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The Mother as Hunter: Significant Reduction in Foraging Costs through Enhancements of Predation in Maternal Rats.

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In previous laboratory investigations, we have identified enhanced cognition and reduced stress in parous rats, which are likely adaptations in mothers needing to efficiently exploit resources to maintain, protect and provision their immature offspring. Here, in a series of seven behavioral tests on rats, we examined a natural interface between cognition and resource gathering: predation. Experiment 1 compared predatory behavior (toward crickets) in age-matched nulliparous (NULL) and postpartum lactating mothers (LACT), revealing a highly significant enhancement of predation in LACT females (mean=~65sec. in LACTs, v. ~. 270sec. in NULLs). Experiment 2 examined the possibility that LACTs, given their increased metabolic rate, were hungrier, and thus more motivated to hunt; doubling the length of time of food deprivation in NULLs did not decrease their predatory latencies. Experiments 3-5, which examined sensory regulation of the effect, indicated that olfaction (anosmia), audition (blockade with white noise), and somatosensation (trimming the vibrissae) appear to play little role in the behavioral enhancement observed in the LACTs; Experiment 6 examined the possibility that visual augmentations may facilitate the improvements in predation; testing LACTs in a 0-lux environment eliminated the behavioral advantage (increasing their latencies from ~65sec. to ~212sec.), which suggests that temporary augmentation to the visual system may be important, and hormone-neural alterations therein a likely candidate for further study. In contrast, testing NULLS in the 0-lux environment had the opposite effect, reducing their latency to catch the cricket (from ~270sec. to ~200sec.). Finally, Experiment 7 examined the development of predatory behavior in Early-pregnant (PREG), Mid-PREG, and Late- PREG females. Here, we observed a significant enhancement of predation in Mid-PREG and Late-PREG females - at a time when maternity-associated bodily changes would be expected to diminish predation ability - relative to NULLs. Therefore, as with the increasing reports of enhancements to the maternal brain, it is apparent that meaningful behavioral adaptations occur that likewise promote the survival of the mother and her infants at a crucial stage of their lives.
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Regular article
The mother as hunter: Signicant reduction in foraging costs through
enhancements of predation in maternal rats
Craig Howard Kinsley
a,
, Jamie C. Blair
a
, Natalie E. Karp
a
, Naomi W. Hester
a
, Ilan M. McNamara
a
,
Angela L. Orthmeyer
a
, Molly C. McSweeney
b
, Massimo M. Bardi
d
, Kate Karelina
a
, Lillian M. Christon
a
,
Maxwell R. Sirkin
a
, Lindsay W. Victoria
a
,DanielleJ.Skurka
a
, Christian R. Fyfe
a
,MargaretB.Hudepohl
a
,
Luciano F. Felicio
c
, R. Adam Franssen
a
, Elizabeth E.A. Meyer
a
, Ilton S. da Silva
c
, Kelly G. Lambert
d
a
Department of Psychology, Center for Neuroscience, University of Richmond, Richmond, VA 23173, USA
b
Department of Psychology, Dickinson College, Carlisle, PA 17013, USA
c
Department of Pathology, School of Veterinary Medicine, University of Sao Paulo, Brazil
d
Department of Psychology, Randolph-Macon College, Ashland, Virginia 23005, USA
abstractarticle info
Article history:
Received 5 June 2014
Revised 1 September 2014
Accepted 9 September 2014
Available online 21 September 2014
Keywords:
Adaptation
Aggression
Lactation
Maternal brain
Motherhood
Neuroplasticity
Predation
Pregnancy
In previous laboratory investigations, we have identied enhanced cognition and reduced stress in parous rats,
which are likely adaptations in mothers needing to efciently exploit resources to maintain, protect and provi-
sion their immature offspring. Here, in a series of seven behavioral tests on rats, we examined a natural interface
between cognition and resource gathering: predation. Experiment 1 compared predatory behavior (toward
crickets) in age-matched nulliparous mothers (NULLs) and postpartum lactating mothers (LACTs), revealing a
highly signicant enhancement of predation in LACT females (mean = ~65 s in LACTs, vs. ~ 270 s in NULLs).
