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Current Biology : CB Nov 2022Social touch is an essential component of communication. Little is known about the underlying pathways and mechanisms. Here, we discovered a novel neuronal pathway from...
Social touch is an essential component of communication. Little is known about the underlying pathways and mechanisms. Here, we discovered a novel neuronal pathway from the posterior intralaminar thalamic nucleus (PIL) to the medial preoptic area (MPOA) involved in the control of social grooming. We found that the neurons in the PIL and MPOA were naturally activated by physical contact between female rats and also by the chemogenetic stimulation of PIL neurons. The activity-dependent tagging of PIL neurons was performed in rats experiencing physical social contact. The chemogenetic activation of these neurons increased social grooming between familiar rats, as did the selective activation of the PIL-MPOA pathway. Neurons projecting from the PIL to the MPOA express the neuropeptide parathyroid hormone 2 (PTH2), and the central infusion of its receptor antagonist diminished social grooming. Finally, we showed a similarity in the anatomical organization of the PIL and the distribution of the PTH2 receptor in the MPOA between the rat and human brain. We propose that the discovered neuronal pathway facilitates physical contact with conspecifics.
Topics: Humans; Rats; Female; Animals; Grooming; Rodentia; Preoptic Area; Neurons; Neuropeptides
PubMed: 36113471
DOI: 10.1016/j.cub.2022.08.062 -
Physiology & Behavior Oct 2018Most maternal caregiving behaviors change across lactation to match the developmental needs of the continuously aging offspring. However, it is mostly unknown whether...
Most maternal caregiving behaviors change across lactation to match the developmental needs of the continuously aging offspring. However, it is mostly unknown whether the dams' postpartum stage or litter age is the primary driving force of these changes. In this study, postnatal day 1 and 8 litters were cross-fostered or in-fostered to postpartum day 1 or 8 dams. Five days later, undisturbed observations of maternal caregiving behaviors were performed on the subsequent two days. We found a main effect of dams' postpartum stage on the frequency that mothers spent with the pups and displayed erect postures over them (hovering over and kyphosis), although it was mostly driven by an interaction between postpartum stage and litter age: early-postpartum dams were in contact with younger litters and in erect postures more often with younger litters compared to later-postpartum dams with younger litters. Additionally, there was an interaction between postpartum stage and litter age on the litter weights because older litters living with later-postpartum dams were heavier than older litters living with early-postpartum dams. There was also an interaction between postpartum stage and litter age on the dams' bodyweight, with early-postpartum dams living with younger litters weighing the least and later-postpartum dams living with younger litters weighing the most. Because activity of the neuropeptide, orexin, within the medial preoptic area (mPOA) has been implicated in maternal nursing and other caregiving behaviors, we measured mPOA levels of orexin-A but it was not affected by postpartum stage or litter age (nor was there an interaction). However, high orexin-A was negatively associated with the frequency of contact with pups and the display of erect postures. These results indicate that changes in caregiving across lactation are driven by endogenous factors in the dams, age-related cues they receive from offspring, and interactions between these factors.
Topics: Age Factors; Animals; Animals, Newborn; Female; Maternal Behavior; Orexins; Postpartum Period; Preoptic Area
PubMed: 29928888
DOI: 10.1016/j.physbeh.2018.06.025 -
The Journal of Neuroscience : the... May 2020Male animals may show alternative behaviors toward infants: attack or parenting. These behaviors are triggered by pup stimuli under the influence of the internal state,...
