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

Abstract

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. P ostpartum rats are highly aggressive toward other animals that enter the vicinity of their nest and pups, with the presumed function of protecting their offspring from harm (1). Maternal aggression is under the control of a wide variety of factors that prime the females for aggression or trigger the aggressive event. The priming of maternal aggression in laboratory rats relies first on the hormonal changes associated with late pregnancy and parturition, and then on exteroceptive stimulation from the pups (2-6). Maternal attacks are triggered by the perception of polymodal sensory cues from the intruder (7). Information from the main olfactory pathway is crucial for high maternal aggression, although any importance for accessory olfactory inputs is less clear (5, 6). Furthermore, somatosensory signaling from the perioral region of the dams' face while they investigate an intruder is critical for attacks (8).Considering the overlap of sensory modalities involved in how offspring cues prime maternal aggression and those involved in how intruders trigger aggressive behavior, experimental approaches that permanently destroy a sensory system are difficult to interpret because the result observed could be due to altered priming or altered triggering of the behavior. For that reason, identifying a brain area that specifically responds to the intruder as a threat would clarify what sensory info...

Expression of a novel serine/threonine kinase gene, Ulk4, in neural progenitors during Xenopus laevis forebrain development

“…The BH is also part of the neuroendocrine system and plays an essential role in the integration of the neuroendocrine and homeostatic functions. This territory is dealing with the control of physiological processes such as the modulation of aggressive behavior, homeostatic regulation of feeding and normal control of daily rhythms of a variety of physiological parameters including corticosterone secretion, body temperature, sleep and locomotor activity (Chou et al, 2003;Gooley et al, 2006;Motta et al, 2013;Saderi et al, 2014). Our results in Xenopus, have shown extensive xUlk4 expression in these basal hypothalamic regions during development and also in the adult, with xUlk4 expression in the mammillary region being particularly high.…”

The neurobiology of offensive aggression: Revealing a modular view

“…However, there is abundant evidence that the PMV is also closely involved in aggression as demonstrated by the pronounced c-fos activation in this area by male and female rats and mice that displayed aggression towards conspecifics. In addition, lesioning this region profoundly reduces aggressiveness [61,114,115]. This focuses our attention again on tiny groups of neurons, sometimes indicated as 'clusters' [116][117][118] when hardly any specific anatomical characteristics were available to differentiate them from surrounding neurons.…”

“…These ideas were strongly influenced by the Nobel prize-winning work of Walter Rudolf Hess [5] and others on brain stimulation and lesion-induced changes in feeding, sexual and aggressive activities, as well as the work of Paul Weiss [207] and Karl Lashley [208] on the hierarchical organization of (motor) behavior. This view was strengthened by the fact that research of the various types of Physiology & Behavior 146 (2015) [111][112][113][114][115][116][117][118][119][120][121][122][123][124][125][126][127] behavior has developed more or less independent from each other. Scientists working on for example aggressive behavior usually did not consider sexual behavior or feeding or any other type of behavior.…”

Acute Lipopolysaccharide Switches the Selection of Maternal Behavior to Predatory Behavior in Female Rats

“…Maternal attacks are triggered by the perception of sensory cues from the intruder, and the ventral premammillary nucleus of hypothalamus is highly responsive to the male intruder [38] , transferring this information to the network organizing MA as the medial preoptic nucleus, ventrolateral part of the ventromedial hypothalamic and the ventral part of the anterior bed nuclei of the stria terminalis, and the lateral and ventrolateral caudal PAG [39] .…”