Experiment 2 examined the possibility that LACTs, given their increased metabolic rate, were hungrier, and
thus more motivated to hunt; doubling the length of time of food deprivation in NULLs did not decrease their
predatory latencies. Experiments 35, which examined sensory regulation of the effect, indicated that olfaction
(anosmia), audition (blockade with white noise), and somatosensation (trimming the vibrissae) appear to play
little role in the behavioral enhancement observed in the LACTs; Experiment 6 examined the possibility that
visual augmentations may facilitate the improvements in predation; testing LACTs in a 0-lux environment elim-
inated the behavioral advantage (increasing their latencies from ~65 s to ~ 212 s), which suggests that temporary
augmentation to the visual system may be important, and with hormone-neural alterations therein a likely
candidate for further study. In contrast, testing NULLS in the 0-lux environment had the opposite effect, reducing
their latency to catch the cricket (from ~270 s to ~ 200 s). Finally, Experiment 7 examined the development of
predatory behavior in Early-pregnant (PREG), Mid-PREG, and Late-PREG females.Here, we observed a signicant
enhancement of predation in Mid-PREG and Late-PREG females at a time when maternity-associated bodily
changes would be expected to diminish predation ability relative to NULLs. Therefore, as with the increasing
reports of enhancements to the maternal brain, it is apparent that meaningful behavioral adaptations occur
that likewise promote the survival of the mother and her infants at a crucial stage of their lives.
© 2014 Elsevier Inc. All rights reserved.
Introduction
Life must adapt, a dictum both clear and unforgiving. Arguably, no
other developmental milestone is exemplied by, nor more reliant on,
the sudden and dramatic behavioral alterations observed in the mater-
nalmammal(Kinsley and Lambert, 2006, 2008). As pregnancy pro-
gresses, the female is literally transformed from an organism that
actively avoided offspring-related signals, to one highly motivated by
those same cues to build nests, retrieve, group, groom, crouch-over,
and care for young (Numan and Insel, 2003). Ancillary responses such
as reference memory, spatial learning, foraging, and boldness improve
in mothers compared to NULLs (Kinsley et al., 1999; Pawluski et al.,
2006a,b). Such modications arise early and are persistent, with neural
benets that last well into senescence (Gatewood et al., 2005). Evolu-
tionarily, such enhancements likely reduce the maternal burdens asso-
ciated with sheltering and feeding the vulnerable young, collectively
strengthening reproductive tness. That is, we presume that plasticity
expressed in response to reproduction may translate into benets to
mother and, hence, offspring. Of the many behaviors that change as a
function of pending or present maternity, therefore, what of predation,
a major pillar of the rat's behavioral repertoire? We present here an
example of a likely temporary but striking enhancement of predation
as a result of reproductive experience.
Hormones and Behavior 66 (2014) 649654
Corresponding author. Fax: +1 804 287 1905.
E-mail address: ckinsley@richmond.edu (C.H. Kinsley).
http://dx.doi.org/10.1016/j.yhbeh.2014.09.004
0018-506X/© 2014 Elsevier Inc. All rights reserved.
Contents lists available at ScienceDirect
Hormones and Behavior
journal homepage: www.elsevier.com/locate/yhbeh
Whereas a large portion of the rat's diet consists of plant materials
and detritus, rats are nonetheless omnivores and procient hunters.
They will prey on a variety of other animals, which they stalk, chase, at-
tack, and eventually consume. Rats are opportunistic and adaptable in
their food choices, having been observed preying on a wide variety of
small animals, including invertebrates (Strecker et al., 1962); other
rodents (Hsuchou et al., 2002); bats (Villa, 1982); birds (Atkinson,
1985); and amphibians and reptiles (Whitaker, 1978). Furthermore,
predation toward insects is a behavior that rats easily display (Kemble
et al., 1985). As these authors report, the insectprey (here, cockroaches)
was more likely to be attacked in their tests, and was attacked more
rapidly, than either other prey objects (mice), or conspecicaggressive
targets (rats) regardless of the previous amount of social experience of
the subjects; the data suggest, perhaps, an afnity for such small prey
objects and efcient sources of food. In general, then, rat predation on
insects is both natural and easily observed, highlights an evolutionary
relationship extending deep into their biological pasts, and represents
a likely bridge between laboratory examinations of behavior and the
rat's natural proclivities. Hence, predatory behavior stands as a repre-
sentative and natural test of the preparedness of rat behavior. The
study of predatorprey relationships is interesting from a number of
levels, from subtle to more obvious, and the behavior would likely ben-
et from both cognitive and motor modications of the sort associated
with the maternal brain.
For example, many recent data show that temporal adaptation is a
hallmark of the maternal female. There are numerous reports of repro-
ductive experience enhancing various aspects of the mother's behavior,
including cognition (Bodensteiner et al., 2006; Buckwalter et al., 1999;
Gatewood et al., 2005; Gonzalez-Marsical and Kinsley, 2009; Kim
et al., 2010; Lambert et al., 2005; Pawluski et al., 2006a,b). Because pre-
dation in the maternalanimal lies at the intersection of personal and off-
spring resource acquisition (viz., lactation), it serves as a valuable model
for examining reproduction-induced modication of maternal behav-
ioral repertoires. In the current set of seven behavioral experiments,
we examined predation (which for the rat, we believe, is also an
ethologically-relevant junction between cognition and resource gather-
ing) in age-matched NULL, PREG and LACT rats. Later-PREG and LACT
females are signicantly better hunters than NULLs; their ability to
trackattack-and-capture prey an enhancement related to possible
compensatory boosts in vision and motor skills occurs at a time
when the female is actually most unwieldy and reliant on collective in-
cremental improvements to balance the costs of reproduction, both
physically (a larger body size) and logistically (the substantial demands
of young). This simple yet robust behavior may shed a light on the nec-
essary behavioral expansionsrequired of the mother at a time in her life
when even the most incremental improvement may spell thedifference
between the mother's and her offspring's survival or not.