Male animals may show alternative behaviors toward infants: attack or parenting. These behaviors are triggered by pup stimuli under the influence of the internal state, including the hormonal environment and/or social experiences. Converging data suggest that the medial preoptic area (MPOA) contributes to the behavioral selection toward the pup. However, the neural mechanisms underlying how integrated stimuli affect the MPOA-dependent behavioral selection remain unclear. Here we focus on the amygdalohippocampal area (AHi) that projects to MPOA and expresses oxytocin receptor, a hormone receptor mediating social behavior toward pups. We describe the activation of MPOA-projection AHi neurons in male mice by social contact with pups. Input mapping using the TRIO method reveals that MPOA-projection AHi neurons receive prominent inputs from several regions, including the thalamus, hypothalamus, and olfactory cortex. Electrophysiological and histologic analysis demonstrates that oxytocin modulates inhibitory synaptic responses on MPOA-projection AHi neurons. In addition, AHi forms the excitatory monosynapse to MPOA, and pharmacological activation of MPOA-projection AHi neurons enhances only aggressive behavior, but not parental behavior. Interestingly, this promoted behavior was related to social experience in male mice. Collectively, our results identified a presynaptic partner of MPOA that can integrate sensory input and hormonal state, and trigger pup-directed aggression. The medial preoptic area (MPOA) plays critical roles in parental behavior, such as motor control, motivation, and social interaction. The MPOA projects to multiple brain regions, and these projections contribute to several neural controls in parental behavior. In contrast, how inputs to MPOA are regulated by social and environmental information is poorly understood. In this study, we focus on the amygdalohippocampal area (AHi) that connects to MPOA and expresses oxytocin receptor. We demonstrate the disruption of the expression of parental behavior triggered by the activation of MPOA-projection AHi neurons. This behavior may be regulated not only by oxytocin but also by neural input from several regions.
Topics: Aggression; Amygdala; Animals; Brain Mapping; Electrophysiological Phenomena; Hippocampus; Male; Mice; Mice, Inbred C57BL; Neural Inhibition; Neural Pathways; Neurons; Paternal Behavior; Preoptic Area; Receptors, Oxytocin; Social Behavior; Social Environment
PubMed: 32284340
DOI: 10.1523/JNEUROSCI.0438-19.2020 -
Neuron Oct 2021Deep brain temperature detection by hypothalamic warm-sensitive neurons (WSNs) has been proposed to provide feedback information relevant for thermoregulation. WSNs...
Deep brain temperature detection by hypothalamic warm-sensitive neurons (WSNs) has been proposed to provide feedback information relevant for thermoregulation. WSNs increase their action potential firing rates upon warming, a property that has been presumed to rely on the composition of thermosensitive ion channels within WSNs. Here, we describe a synaptic mechanism that regulates temperature sensitivity of preoptic WSNs and body temperature. Experimentally induced warming of the mouse hypothalamic preoptic area in vivo triggers body cooling. TRPM2 ion channels facilitate this homeostatic response and, at the cellular level, enhance temperature responses of WSNs, thereby linking WSN function with thermoregulation for the first time. Rather than acting within WSNs, we-unexpectedly-find TRPM2 to temperature-dependently increase synaptic drive onto WSNs by disinhibition. Our data emphasize a network-based interoceptive paradigm that likely plays a key role in encoding body temperature and that may facilitate integration of diverse inputs into thermoregulatory pathways.
Topics: Animals; Body Temperature; Body Temperature Regulation; Interoception; Mice; Mice, Knockout; Neural Inhibition; Neurons; Preoptic Area; Synapses; TRPM Cation Channels; Thermosensing
PubMed: 34672983
DOI: 10.1016/j.neuron.2021.10.001 -
General and Comparative Endocrinology Nov 1999Alternative reproductive tactics within one sex, adult sex or role change, and reproductive suppression are all forms of reproductive plasticity commonly exhibited among... (Review)
Review
Alternative reproductive tactics within one sex, adult sex or role change, and reproductive suppression are all forms of reproductive plasticity commonly exhibited among teleost fishes. The two neuropeptides that have been most extensively studied with regard to such behavioral plasticity are gonadotropin releasing hormone (GnRH) and arginine vasotocin (AVT). Here, we review intra- and intersexual variation in the number and size of GnRH and AVT neurons along with gonadal phenotype in those species of teleosts showing intraspecific plasticity in reproductive behavior. In several species, male dimorphisms in the number and/or size of GnRH neurons in the forebrain's preoptic area parallel a divergence in relative gonad size and reproductive tactics. The available studies of AVT-containing neurons in the preoptic area also indicate intrasexual dimorphisms among males, although a proximate link to other reproductive traits and behavioral outcomes is more difficult to recognize. For both GnRH and AVT, there are also species-typical patterns in the coupling between structural (e.g., neuronal and gonadal) traits and reproductive tactic expressed, which likely reflect distinct patterns of adaptation to particular ecological environments. As discussed, neurophysiological, biochemical, and receptor density studies are now essential to establish the functional significance of the diverse organizational patterns of GnRH and AVT neurons in teleosts. Similar studies also need to be carried out in species of other vertebrate groups that show comparable behavioral plasticity.
