Nucleus of the lateral olfactory tract: A hub linking the water homeostasis‐associated supraoptic nucleus‐arginine vasopressin circuit and neocortical regions to promote social behavior under osmotic challenge

Abstract

Homeostatic challenges may alter the drive for social interaction. The neural activity that prompts this motivation remains poorly understood. In the present study, we identify direct projections from the hypothalamic supraoptic nucleus to the cortico‐amygdalar nucleus of the lateral olfactory tract (NLOT). Dual in situ hybridization with probes for pituitary adenylate cyclase‐activating polypeptide (PACAP), as well as vesicular glutamate transporter (VGLUT)1, VGLUT2, V1a and V1b, revealed a population of vasopressin‐receptive PACAPergic neurons in NLOT layer 2 (NLOT2). Water deprivation (48 h, WD48) increased sociability compared to euhydrated subjects, as assessed with the three‐chamber social interaction test (3CST). Fos expression immunohistochemistry showed NLOT and its main efferent regions had further increases in rats subjected to WD48 + 3CST. These regions strongly expressed PAC1 mRNA. Microinjections of arginine vasopressin (AVP) into the NLOT produced similar changes in sociability to water deprivation, and these were reduced by co‐injection of V1a or V1b antagonists along with AVP. We conclude that, during challenge to water homeostasis, there is a recruitment of a glutamatergic‐multi‐peptidergic cooperative circuit that promotes social behavior.

Morphological signatures of neurogenesis and neuronal migration in hypothalamic vasopressinergic magnocellular nuclei of the adult rat

“…Connections between hypothalamic AVP-MCNs and other brain areas involved in stress coping and emotional/motivational behaviors have been demonstrated, through the employment of techniques such as juxtacellular labeling and tract-tracing methods combined with brain serial sectioning in cutting planes at coronal, sagittal, septo-temporal oblique and horizontal orientations. Histochemical reaction against neurobiotin, immunohistochemistry (IHC) against antigens of interest and systematic neuroanatomical analyses were performed (Zhang and Hernandez 2013, Hernandez, Vazquez-Juarez et al 2015, Hernandez, Hernandez et al 2016, Zhang, Hernandez et al 2016, Campos-Lira, Kelly et al 2018, Hernandez-Perez, Hernandez et al 2019, Hernandez-Perez, Hernandez et al 2022). During these studies, a collateral observation was repeatedly made: AVP immunoreactive (AVP-ir) magnocellular neurons seemed to be dispersed from the above-mentioned loci to adjacent subcortical regions.…”

“…With the observations mentioned above, we then asked if neurogenesis could be modified as an allostatic mechanism for stress adaptation. AVP-MNNs are able to respond to homeostatic challenges by increasing their metabolic activity generating physiological changes in dehydrated rats (Zhang, Hernandez et al 2016, Zhang, Hernandez et al 2018, Hernandez-Perez, Hernandez et al 2022. A recent comprehensive transcriptomic study has reported change of 2247 RNA transcripts, including Ephrin receptor 6, a gene related to adult neurogenesis, in the SON of Wistar Han rats, after 3 days of water deprivation (Pauza, Mecawi et al 2021).…”

Synaptic connectivity and electrophysiological properties of the nucleus of the lateral olfactory tract

“…Second, odor responses in NLOT are strongly influenced by odor valence (Tanisumi et al, 2021), similarly to the olfactory tubercle (OT) (Gadziola et al, 2015; Millman and Murthy, 2020). Third, perturbation of NLOT activity affects social behavior in rats, that is known to rely on olfaction and be affected by emotional state (Hernández-Pérez et al, 2022). Lastly, NLOT neurons show marked transcriptomic changes following fear conditioning (Hochgerner et al, 2023).…”

“…Layer 2 contains most of NLOT neurons. However, unlike PC, layer 2 neurons are almost exclusively glutamatergic, pyramidal-like neurons (McDonald, 1983; Millhouse and Uemura-Sumi, 1985; Hernández-Pérez et al, 2022). These send their apical dendrites ventrally into layer 1 where they branch and form synaptic connections with olfactory bulb mitral cell axons.…”

Advances in peptide modulation in systems physiology

“…everyone at the conference in efforts aimed at overcoming intellectual dead-ends, creating new conceptualizations for regulatory peptide research, and promoting international collaborations for solving common problems with complementary expertise and technology. The Hernandez-Perez et al 1 provide a novel example of how two neuropeptides, vasopressin and pituitary adenylate cyclase-activating polypeptide (PACAP), interact to transmit prosocial need when the organism is under homeostatic challenge, by a circuit from the hypothalamus to the cortex via a 'hub' in the amygdaloid complex. In line with this, Peles et al 2 provide new evidence on shaping of the regulatory peptide architecture and action within the stress axis in the adult zebrafish, and what can be learned with this versatile model organism.…”