Materials and methods
Animals and reproductive experience
Approximately 138 adult (90120 days) nulliparous (NULL) female
SpragueDawley rats (Crl:CD[SD]BR), offspring of stock originally pur-
chased from Charles River Laboratories, Inc. (Wilmington, MA) were
used in the present set of experiments. These females either remained
un-mated (NULL) or were timed mated in our laboratory. For the
mated females, the day that a vaginal plug, or sperm in the vaginal
lavage, was observed was designated Day 0 of pregnancy. The mated fe-
males were then removed from the male's cage and, together with the
separate groups of un-mated NULL females, were housed individually
in modied standard rat cages (20 × 45 × 25 cm polypropylene
cages), the oors of which were covered with pine shavings. Food
(Purina rat chow) and water were available ad libitum and all animals
were housed in a reversed light:dark cycle (off from 08001800 h)
and temperature (2124 °C)-controlled testing rooms for the duration
of the present work. All animals used in this study were maintained in
accordance with the guidelines of the Institutional Animal Care and
Use Committee (IACUC) of the University of Richmond (protocols #:
09-04-1 and 12-04-1) and in accordance with the Guidelines for the
Care and Use of Mammals in Neuroscience and Behavioral Research
[(National Research Council, 2003); University of Richmond's assurance
number: A3615-01].
General predatory behavior procedure
All of the subjects were exposed to three-days of three 10-minute
pre-exposures/habituations to the testing arena, a large (152.4 cm ×
152.4 cm × 91.44 cm) open-walled enclosure. On Day 4, the animals
were food deprived for at least 10 h. Testing consisted of a 5-min accli-
mation period in the open-walled arena, followed by placing the prey
(an adult cricket, Acheta domesticus) opposite to the animal in the
arena. We observed and recorded (with video documentation) the
latency (out of 5-min/300-s) to capture the cricket and to begin to con-
sume it (all but the last experiment, which took place in the dark; see
experimental details below.) The data were collapsed to produce
mean latencies (three-trials over three-days). We operationally-
dened the predatory attack as the female attacking (an intentional
movement toward the prey) and subduing the cricket, typically with
the forepaws, preparatory to its being consumed. A small (b8%) subset
of animals (slightly more in the NULL group, but not demonstrating a
major trend for any group) caught the prey, but allowed the cricket to
slip away at least once before consuming it. In these cases, we used
the original latency to catch the cricket as the data point.
Specic experimental procedures
In Experiment 1, 90 days120 days (nulliparous [NULL]) and Day
ve/six lactating mothers (LACT; n = 12/group) were food-restricted
and habituated as described above, followed by the placement therein
of the single adult cricket.
To control for potential differences in hunger motivation, Experi-
ment 2 examined NULLs (n = 10) food-deprived for 20 h, twice as
long as those in Experiment 1. These animals were compared with the
NULL group from Experiment 1. In every other respect, these animals
were treated identically to those NULLs in Experiment 1.
For Experiments 35, which examined potential sensory system en-
hancements in the maternal female, only LACT females were used. Ex-
periment 3 examined possible modications to the sense of olfaction
via comparisons between controls and anosmic LACTs. LACTs in the an-
osmic group (n = 9) were lightly restrained and had their nares infused
with an intranasal treatment of isotonic zinc sulfate (ZnSO
4
; 10% in 0.9%
saline). Control mothers (n = 9) were infused with 0.9% saline alone.
Care was taken to ensure that the anosmic females cared for their
pups, and that all pups displayed prominent milk bands during the con-
duct of the testing, indicating the LACTs' normal lactation and attention.
Such anosmic effects typically last seven days (McBride et al., 2003),
well within the window of our testing regimen. Post-testing, all animals
were exposed to a hidden pieceof cookie in their cages to determine the
persistence of the anosmia. Any animal that investigated or found the
cookie had its data removed from the group results.
In Experiment 4 we studied possible reliance on audition. Here, we
tested LACTs (n = 7) in the presence or absence of white noise. We
employed a gray plastic-housed white noise generator producing
65 dB of white noise, which effectively masked the sound of the cricket
as it moved about the bedding (dimensions: 14 cm diameter; 12 cm
height). LACT controls (n = 7) were tested as per the regular regimen,
but with the white noise generator present but switched-off.
