Paralemniscal TIP39 is induced in rat dams and may participate in maternal functions

Abstract

The paralemniscal area, situated between the pontine reticular formation and the lateral lemniscus in the pontomesencephalic tegmentum contains some tuberoin-fundibular peptide of 39 residues (TIP39)-expressing neurons. In the present study, we measured a 4 times increase in the level of TIP39 mRNA in the paralemniscal area of lactating mothers as opposed to nulliparous females and mothers deprived of pups using real-time RT-PCR. In situ hybridization histochemistry and immunolabeling demonstrated that the induction of TIP39 in mothers takes place within the medial paralemniscal nucleus, a cytoarchitectonically distinct part of the paralemniscal area, and that the increase in TIP39 mRNA levels translates into elevated peptide levels in dams. The paralemniscal area has been implicated in maternal control as well as in pain perception. To establish the function of induced TIP39, we investigated the activation of TIP39 neurons in response to pup exposure as maternal, and formalin injection as noxious stimulus. Both stimuli elicited c-fos expression in the paralemniscal area. Subsequent double labeling demonstrated that 95% of neurons expressing Fos in response to pup exposure also contained TIP39 immunoreactivity and 91% of TIP39 neurons showed c-fos activation by pup exposure. In contrast, formalin-induced Fos does not co-localize with TIP39. Instead, most formalin-activated neurons are situated medial to the TIP39 cell group. Our data indicate that paralemniscal neurons may be involved in the processing of maternal and nociceptive information. However, two different groups of paralemniscal neurons participate in the two functions. In particular, TIP39 neurons may participate in the control of maternal functions.

Thalamic integration of social stimuli regulating parental behavior and the oxytocin system

“…2) and peptide level in the postpartum period, starting at parturition and lasting until weaning of the pups, indicating that TIP39 levels remain elevated throughout lactation (Cservenak et al, 2010; Cservenák et al, 2013). In addition, the pontine site of TIP39 expression, the medial paralemniscal nucleus (Varga et al, 2008), also showed maternal induction, albeit to a lesser degree than the PIL (Varga et al, 2012). Interestingly, TIP39 was not induced at all in the periventricular gray of the thalamus, rather a tendency for further decrease was found there (Cservenak et al, 2010; Cservenák et al, 2013), so the major site of expression of TIP39 in the forebrain of mothers is the PIL (Fig.…”

Thalamic neuropeptide mediating the effects of nursing on lactation and maternal motivation

“…TIP39 levels decrease markedly in all three areas during early postnatal development (Dobolyi et al, 2006b; Brenner et al, 2008). We previously found that in postpartum day 9 dams TIP39 levels are dramatically elevated over that of non-lactating dams in the PIL and the medial paralemniscal nucleus, but not in the periventricular gray of the thalamus (Cservenak et al, 2010; Varga et al, 2012). We also observed that pup exposure induces Fos in TIP39 neurons of the PIL and the medial paralemniscal nucleus (Cservenak et al, 2010; Varga et al, 2012).…”

“…We previously found that in postpartum day 9 dams TIP39 levels are dramatically elevated over that of non-lactating dams in the PIL and the medial paralemniscal nucleus, but not in the periventricular gray of the thalamus (Cservenak et al, 2010; Varga et al, 2012). We also observed that pup exposure induces Fos in TIP39 neurons of the PIL and the medial paralemniscal nucleus (Cservenak et al, 2010; Varga et al, 2012). In addition, the body weight of pups reared by dams lacking TIP39 signaling is reduced during the lactation period (Coutellier et al, 2011).…”

Preoptic Inputs and Mechanisms that Regulate Maternal Responsiveness

“…Tip39 is expressed in two thalamic and a pontine site and almost completely disappears from the brain by the end of pubertal development . However, it is induced dramatically in lactating mothers in the posterior intralaminar complex (PIL) of the thalamus immediately ventromedial to the medial geniculate body and the medial paralemniscal nucleus but not the third site of its expression in the periventricular gray of the thalamus. The vast majority of neurones with induced Tip39 expression are labelled with Fos in response to suckling .…”

“…However, it is induced dramatically in lactating mothers in the posterior intralaminar complex (PIL) of the thalamus immediately ventromedial to the medial geniculate body and the medial paralemniscal nucleus but not the third site of its expression in the periventricular gray of the thalamus. The vast majority of neurones with induced Tip39 expression are labelled with Fos in response to suckling . The active role of Tip39 in mediating the suckling reflex was demonstrated by the near complete blockade of suckling‐induced prolactin release by a Pth2r antagonist .…”