Topics: Animals; Female; Fishes; Gonadotropin-Releasing Hormone; Male; Neurons; Preoptic Area; Reproduction; Sex Characteristics; Sexual Behavior, Animal; Vasotocin
PubMed: 10562445
DOI: 10.1006/gcen.1999.7357 -
Sleep Sep 2015The ventrolateral preoptic area (VLPO) and the orexin/hypocretin neuronal system are key regulators of sleep onset, transitions between vigilance states, and energy...
STUDY OBJECTIVES
The ventrolateral preoptic area (VLPO) and the orexin/hypocretin neuronal system are key regulators of sleep onset, transitions between vigilance states, and energy homeostasis. Reciprocal projections exist between the VLPO and orexin/hypocretin neurons. Although the importance of the VLPO to sleep regulation is clear, it is unknown whether VLPO neurons are involved in energy balance. The purpose of these studies was to determine if the VLPO is a site of action for orexin-A, and which orexin receptor subtype(s) would mediate these effects of orexin-A. We hypothesized that orexin-A in the VLPO modulates behaviors (sleep and wakefulness, feeding, spontaneous physical activity [SPA]) to increase energy expenditure.
DESIGN AND MEASUREMENTS
Sleep, wakefulness, SPA, feeding, and energy expenditure were determined after orexin-A microinjection in the VLPO of male Sprague-Dawley rats with unilateral cannulae targeting the VLPO. We also tested whether pretreatment with a dual orexin receptor antagonist (DORA, TCS-1102) or an OX2R antagonist (JNJ-10397049) blocked the effects of orexin-A on the sleep/wake cycle or SPA, respectively.
RESULTS
Orexin-A injected into the VLPO significantly increased wakefulness, SPA, and energy expenditure (SPA-induced and total) and reduced NREM sleep and REM sleep with no effect on food intake. Pretreatment with DORA blocked the increase in wakefulness and the reduction in NREM sleep elicited by orexin-A, and the OX2R antagonist reduced SPA stimulated by orexin-A.
CONCLUSIONS
These data show the ventrolateral preoptic area is a site of action for orexin-A, which may promote negative energy balance by modulating sleep/wakefulness and stimulating spontaneous physical activity and energy expenditure.
Topics: Animals; Attention; Dioxanes; Eating; Energy Metabolism; Male; Neurons; Orexin Receptor Antagonists; Orexin Receptors; Orexins; Phenylurea Compounds; Preoptic Area; Rats; Rats, Sprague-Dawley; Sleep; Sleep Deprivation; Time Factors; Wakefulness
PubMed: 25845696
DOI: 10.5665/sleep.4970 -
Genes, Brain, and Behavior Jul 2017Social context often has profound effects on behavior, yet the neural and molecular mechanisms which mediate flexible behavioral responses to different social...