In Experiment 5 we examined general somatosensory sensitivity.
LACTs (n = 9) were lightly restrained and had their vibrissae trimmed
to within 1 mm of the facial fur. LACT controls (n = 9) were likewise
650 C.H. Kinsley et al. / Hormones and Behavior 66 (2014) 649654
restrained, but merely had their vibrissae stroked. Testing then com-
menced as above.
Last, in light of the relative absence of effects on the other sensory
systems, in Experiment6, LACTs (n = 8) and NULLs (n = 6) were habit-
uated in the regular open eld enclosure in normal uorescent lighting
(as above), but testing took place in a 0-lux room. Behavioral observa-
tions were performed using a set of night-vision goggles which pro-
duced a thin red laser beam as a light-reecting source. Observations
here indicated that, without the use of the goggles, one was unable to
see one's hand placed 0.5 m in front of the observer. The goggles, how-
ever, which project a laser beam onto the scene and amplify the light,
afforded a clear view of both rat and prey.
In the nal experiment (7), we examined the progression of the ef-
fects on predation with advancing pregnancy: to what degree does
the behavior change from early (expected to be less effective) through
later pregnancy (displaying improvements, as the females approach
parturition). Separate groups of adult females were used: timed-
mated females at three differenttimes of pregnancy. Therefore, we pro-
duced Early (Days 46, n = 11), Mid (Days 1114, n = 9) and Late
(Days 1820, n = 10) pregnant subjects (PREG). (We dene Day 0 of
pregnancy as the rst day that sperm is observed in the vaginal lavage.)
Testing for predation was performed similarly to the procedures above.
Statistical analyses
For Experiments 16, the data were originally analyzed using a
three-way mixed Analysis of Variance (ANOVA) and, where signicant,
followed by Least Signicant Differences (LSD) post-hoc tests and
Cohen's-d, (to indicate effect size). Experiment 7 utilized a one-way
ANOVA followed by the post-hoc and effect size tests. For ease and clar-
ity of interpretation, the data were subsequently collapsed across trials
and days to produce a summary analysis of groups within each experi-
ment (used above). In brief, where signicant, we used partial eta
squared (η
p
2
) and Cohen's-dto provide measures of effect size. Partial
eta-squared indicates the percentage of variance in the dependent var-
iable (DV) that is attributable to a particular independent variable (IV).
Cohen's-dindicates the size of the difference (effect size) between two
means in standard deviation units for each pairwise comparison of in-
terest, using the formula δ=μ
2
μ
1
/σ,whereδis the population pa-
rameter of Cohen's-d, and where it is assumed that σ
1
=σ
2
=σ,
i.e., homogeneous population variances, and μ
1
is the mean of the re-
spective population.
For ease and clarity of interpretation, the data were subsequently
collapsed across trials and days to produce a summary analysis of
groups within each experiment (used above). Standard deviations
(SD) were included in the text for all mean values. Signicance was con-
sidered to be p b0.05 for all analyses.
Results
Experiment 1
LACTs were signicantly and dramatically more effective at catching
crickets than NULLs. The LACTs' mean latency to catch the cricket =
63.95 ± 26.82 SD s; the NULL mean latency = 262.99 ± 58.13 SD s,
(F
1,22
=104.5,N=24,pb0.0001; Fig. 1a). This effect had a very high
strength; indeed, it was able to explain 83% of the variance (η
p
2
=0.83).
Tests of within-subjects effects showed a signicant effect of the par-
ity × day interaction when comparing predation latency between LACTs
and NULLs: whereas latency of predation decreased in LACTs (from
77 ± 54 SD s on Day one to 41 ± 16.00 SD s on Day three), it increased
in NULLs (from 248 ± 64 SD s on Day one to 268 ± 64 SD s on Day
three), (F
2,44
=5.65,N= 24, pb0.01). Therefore, the data suggest
that not only LACTs were better at catching crickets compared to
NULLs, but they also kept improving during the experiment, whereas
Fig. 1. Reproductive experience andregulation of predation. (1.1): Comparedto nulliparousfemales (NULLs),lactating mothers(LACTs) weresignicantly anddramatically fasterat catch-
ing prey. (1.2): When food-restricted for 20 h, NULLs appear neither more motivated nor better at capturing prey (theformer are the same as in[1.1]). (1.3): Temporarily-anosmic LACTs
(using ZnSO4-laced saline) are not signicantly different from controls (salinealone). (1.4): White-noise-masking prey appears not to affect predation latencies in LACTs versus controls.
