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FRANZ ET AL.
mesencephalon, ventral tegmental area, median and dorsal
raphe nuclei, midbrain reticular formation, and pontine cen-
tral gray [5, 10, II, 36, 56, 59].
Since many of the descending projections of the MPO
course through the MFB, and since the MFB is an important
pathway connecting the basal forebrain and hypothalamus
with lower brainstem areas (see [35,36] for review), it is not
surprising that bilateral knife cuts that sever the connections
between the MPO and the MFB disrupt maternal behavior
[29-31, 39, 41, 57, 60]. Numan and his colleagues have re-
cently suggested that a particular subset of these descending
lateral MPO projections—those that course laterally into the
lateral preoptic area, then from there through the dorsal
MFB to the ventral tegmental area—are critical for
postpartum maternal behavior [42, 43, 45]. Numan et al. [42]
concluded that although surgical interruption of MPO effer-
ents that descend directly to the brainstem via the ventral
portion of the MFB may induce some transient effects on
postpartum maternal behavior, these efferents are not es-
sential for such maternal behavior. On the other hand, since
surgical damage of the dorsal portion of the MFB, perhaps
because of the interruption of MPO efferents within the
MPO-Iateral preoptic-ventral tegmentum circuit, produces
severe deficits in maternal behavior, this pathway is critical
for the expression of postpartum maternal behavior.
There is also some evidence to suggest that other lateral
MPO projections, which do not descend through the MFB
but instead descend in the region of the supraoptic commis-
sures, may also be important for the onset of pup retrieval
and nursing behavior in both postpartum and virgin rats con-
tinuously housed with foster pups [29-31].
Since the initiation of placentophagia (ingestion of the
afterbirth) and infant-directed caretaking behavior occur in
close temporal contiguity during or after parturition in most
mammals-, and'since placentophagia can be conceptualized
as both a maternal and an ingestive behavior, one might
expect that these behaviors are governed by related physi-
ological mechanisms. Furthermore, research has confirmed
that the physiological control mechanisms for placen-
tophagia in primiparae are different from those in multiparae,
and control mechanisms in virgins are different from those in
parturient rats (see [22] for review). Kristal and his col-
leagues found that lateral hypothalamic lesions that elimi-
nated feeding and drinking also eliminated placentophagia in
nonpregnant nulliparae presented with placentas obtained
from donor females, and in rats giving birth for the first time,
but did not eliminate placentophagia in nonpregnant mul-
tiparae presented with donor placenta, or in rats giving birth
for the second time [21,37]. Likewise, Noonan and Kristal
[38] found that medial MPO lesions had no effect on placen-
tophagia in virgins, but that such lesions did disrupt placen-
tophagia at parturition. They also found that such MPO le-
sions also produce deficits in postpartum maternal behavior.
Taken together, the results of these studies suggest that the
physiological mechanisms that regulate placentophagia in
nonpregnant rats are different from those that regulate
placentophagia in parturient rats, and that postpartum ma-
ternal behavior and placentophagia may have some common
neural elements.
Since MPO lesions disrupt parturitional placentophagia as
well as postpartum caretaking behavior in primiparae, and
since lateral hypothalamic lesions eliminate parturitional
placentophagia in primiparae, it is plausible that connections
between the MPO and the lateral hypothalamus are impor-
tant for the onset of both behaviors at parturition. With re-
gard to pup-directed maternal behavior, this hypothesis is
strongly supported by the finding that knife cuts that sever
the lateral connections of the MPO and that disrupt maternal
behavior necessarily sever axons connecting the MPO and
lateral hypothalamus, and by the finding of several inves-
tigators that deficits in postpartum maternal behavior are
evident after lesions or knife cuts that damage the lateral
hypothalamus, and after lesions or knife cuts that damage
the MFB as it courses through the lateral hypothalamus [1-3,
21, 42]. With regard to parturitional placentophagia, the im-
portance of MPO-Iateral hypothalamic pathways is sup-
ported by the results from Kristal’s laboratory showing that
MPO lesions disrupt parturitional placentophagia as well as
pup-directed maternal behavior, and that lateral hypotha-
lamic lesions disrupt parturitional placentophagia in
primiparae.
In summary, the MPO and its lateral connections are im-
portant for the initiation of placentophagia and pup-directed
maternal behavior in parturient rats, for the maintenance of
maternal behavior in Iactating primiparous rats, for the hor-
monal induction of maternal behavior in hysterectomized-
Ovariectomized pregnant rats, and for pup-induced maternal
behavior in virgin rats. The importance of the MPO apd its
lateral connections for placentophagia and maternal behav-
ior in multiparae, however, has not yet been investigated. It
is possible that the degree of importance differs in nulliparae,
primiparae and multiparae, since the physiological mech-
anisms that operate to produce placentophagia and the rapid
onset of maternal behavior during the first parturition may
not be the same mechanisms that operate during subsequent
parturitions, or that operate in virgins to produce placen-
tophagia or pup-induced maternal behavior [6-8, 16, 21, 22,
30, 32-34, 50, 51].
The two studies presented here were designed to deter-
mine (a) whether the integrity of the longitudinal system
consisting of fibers running from the MPO to the lateral
preoptic area and then descending through the MFB is im-
portant for the initiation of pup-directed maternal behavior at
parturition, (b) whether this system is also important for
placentophagia at parturition, and (c) whether parturitional
experience affects this hypothalamic control system. Ac-
cordingly, Experiment I addressed the hypothesis that the
initiation of placentophagia and the rapid onset of nestbuild-
ing and pup-directed maternal behavior in parturient
primiparae are mediated by connections between the MPO
and the MFB. This was done by comparing the effects of
bilateral knife cuts on the lateral border of the MPO with
bilateral knife cuts of the posterior MFB, and with knife cuts
combining a unilateral MPO cut with a contralateral MFB
cut (asymmetrical cuts). Those behaviors disrupted by all
three types of knife cuts can therefore be considered to be
controlled by a continuous functional system linking the
MPO and the MFB. Use of the asymmetrical knife-cut de-
sign rests on the assumption that the connections between
the MFB and the MPO must be severed bilaterally in order to
produce deficits [18,46]. This assumption is supported by
findings to be reported here that animals with unilateral knife
cuts are not different from animals with sham knife cuts.
Also, within the framework of this design, we compared the
effects of the different knife cuts on each of several different
behaviors characteristic of maternal female rats. Behavioral
observations of all groups therefore included tests of placen-
tophagia, nestbuilding, retrieving, crouching, and pup-
licking. Finally, since Kristal has shown that the behavior of
nonpregnant rats towards placenta is dichotomous—they