Social context often has profound effects on behavior, yet the neural and molecular mechanisms which mediate flexible behavioral responses to different social environments are not well understood. We used the African cichlid fish, Astatotilapia burtoni, to examine aggressive defense behavior across three social contexts representing different motivational states: a reproductive opportunity, a familiar male and a neutral context. To elucidate how differences in behavior across contexts may be mediated by neural gene expression, we examined gene expression in the preoptic area, a brain region known to control male aggressive and sexual behavior. We show that social context has broad effects on preoptic gene expression. Specifically, we found that the expression of genes encoding nonapeptides and sex steroid receptors are upregulated in the familiar male context. Furthermore, circulating levels of testosterone and cortisol varied markedly depending on social context. We also manipulated the D2 receptor (D2R) in each social context, given that it has been implicated in mediating context-dependent behavior. We found that a D2R agonist reduced intruder-directed aggression in the reproductive opportunity and familiar male contexts, while a D2R antagonist inhibited intruder-directed aggression in the reproductive opportunity context and increased aggression in the neutral context. Our results demonstrate a critical role for preoptic gene expression, as well as circulating steroid hormone levels, in encoding information from the social environment and in shaping adaptive behavior. In addition, they provide further evidence for a role of D2R in context-dependent behavior.
Topics: Aggression; Animals; Cichlids; Dopamine Agonists; Dopamine Antagonists; Fish Proteins; Hydrocortisone; Male; Preoptic Area; Receptors, Dopamine D2; Spatial Behavior; Testosterone
PubMed: 28466980
DOI: 10.1111/gbb.12389 -
Brain Structure & Function Jul 2018The lateral preoptic area (LPO) and ventral pallidum (VP) are structurally and functionally distinct territories in the subcommissural basal forebrain. It was recently...
The lateral preoptic area (LPO) and ventral pallidum (VP) are structurally and functionally distinct territories in the subcommissural basal forebrain. It was recently shown that unilateral infusion of the GABA receptor antagonist, bicuculline, into the LPO strongly invigorates exploratory locomotion, whereas bicuculline infused unilaterally into the VP has a negligible locomotor effect, but when infused bilaterally, produces vigorous, abnormal pivoting and gnawing movements and compulsive ingestion. This study was done to further characterize these responses. We observed that bilateral LPO infusions of bicuculline activate exploratory locomotion only slightly more potently than unilateral infusions and that unilateral and bilateral LPO injections of the GABA receptor agonist muscimol potently suppress basal locomotion, but only modestly inhibit locomotion invigorated by amphetamine. In contrast, unilateral infusions of muscimol into the VP affect basal and amphetamine-elicited locomotion negligibly, but bilateral VP muscimol infusions profoundly suppress both. Locomotor activation elicited from the LPO by bicuculline was inhibited modestly and profoundly by blockade of dopamine D2 and D1 receptors, respectively, but was not entirely abolished even under combined blockade of dopamine D1 and D2 receptors. That is, infusing the LPO with bic caused instances of near normal, even if sporadic, invigoration of locomotion in the presence of saturating dopamine receptor blockade, indicating that LPO can stimulate locomotion in the absence of dopamine signaling. Pivoting following bilateral VP bicuculline infusions was unaffected by dopamine D2 receptor blockade, but was completely suppressed by D1 receptor blockade. The present results are discussed in a context of neuroanatomical and functional organization underlying exploratory locomotion and adaptive movements.