(1.5): Trimming LACTs'vibrissae had no effect on latencies to catch preycompared to LACT shams.(1.6): Compared to lightedconditions (see 1.1), testing under0-lux conditions resulted
in signicantly increased latencies in LACTs, and signicantly reduced latencies in NULLs. (Values represent mean ± SEM of three trials over three days.)
##
: signicantly different,
pb0.0001. See main text for more experimental details.
651C.H. Kinsley et al. / Hormones and Behavior 66 (2014) 649654
NULLs showed little or no improvement. This treatment-by-day interac-
tion had a marginal strength, (η
p
2
= 0.27).
Experiment 2
As discussed, to control for potential differences in hunger motiva-
tion, Experiment 2 examined NULLs that were food-deprived for 20 h,
and compared to NULLs, which were food deprived for 10 h. The extra
food-restricted NULLs displayed mean latencies not dissimilar to those
food deprived for 10 h from Experiment 1, (F
1,20
=0.11,N= 22, ns).
(Experiments 36 investigated the possible sensory systems likely
involved in or regulating the results above.)
Experiment 3
Here, we examined olfactory regulation of the predatory behavior by
temporarily rendering anosmic LACTs (using naris-infusions of zinc sul-
fate [ZnSO
4
]). Here, there was a trend, and mean latencies were slightly,
but not signicantly, longer than saline-treated control LACTs (anos-
mics' mean latency = 93.07 ± 20.24 SD s; controls' mean latency =
74.97 ± 18.28 SD s; F
1,16
=3.96,N=18,p=0.064;η
p
2
=0.20).
Experiment 4
Here, we focused on the role of the auditory system by testing LACTs
in the presence of a white noise generator, thereby obscuring the
sound of the cricket moving about the enclosure. Mean latencies were
again similar to Experiment 1 (white noise-exposed LACTs' mean
latency = 68.33 ± 9.00 SD s; LACT non-white noise-controls' mean
latency = 71.68 ± 12.91 SD s; F
1,12
= 0.31, N=14,p= 0.59).
Experiment 5
Examined possible increased sensitivity to airborne vibrations in
LACTs, through vibrissae-versus-sham-removal. Vibrissae removal has
been shown to result in a lasting negative effect on prey capture, even
after vibrissae regrowth (Anjum et al., 2006; Anjum and Brecht,
2012). No effect on mean predation latencies was found (LACTs with vi-
brissae trimmed, mean latency = 80.80 ± 9.70 SD s; control LACTs'
mean latency = 73.96 ± 9.35 SD s; F
1,16
=2.32,N=18,p=0.15).
Experiment 6
Examined the role of visual regulation by testing NULLs and LACTs
under zero-lux conditions. This nal sensory manipulation, the only
one to have a signicant impact, reduced mean latencies in NULLs
(from 271 ± 63 SD s to 200 ± 91 SD s; F
1,16
=2.30,N=18,p=
0.036; η
p
2
= 0.18), while extending them in LACTs (from 67 ± 21 SD s
to 213 ± 71 SD s; F
1,18
=6.83,N= 20, p b0.0001; η
p
2
= 0.39), (relative
to results from Experiment 1).
Experiment 7
This experiment examined the progression of the behavioral im-
provement over the course of pregnancy, through Early (Days 46),
Mid (Days 1113) and Late (Days 1820) PREG. Paradoxically, as fe-
males become more cumbersome with advancing pregnancy (in the
present females, we found upwards of a 35% body weight increase),
they displayed a steady decrease in mean latencies to catch prey
(Early-PREG: 224 ± 28 SD s; Mid-PREG: 127 ± 80 SD s; Late-PREG:
124 ± 37 SD s; p = 0.001; η
p
2
=0.39;Fig. 2), with Early-PREG signi-
cantly different from both Mid-PREG and Late-PREG, whereas Mid-
PREG was not signicantly different from Late-PREG according to LSD
post-hoc tests (p b0.001; Cohen's d= .87; p = .908; Cohen's d= .05).
Discussion
These data suggest a remarkable enhancement of predation in the
rat with concurrent or rapidly-approaching maternity, persistence in
the face of specic sensory attenuation, and with heretofore unidenti-
ed changes to the visual system worth examining. The improvements
come at a crucial time; for the mother, time spent foraging is time re-
moved from vulnerable young. Increased efciencies, such as those as-
sociated with resource acquisition, translate into a lower cost:benet
ratio, better survivability odds for both mother and young, and maxi-
mized parental investment (Kinsley et al., 1999; Gatewood et al.,
2005). Further, that the behavioral enhancements come at a time, too,
when the mother is physically larger and more unwieldy compared to
her NULL counterpart (especially during mid-late pregnancy), suggests
a (likely) set of strong compensatory motor mechanisms that provide a
signicant boost to the female's behavioral repertoire. We have report-
ed positive modications to a constellation of strength and agility mea-
sures (Lambert and Kinsley, 2009), whichlikely would contribute to the
progressive improvement of predation with encroaching size and in-
creases in weight; herethe data show a translation of those motoric im-
provements into a practical benet.
