Ventral premammillary nucleus as a critical sensory relay to the maternal aggression network.

Maternal aggression is under the control of a wide variety of factors that prime the females for aggression or trigger the aggressive event. Maternal attacks are triggered by the perception of sensory cues from the intruder, and here we have identified a site in the hypothalamus of lactating rats that is highly responsive to the male intruder--the ventral premammillary nucleus (PMv). The PMv is heavily targeted by the medial amygdalar nucleus, and we used lesion and immediate-early gene studies to test our working hypothesis that the PMv signals the presence of a male intruder and transfers this information to the network organizing maternal aggression. PMv-lesioned dams exhibit significantly reduced maternal aggression, without affecting maternal care. The Fos analysis revealed that PMv influences the activation of hypothalamic and septal sites shown to be mobilized during maternal aggression, including the medial preoptic nucleus (likely to represent an important locus to integrate priming stimuli critical for maternal aggression), the caudal two-thirds of the hypothalamic attack area (comprising the ventrolateral part of the ventromedial hypothalamic nucleus and the adjacent tuberal region of the lateral hypothalamic area, critical for the expression of maternal aggression), and the ventral part of the anterior bed nuclei of the stria terminalis (presently discussed as being involved in controlling neuroendocrine and autonomic responses accompanying maternal aggression). These findings reveal an important role for the PMv in detecting the male intruder and how this nucleus modulates the network controlling maternal aggression.

The periaqueductal gray as a critical site to mediate reward seeking during predatory hunting.

Previous studies using morphine-treated dams reported a role for the rostral lateral periaqueductal gray (rlPAG) in the behavioral switching between nursing and insect hunting, likely to depend on an enhanced seeking response to the presence of an appetitive rewarding cue (i.e., the roach). To elucidate the neural mechanisms mediating such responses, in the present study, we first observed how the rlPAG influences predatory hunting in male rats. Our behavioral observations indicated that bilateral rlPAG NMDA lesions dramatically interfere with prey hunting, leaving the animal without chasing or attacking the prey, but do not seem to affect the general levels of arousal, locomotor activity and regular feeding. Next, using Phaseolus vulgaris-leucoagglutinin (PHA-L), we have reviewed the rlPAG connection pattern, and pointed out a particularly dense projection to the hypothalamic orexinergic cell group. Double labeled PHA-L and orexin sections showed an extensive overlap between PHA-L labeled fibers and orexin cells, revealing that both the medial/perifornical and lateral hypothalamic orexinergic cell groups receive a substantial innervation from the rlPAG. We have further observed that both the medial/perifornical and lateral hypothalamic orexinergic cell groups up-regulate Fos expression during prey hunting, and that rlPAG lesions blunted this Fos increase only in the lateral hypothalamic, but not in the medial/perifornical, orexinergic group, a finding supposedly associated with the lack of motivational drive to actively pursue the prey. Overall, the present results suggest that the rlPAG should exert a critical influence on reward seeking by activating the lateral hypothalamic orexinergic cell group.

The periaqueductal gray and its potential role in maternal behavior inhibition in response to predatory threats.

Animals faced with conflicting cues, such as predatory threat and a given rewarding stimulus, must make rapid decisions to engage in defensive versus other appetitive behaviors. The brain mechanisms mediating such responses are poorly understood. However, the periaqueductal gray (PAG) seems particularly suitable for accomplishing this task. The PAG is thought to have, at least, two distinct general roles on the organization of motivated responses, i.e., one on the execution of defensive and reproductive behaviors, and the other on the motivational drive underlying adaptive responses. We have presently examined how the PAG would be involved in mediating the behavioral choice between mutually incompatible behaviors, such as reproduction or defense, when dams are exposed to pups and cat odor. First, we established the behavioral protocol and observed that lactating rats, simultaneously exposed to pups and cat odor, inhibited maternal behavior and expressed clear defensive responses. We have further revealed that cat odor exposure up-regulated Fos expression in the dorsal PAG, and that NMDA cytotoxic lesions therein were able to restore maternal responses, and, at the same time, block defensive responsiveness to cat odor. Potential paths mediating the dorsal PAG influences on the inhibition of appetitive (i.e., retrieving behavior) and consummatory (i.e., nursing) maternal responses are discussed. Overall, we were able to confirm the dual role of the PAG, where, in the present case, the dorsal PAG, apart from organizing defensive responses, also appears to account for the behavioral inhibition of non-defensive responses.

Afferent connections to the rostrolateral part of the periaqueductal gray: a critical region influencing the motivation drive to hunt and forage.

Previous studies have shown that a particular site in the periaqueductal gray (PAG), the rostrolateral PAG, influences the motivation drive to forage or hunt. To have a deeper understanding on the putative paths involved in the decision-making process between foraging, hunting, and other behavioral responses, in the present investigation, we carried out a systematic analysis of the neural inputs to the rostrolateral PAG (rlPAG), using Fluorogold as a retrograde tracer. According to the present findings, the rlPAG appears to be importantly driven by medial prefrontal cortical areas involved in controlling attention-related and decision-making processes. Moreover, the rlPAG also receives a wealth of information from different amygdalar, hypothalamic, and brainstem sites related to feeding, drinking, or hunting behavioral responses. Therefore, this unique combination of afferent connections puts the rlPAG in a privileged position to influence the motivation drive to choose whether hunting and foraging would be the most appropriate adaptive responses.