Topics: Amphetamine; Animals; Basal Forebrain; Bicuculline; Central Nervous System Stimulants; Dopamine Agents; Functional Laterality; GABA-A Receptor Agonists; GABA-A Receptor Antagonists; Locomotion; Male; Movement; Muscimol; Preoptic Area; Rats; Rats, Sprague-Dawley; Time Factors
PubMed: 29700637
DOI: 10.1007/s00429-018-1669-2 -
Biological Psychiatry Mar 2017The male bias in autism spectrum disorder incidence is among the most extreme of all neuropsychiatric disorders, yet the origins of the sex difference remain obscure.... (Review)
Review
The male bias in autism spectrum disorder incidence is among the most extreme of all neuropsychiatric disorders, yet the origins of the sex difference remain obscure. Developmentally, males are exposed to high levels of testosterone and its byproduct, estradiol. Together these steroids modify the course of brain development by altering neurogenesis, cell death, migration, differentiation, dendritic and axonal growth, synaptogenesis, and synaptic pruning, all of which can be deleteriously impacted during the course of developmental neuropsychiatric disorders. Elucidating the cellular mechanisms by which steroids modulate brain development provides valuable insights into how these processes may go awry. An emerging theme is the role of inflammatory signaling molecules and the innate immune system in directing brain masculinization, the evidence for which we review here. Evidence is also emerging that the neuroimmune system is overactivated in individuals with autism spectrum disorder. These combined observations lead us to propose that the natural process of brain masculinization puts males at risk by moving them closer to a vulnerability threshold that could more easily be breached by inflammation during critical periods of brain development. Two brain regions are highlighted: the preoptic area and the cerebellum. Both are developmentally regulated by the inflammatory prostaglandin E2, but in different ways. Microglia, innate immune cells of the brain, and astrocytes are also critical contributors to masculinization and illustrate the importance of nonneuronal cells to the health of the developing brain.
Topics: Animals; Astrocytes; Autism Spectrum Disorder; Behavior, Animal; Brain; Cerebellum; Dinoprostone; Disease Models, Animal; Female; Humans; Immunity, Innate; Inflammation; Male; Mice; Microglia; Neuroimmunomodulation; Preoptic Area; Rats; Risk Factors; Sex Characteristics; Sex Differentiation; Sex Factors
PubMed: 27871670
DOI: 10.1016/j.biopsych.2016.10.004 -
Integrative and Comparative Biology Nov 2017Males of many species rely on chemosensory information for social communication. In male Syrian hamsters (Mesocricetus auratus), as in many species, female chemosignals...
Males of many species rely on chemosensory information for social communication. In male Syrian hamsters (Mesocricetus auratus), as in many species, female chemosignals potently stimulate sexual behavior and a concurrent, rapid increase in circulating luteinizing hormone (LH) and testosterone (T). However, under winter-like, short-day (SD) photoperiods, when Syrian hamsters are reproductively quiescent, these same female chemosignals fail to elicit behavioral or hormonal responses, even after T replacement. It is currently unknown where in the brain chemosensory processing is gated in a seasonally dependent manner such that reproductive responses are only displayed during the appropriate breeding season. The goal of the present study was to determine where this gating occurred by identifying neural loci that respond differentially to female chemosignals across photoperiods, independent of circulating T concentrations. Adult male Syrian hamsters were housed under either long-day (LD) (reproductively active) or SD (reproductively inactive) photoperiods with half of the SD animals receiving T replacement. Animals were exposed to either female hamster vaginal secretions (FHVSs) diluted in mineral oil or to vehicle, and the activational state of chemosensory processing centers and elements of the neuroendocrine reproductive axis were examined. Components of the chemosensory pathway upstream of hypothalamic centers increased expression of FOS, an indirect marker of neuronal activation, similarly across photoperiods. In contrast, the preoptic area (POA) of the hypothalamus responded to FHVS only in LD animals, consistent with its role in promoting expression of male sexual behavior. Within the neuroendocrine axis, the RF-amide related peptide (RFRP), but not the kisspeptin neuronal system responded to FHVS only in LD animals. Neither response within the POA or the RFRP neuronal system was rescued by T replacement in SD animals, mirroring photoperiodic regulation of reproductive responses. Considering the POA and the RFRP neuronal system promote reproductive behavior and function in male Syrian hamsters, differential activation of these systems represents a potential means by which photoperiod limits expression of reproduction to the appropriate environmental context.
Topics: Animals; Male; Mesocricetus; Neurons; Neuropeptides; Photoperiod; Preoptic Area; Seasons; Sensory Gating; Sex Attractants; Testosterone
PubMed: 28985371
DOI: 10.1093/icb/icx099