Further, the observed motor paradox is akin to reported human
musculoskeletal changes that involve pregnancy-induced modications
of the vertebrae, an apparent compensation for bipedal obstetric fetal
load (Whitcome et al., 2007). Because the offspring place multiple de-
mands on mothers that are not required of nullipara, the data demon-
strate another avenue through which the maternal animal is able to
provide for her offspring. The data, therefore, add to the burgeoning pic-
ture of enhanced cognition and resourceful behavior in service to suc-
cessful reproduction. Again, adaptation is a hallmark of the maternal
brain.
Further, observations of the different predation strategies employed
by the mothers and NULLs denote some interesting contributionsto the
variability in their ultimate success. A typical bout between NULL and
cricket could be summed-up in a single word: inefcient. The animal
would take an angle on the prey that was more catch-up than capture,
resulting in attacks that missed their mark. The rat would chase the
cricket hither-and-thither, a haphazard pattern which, if displayed out-
side the connes of a testing arena, would itself likely attract the atten-
tion of predators. In some cases, once the NULL rat caught the cricket,
the cricket would slip the grasp and the chase would commence
again. The mother rats' behavior, however, was, in a word, economical.
Fig. 2. Reproductive experience and development of predation enhancement over the
course of pregnancy. With advancing pregnancy and increasing weightand its differen-
tial distributioncomes, counter-intuitively,improvementin predation latencies. Eachfe-
male from eachpregnancy group wasgiven three trials a day overthe course of three days
representing a phase of pregnancy. Data represent mean ± SEM for each trial. The three
groups of pregnant (PREG) subjects were dened as: Early (Days 46, n = 11); Mid
(Days 1114, n = 9); and Late (D ays 1820, n = 10). Both Mid-PREG and Late-PREG
were signicantly different from Early-PREG (at p b0.001), but neither was differen t
from each other.
652 C.H. Kinsley et al. / Hormones and Behavior 66 (2014) 649654
The capture trajectories appeared to be more direct and lethal. And the
maternal animals were much less likely to release the prey before the
typical kill-crunch denouement. The stark difference in latency to cap-
ture the prey, therefore, was likely due to the accumulation of incre-
mental motor and sensory (primarily visual?) adaptations. As the
overall data suggest, no one sensory system appears to be particularly
contributory to predation success, under our testing conditions, save
for vision.
With regard to vision, Experiment 6 suggests a role for sight in the
enhanced predationof mothers,but it is a conclusion requiring caution.
Our logic concerning this interpretation relies upon the following planks
for support and extension. First, there is a marked difference in preda-
tion efciency between animals tested in the light (where most of the
current work took place), and a completely darkened room. In the for-
mer state, and examining just reproductive state, mothers clearly out-
perform the NULLs. In the dark, however, the advantage is reversed,
and the NULLs' latencies resemble those of the light-tested mothers.
We believe that the difference between light and dark in the case of
the NULLs relates to allowing for their more natural nocturnal tenden-
cies to play out. Rats are normally active at night; requiring NULLS
which we and others have demonstrated are more anxious than parous
females (Wartella et al., 2003)to forage in the light, may exacerbate
their baseline fearfulness. The dark partially removes that wariness;
consequently, latencies improve.
In the case of the mothers, whose rest-to-activity schedule ratio is
signicantly truncated and variable due to the changing and insistent
demands of the developing pups, foraging may shift from adult to off-
spring initiated. That is, whereas previously the pup-free female could
forage primarily in the dark, new demands place new constraints on
the mother. A subtle shift in visual acuity perhaps allows the female to
adapt to, and rely on, its increasing role in predation ability. Removing
that advantage by requiring predation under 0-lux conditions may ex-
pose this dependence. Hence, these females' latencies increase. One ob-
servation may be illuminating. We observed a virgin animal at sixes-
and-sevensas she attempts to chase-down the cricket. As she nears
the far corner, she misjudges the distance and bumps her snout against
the wall. It is but a single example, but it looked as if her depth percep-
tion was compromised. In contrast, a LACT female under identical con-
ditions stops and looks in the direction of a cricket placed in the arena,
moves swiftly toward it, and using the shortest distance required to in-
tercept it, pounces and quickly devours it. A LACT female having become
reliant on an improvement in vision, available in the light, may see that
advantage disappears if tested in pitch dark. To summarize, mothers
must hunt and forage when opportunity presents including in the
dark. NULLs have no such exigency. If, as the data suggest, some facet
of eyesight improves, may be employed and relied-upon, and then is
disrupted (as by testing in the dark) latencies could be expected to
increase.
