Year: 2017
Type: article
Abstract: The neurohormone oxytocin is an important regulator of social behavior across species. Primarily synthesized in the paraventricular nucleus of the hypothalamus (PVN), oxytocin neurons project to various parts of the brain and modulate behaviors in sex-, brain region–, and context-specific ways [reviewed in Caldwell and Albers (1)]. Many of the brain nuclei that contain oxytocin receptors are a part of the social behavior neural network (SBNN) (2). These nuclei or “nodes” include, but are not restricted to, the extended amygdala, the bed nucleus of the stria terminalis, the medial preoptic area, and the anterior hypothalamus. Social behaviors are an emergent property of the reciprocal connections between these nuclei. However, the SBNN cannot function in isolation; sensory information must be relayed to nodes within the network to provide information about an animal’s social context. But what exactly is social context? Although it is perhaps intuitive that social context refers to the physical and social setting in which an animal finds itself, how will this information ultimately be integrated and used to help determine the appropriate behavioral response? To date, most research in nonprimate mammals has focused on chemosensory input into the SBNN. For instance, it is known that both the main and accessory olfactory systems interact with the oxytocin system, potentially affecting odor processing in key brain regions such as the medial amygdala, the bed nucleus of the stria terminalis, and the medial preoptic area–anterior hypothalamus (3–5). However, chemosensory input is not the only sensory input that is important for conveying information relevant to social context. Furthermore, little is known about how social context may alter the activity of PVN oxytocin neurons. Fortunately, in this issue of Endocrinology, an article by Cservenák et al. (6) sheds light on how other types of sensory input specifically somatosensory information, alters PVN oxytocin activity in females. It has been known for some time that A1/A2 noradrenergic inputs from the brainstem, which convey somatosensory information to the PVN (7), can affect pituitary magnocellular neuron-mediated oxytocin release (8) in the context of oxytocin-dependent milk letdown (9). However, little to nothing is known about how information associated with social context may alter PVN-regulated oxytocin neurons that project centrally. Using a combination of immunohistochemistry, electron microscopy, in situ hybridization, retrograde labeling, and c-fos mapping, Cservenák et al. (6) have identified novel tuberoinfundibular peptide 39 (TIP39)–immunopositive projections from the posterior intralaminar complex of the thalamus (PIL) to the PVN. TIP39 is a ligand for the parathyroid hormone receptor (10), but TIP39 messenger RNA expression levels increase within the PIL around parturition and during lactation (11, 12), and TIP39 fibers are abundant in the PVN (13). This TIP39 PIL-PVN projection innervates oxytocin neurons and appears to be excitatory, based on the expression of vesicular glutamate transporter 2 messenger RNA and the presence of asymmetrical synapses. Using a retrograde tracer, Cservenák et al. (6) determined that the PIL is innervated by numerous brain regions, including the brainstem, as well as regions of the spinal cord. Inputs from the spinal cord to the PIL may relay sensory information relevant to social encounters. To test this hypothesis c-fos expression was examined in 2 contexts: following exposure to other females or in dams after contact with pups. They observed social interaction-dependent increases in c-fos expression in the PIL, with most of these c-fos–immunopositive neurons also expressing calbindin. Thus, the authors have identified a novel PIL-PVN ascending pathway through which somatosensory information could be conveyed to oxytocinergic neurons within the PVN, potentially affecting social behavior. This study strongly suggests a functional link between the PIL-PVN pathway and the modulation of social behavior. It is also among the first to provide a possible means by which somatosensory information associated with a social interaction could be conveyed to the PVN and directly affect the activation of oxytocin neurons. As oxytocin neurons in the PVN are known to project to many of the nodes within the SBNN, it is reasonable to hypothesize that this input could directly alter the firing patterns of PVN oxytocin neurons, in turn affecting behavioral output. Important next steps include determining whether the PIL-PVN (oxytocin) circuit activation is specific to females or even to particular social contexts, as well as the elucidation of the types of somatosensory information that is conveyed via the ascending projections to the PIL. By identifying specific, social cue-dependent projections from the PIL to oxytocin neurons of the PVN, this study has elucidated how PVN oxytocin neurons can be activated. Furthermore, because it seems likely that the PIL-PVN pathway is conserved in other species, this work will shape the way in which we think about how animals determine their social context. posterior intralaminar complex of the thalamus paraventricular nucleus social behavior neural network tuberoinfundibular peptide 39. This work was supported by the National Science Foundation IOS 1353859. Disclosure Summary: The author has nothing to disclose.
Source: Endocrinology
DOI: 10.1210/en.2016-1892
Author: Heather K. Caldwell
Institution: Kent State University
Language: English
Subfield: Social Psychology
Field: Psychology
Domain: Social Sciences
Open Access status: bronze
OpenAlex ID: W2607265461