent de manière stable au cours du temps et dans différents contextes dans leur comportement, un phénomène souvent nommé personnalité animale. Les animaux diffèrent ainsi dans leur niveau d’expression de différents traits de personnalités. Cependant l’étude de la stabilité des traits de personnalité chez les jeunes animaux apporte des résultats controversés. Les deux principaux objectifs de cette thèse ont donc été d’évaluer comment l’environnement précoce des animaux façonnait leur personnalité et si l’expression de leur comportement était stable au cours du développement. Notre modèle d’étude était un petit rongeur d’origine sauvage, la souris glaneuse Mus spicilegus. Cette souris se trouve dans les zones agricoles d’Europe centrale et orientale. Il s'agit d'une espèce monogame et la femelle et le mâle participent aux soins parentaux. Les principaux résultats de cette thèse soulignent la stabilité des réponses comportementales des souris glaneuses dans des contextes sociaux et non-sociaux tôt lors de la période post-natale jusqu’à la maturité. De nombreux traits de personnalité étaient associés à travers différents contextes ; formant ainsi ce qu'il est convenu d'appeler un syndrome comportemental. Cette stabilité dans le comportement était avérée que l'analyse porte sur la totalité de l'échantillon ou qu'elle prenait en compte les différences intra-portées. L’environnement précoce et en particulier la présence du père apparaissent déterminants dans l’émergence et la modulation de la personnalité. Les individus élevés sans père montraient une plus grande réactivité dans deux tests différents par rapport à ceux élevés avec les deux parents. Différentes personnalités étaient associées à des mécanismes physiologiques. Confrontés à un stresseur chronique, les individus exprimant différentes personnalités montraient des différences physiologiques caractérisées par des profils immunologiques et hormonaux distincts. D'autre part les couples possédant des scores similaires d’anxiété, indépendamment du score des deux partenaires du couple, avaient une plus grande probabilité de reproduction durant la période d’observation, que les couples aux scores différents suggérant de potentiels avantages évolutifs. Cette thèse aborde en parallèle les aspects proximaux et ultimes du comportement chez un même modèle biologique ce qui est un but rarement atteint dans une étude éthologique.
Article
Previous studies of freezing and open-field activity have demonstrated that lactating rats are less fearful or less anxious than nonpregnant ones. The purpose of this investigation was to observe the behavior of mother rats in conflict tests, which are frequently used in studies on the neurobiology of anxiety. In the punished drinking test, in which licking from a water spout is punished by electric shocks, mothers (observed on Day 1 postpartum following 24 hr of water deprivation) were found to drink more than virgins. Mothers (Day 1 postpartum) also consumed more food than controls in an unfamiliar open field. In contrast, no difference between mothers (Day 5 postpartum) and virgins was present in the exploration of an electrified shock probe. The largest maternal anticonflict effects in the drinking and feeding tests were recorded when the females were tested with their pups. Increased punished drinking was also observed in virgin rats treated with the anxiolytic benzodiazepine midazolam. Water-deprived virgins and mothers did not differ in the shock titration test, a result suggesting that diminished pain reactivity was unlikely to account for the increased punished drinking in mothers. Moreover, females in late pregnancy, which are hypoalgesic (Gintzler, 1980), did not lick more than virgins in the punished drinking test. Following 24 hr of water deprivation, unpunished drinking was higher in lactating females than in virgins, so the increased acceptance of punishment by mothers might have been due to their being more thirsty than virgins. However, virgins, deprived of water for 48 hr and whose unpunished drinking was similar to that of mothers deprived for 24 hr, did not accept as many punishments as the lactating females. Binding of [³H]-flunitrazepam, [³H]-muscimol, and [³⁵S]-t-butylbicyclophosphorothionate in tissue samples from cortex, limbic system, and hypothalamus was similar in mother and virgin rats. Thus, motherhood does not appear to be associated with any major sensitivity changes to the various ligands of the GABA-gated chloride channel.
Article
The evolutionary continuity between humans and other animals suggests that some dimensions of personality may be common across a wide range of species. Unfortunately, there is no unified body of research on animal personality; studies are dispersed across multiple disciplines and diverse journals. To review 19 studies of personality factors in 12 nonhuman species, we used the human Five-Factor Model plus Dominance and Activity as a preliminary framework. Extraversion, Neuroticism, and Agreeableness showed the strongest cross-species generality, followed by Openness; a separate Conscientiousness dimension appeared only in chimpanzees, humans' closest relatives. Cross-species evidence was modest for a separate Dominance dimension but scant for Activity. The comparative approach taken here offers a fresh perspective on human personality and should facilitate hypothesis-driven research on the social and biological bases of personality.
Article
CALVO–TORRENT, A., P. F. BRAIN AND M. MARTINEZ. Effect of predatory stress on sucrose intake and behavior on the plus-maze in male mice. PHYSIOL BEHAV 67(2) 189–196, 1999.—In this study, the effect of the exposure of male mice to sensory stimuli from rats was assessed on both sucrose intake and the elevated plus-maze tests. CDl male mice were trained in the sucrose intake task (the prestress phase) and, subsequently, distributed into two groups. The stressed group was accommodated in the same room as rats and the control group with mice (the stress phase). After being transferred, animals were tested on sucrose intake and the plus-maze (acute tests) and retested three times a week for sucrose intake and once on plus-maze on the last day (chronic tests). After acute exposure to the predator, the only difference between stressed and control animals was a higher number of fecal boli left on the plus-maze by the former. During the chronic phase, stressed animals showed a lower level of sucrose intake and higher level of anxiety than controls. In conclusion, this study shows that chronic exposure of male mice to stimuli from rats reduces the sensitivity to the rewarding properties of sucrose and prevents the habituation to the plus-maze observed in controls. Thus, this study suggests that exposure of mice to sensory stimuli from rats may provide an animal model of stress, and that these species should not be routinely housed together.
Article
The evolutionary continuity between humans and other animals suggests that some dimensions of personality may be common across a wide range of species. Unfortunately, there is no unified body of research on animal personality; studies are dispersed across multiple disciplines and diverse journals. To review 19 studies of personality factors in 12 nonhuman species, we used the human Five-Factor Model plus Dominance and Activity as a preliminary framework. Extraversion, Neuroticism, and Agreeableness showed the strongest cross-species generality, followed by Openness; a separate Conscientiousness dimension appeared only in chimpanzees, humans' closest relatives. Cross-species evidence was modest for a separate Dominance dimension but scant for Activity. The comparative approach taken here offers a fresh perspective on human personality and should facilitate hypothesis-driven research on the social and biological bases of personality.