Predation is an important component of the mother's suite of
behaviors, here presented as supportive of maternal behavior in the
sense that enhancements would be expected to aid the female in main-
taining the higher metabolic rate characteristic of pregnancy and lacta-
tion. Together with foraging, predation, especially effective/efcient
predation, represents an opportunity for the mother to obtain resources
for her offspring that can complement other sources of food and the
strategies employed to acquirethem. Insects, virtually fully protein, pro-
vide the mother with nutrients of the sort most valuable to her and her
metabolicallycostly charges. Being able to obtain them economically
and prociently helps the mother minimize energetic costs to herself,
while maximizing thebenets to her and the litter. Because the mother
is feeding better, her offspring are fed better.
Brain regions that regulate various facets of maternal and ancillary
responses show changes over the course of reproduction. Previous
work has shown signicant pregnancy hormone stimulation of neuro-
nal somal volumes in the medial preoptic area (mPOA), a site crucial
for the display of maternal behavior (Keyser et al., 2001). Other research
has shown that a similar pregnancy hormone regimen stimulates an in-
crease in dendritic spine concentrations in the CA1 region of the female
hippocampus, presumably contributing to the enhanced spatial and
other learning reported in mothers compared to nulliparous females
(Kinsley et al., 2006). The degree to which the effects reported here re-
late to enhanced learning and memory are arguable, but it is unlikely
that they do not play a role. As suggested above, perhaps there is an
efciency of the calculation of the assumed projected parabolic
trajectoryinvolved between two moving objects mother and prey
as they converge, much like a baseball outelder chases down a y
ball (McBeath et al., 1995).
The nal sensory experiment, on the visual system, also heralds an
interesting set of research possibilities. Prolactin-induced regulation of
retinal cell activity (Rivera et al., 2008) has been reported, together
with evidence of αand βestrogen receptor expression in the cornea;
hence, pregnancy hormones, through an as yet unidentied mecha-
nism, may mediate some visual contribution to the predatory enhance-
ments reported here (Tachibana et al., 2000).
Regarding predation, Felicio and colleagues have demonstrated that
the periaqueductal gray (PAG), in rats, crucial for the expression of de-
fensive responses, plays a major role in the expression of predation, as
well; in fact, the PAG appears to regulate an interesting form of behav-
ioral choice (Sukikara et al., 2006), in which the rostral lateral PAG
(rlPAG) inuences switching from maternal to hunting behavior in
morphine-treated dams, choosingbetween adaptive behavioral re-
sponses, either hunting of prey (in this case, cockroaches) or engaging
in pup-directed behaviors. The rlPAG is implicated in this behavioral
switch as lesions therein impair predation and restore the maternal
response. The lateral PAG receives projections from the superior
colliculus, a midbrain region known to be important for controlling vi-
suospatial orienting (Grobstein, 1988). Recently, it has been demon-
strated that these projections are functionally relevant for predatory
hunting (Furigo et al., 2010). The rlPAG inuences switching from ma-
ternal to hunting behavior in morphine treated dams, thus supporting
a previously unsuspected role for the PAG in the selection of adaptive
behavioral responses. The regulation represented here may be relevant
for improving survival chances in food-lacking or aversive environ-
ments (Sukikara et al., 2006, 2007). Interestingly, it is possible that
choosingto forage or remain in the nest during the day may also in-
volve the PAG.
Additionally, the hypothalamus, which is rich in orexinegic (and,
hence, appetitive-modulating) innervation, undergoes plastic changes
throughout and following reproductive experience. Its efferents include
the PAG, whichMota-Ortiz and colleagueshave shown to play a decisive
role in the behavioral switching between maternal and predatory be-
haviors (Mota-Ortiz et al., 2012). Perhaps some of the improvementsre-
ported here involve similar systems or sensorimotor modications/
enhancements; some changes along those lines could be playing a role
in modulating the prey object's value: as we observed in Experiment
2, although there doesnot appearto be an increase in the hedonic prop-
erties of the cricket in extra-hungry NULLs, we cannot rule out a similar
baseline effect in our mothers. Just as a thirsty man is more careful with
the rare cup of water, perhaps a maternal female is more efcient when
attacking and capturing prey.
Predatorprey interactions play a major role in determining the pat-
terns of the history of lifeon this planet (Abrams, 2000; Bergstrom et al.,
2009). A delicate balance is essential for the proper (or natural) evolu-
tion of predatorprey relationships. Imbalances favoring one or the
other until privation, either too effective predation, with consequent
loss of prey availability, or having prey that are too elusive, which may
allow them to outstrip the local environment, may force an adaptation
that reverses the counter-advantage. Either way, modications to pre-
dation, even temporary ones, represent signicant effects on a funda-
mental behavioral repertoire. That the changes appear to favor
mothers is simultaneously logical, tting, and advantageous, as they
would be expected to reduce the mounting reproductive costs to the
653C.H. Kinsley et al. / Hormones and Behavior 66 (2014) 649654
female. Hence, as reported here, even a temporal improvement in pred-
atory responses, as would occur following reproduction, may be signif-
icant at a number of levels.
In closing, maternally-enhanced aggressiveness and hunting skill,
together with a variety of germane neuroplastic changes, may be char-
acteristic of mothersacross a number of species faced with the pros-
pect of reproduction in an unforgiving environment. Beach, in an
interesting parity effect parallel to what we describe here, reported
that female mosquitoes transform from passive creatures to the noi-
some organism with which we are all-too-familiar due to hormone-
induced modications necessary to provide a blood meal for their de-
veloping offspring (Beach, 1979). In social wasps, exposure to young
or reproduction itself leads to the expression of a wide number of
genes (Toth et al., 2007), with telling effects on a cluster of insulin-
related peptides. The latter are themselves implicated in hippocampal
function, synaptogenesis, and memory in mammals (rats; Wan et al.,
1997), as well as neuroprotection (Dore' et al., 1997) of the sort ob-
served above (Gatewood et al., 2005). Collectively, our data may simply
illustrate the evolutionary and developmental underpinnings in re-
sponse to the demands placed upon mothers of all species. Changes rec-
ognized and mythologized by the ancients in the form of Artemis, the
Greek Goddess of childbirth and of the hunt the epitome of the com-
plementary activities required of the mother.
Acknowledgments
Thank you to Thomas Wooldridge (Virginia Commonwealth Univer-
sity) for his helpful background research. The authors would like to
thank the National Science Foundation (BCS-1126471; BCS-0619544);
the Grainger Foundation; and the Howard Hughes Medical Institute
(HHMI) (52007567) for their support. Also, the authors want to express
their gratitude for the continuous support by the University of Rich-
mond for the research and scholarship carried out by its students and
faculty.
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We describe and review maternal behavior in mammals (viz., rodents, rabbits, and ungulates), and the participation of steroid/peptide hormones in its regulation (e.g., nest-building, nursing, and aggression). We discuss the neurobiology involved in the onset and offset of specific behavioral patterns and the transmission and interpretation of signals from the young, which facilitate the offspring's development. The impact of mothering styles on the psychobiological development of organisms and their emotional reactivity as adults is addressed, as well as the epigenetic mechanisms participating in the intergenerational transmission of such acquired traits. We also discuss the ancillary and complementary changes that occur to the mother's brain and behavior, which support the display of care and protection for young, and which extend to well beyond the peripartum and lactation periods of the mother's life. Such behavioral alterations, among them enhanced cognition and reductions in fear and anxiety, translate into more efficient behavior and a cost:benefit ratio that favors the survival of both mother and young. We draw attention to topics that merit further investigation (e.g., epigenetic transmission of behavior in mammals other than rodents and mechanisms involved in the facilitation of cognition by motherhood) and to little explored issues (e.g., placentophagia, nest-building, and food preferences).
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The Neurobiology of Parental Behavior takes an integrative approach that analyzes the neural underpinnings of parental behavior in mammals, including humans.
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This article reviews some recent findings on the character of the neuronal organization lying between the optic tectum and motor pattern-generating circuitry in the case of orienting behaviors. It focuses on frogs but notes parallels to existing work on saccade control in mammals and suggests some additional ones for further exploration. In general, the map-like function of orienting does not appear to be subserved by a comparable map-like organization. It is argued that the current conceptual vocabulary for describing interface organization (sensory map, motor map, pattern-generating circuitry) is inadequate and that some additional concepts (activity-gated divergence, intermediate spatial representation) are necessary. Finally, some questions are raised about the appropriateness of the term 'motor map’.Copyright © 1988 S. Karger AG, Basel
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The hormones of pregnancy may prepare sites that regulate learning and memory, in much the same way that they stimulate the medial preoptic area to respond with maternal behavior when pups are born. This study investigated this idea by testing multiparous (animals that had given birth and lactated twice) and age-matched nulliparous (virgin) female rats on a 16-day regimen of radial-arm maze tests. On the 1st 6 days, multiparous Ss made significantly more correct choices than nulliparous females. In a 2nd experiment, virgin female rats were assigned to 1 of 3 groups: fosters, maternals, and nulliparous. In the dry-land version of the Morris watermaze, maternal Ss took significantly less time than nulliparous Ss to recall and locate the food reward. No significant differences were observed between foster and maternal rats. These results show that a combination of reproductive and pup experience and stimulation is beneficial to learning and memory in female rats. Findings indicate that hormone-induced modifications to the hippocampus may improve the navigation skills involved in parental resource-gathering behaviors. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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