Neural control of sexually dimorphic social behaviors

McKinsey, Gabriel L.; Ahmed, Osama M.; Shah, Nirao M.

doi:10.1016/j.cophys.2018.08.003

Cited by 27 publications

(20 citation statements)

References 69 publications

(84 reference statements)

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“…Within the hypothalamus, we observed labeling of neurons in the medial preoptic area (POA, Figure 1A–B ), a region that plays a crucial role in sexual behavior ( Balthazart and Ball, 2007 ; McKinsey et al, 2018 ; Newman, 1999 ; Wei et al, 2018 ) and more specifically in the production of courtship vocalizations in rodents and in songbirds ( Alger and Riters, 2006 ; Bean et al, 1981 ; Floody, 1989 ; Floody, 2009 ; Floody et al, 1998 ; Fu and Brudzynski, 1994 ; Gao et al, 2019 ; Riters and Ball, 1999 ; Vandries et al, 2019 ). Within the amygdala, we observed inputs to both PAG cell types from neurons spanning the rostral portion of the boundary between the central and medial amygdala (referred to here as the central-medial boundary zone (Amg C/M ), see below) continuing caudally to the central amygdala (CeA) ( Figure 1A–B ).…”

Section: Resultsmentioning

confidence: 99%

Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization

Michael

Goffinet

Pearson

et al. 2020

eLife

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Animals vocalize only in certain behavioral contexts, but the circuits and synapses through which forebrain neurons trigger or suppress vocalization remain unknown. Here, we used transsynaptic tracing to identify two populations of inhibitory neurons that lie upstream of neurons in the periaqueductal gray (PAG) that gate the production of ultrasonic vocalizations (USVs) in mice (i.e. PAG-USV neurons). Activating PAG-projecting neurons in the preoptic area of the hypothalamus (POAPAG neurons) elicited USV production in the absence of social cues. In contrast, activating PAG-projecting neurons in the central-medial boundary zone of the amygdala (AmgC/M-PAG neurons) transiently suppressed USV production without disrupting non-vocal social behavior. Optogenetics-assisted circuit mapping in brain slices revealed that POAPAG neurons directly inhibit PAG interneurons, which in turn inhibit PAG-USV neurons, whereas AmgC/M-PAG neurons directly inhibit PAG-USV neurons. These experiments identify two major forebrain inputs to the PAG that trigger and suppress vocalization, respectively, while also establishing the synaptic mechanisms through which these neurons exert opposing behavioral effects.

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Section: Resultsmentioning

confidence: 99%

Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization

Michael

Goffinet

Pearson

et al. 2020

eLife

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“…The hypothalamus is a subcortical region involved in the homeostatic and circadian regulation of wide array of physiological processes and behaviors (McKinsey, Ahmed, & Shah, 2018; Saper, Lu, Chou, & Gooley, 2005; Sisley & Sandoval, 2011; Tan & Knight, 2018). mWake exhibits significant expression in multiple regions of the hypothalamus, with notable enrichment in the SCN, the circadian pacemaker in mammals (Bell et al, 2020; Liu et al, 2014; Zhang et al, 2015).…”

Section: Resultsmentioning

confidence: 99%

Characterization of mWake expression in the murine brain

Bell

Wang

Kim

et al. 2020

J of Comparative Neurology

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Structure-function analyses of the mammalian brain have historically relied on anatomically-based approaches. In these investigations, physical, chemical, or electrolytic lesions of anatomical structures are applied, and the resulting behavioral or physiological responses assayed. An alternative approach is to focus on the expression pattern of a molecule whose function has been characterized and then use genetic intersectional methods to optogenetically or chemogenetically manipulate distinct circuits. We previously identified WIDE AWAKE (WAKE) in Drosophila, a clock output molecule that mediates the temporal regulation of sleep onset and sleep maintenance. More recently, we have studied the mouse homolog, mWAKE/ANKFN1, and our data suggest that its basic role in the circadian regulation of arousal is conserved. Here, we perform a systematic analysis of the expression pattern of mWake mRNA, protein, and cells throughout the adult mouse brain. We find that mWAKE labels neurons in a restricted, but distributed manner, in multiple regions of the hypothalamus (including the suprachiasmatic nucleus, dorsomedial hypothalamus, and tuberomammillary nucleus region), the limbic system, sensory processing nuclei, and additional specific brainstem, subcortical, and cortical areas. Interestingly, mWAKE is also observed in non-neuronal ependymal cells. In addition, to describe the molecular identities and clustering of mWake + cells, we provide detailed analyses of single cell RNA sequencing data from the hypothalamus, a region with particularly significant mWAKE expression. These findings lay the groundwork for future studies into the potential role of mWAKE + cells in the rhythmic control of diverse behaviors and physiological processes.

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“…Within the hypothalamus, we observed dense labeling of neurons in the medial preoptic area 87 (POA, Fig. 1A-B), a region that plays a crucial role in sexual behavior (Balthazart and Ball, 88 2007;McKinsey et al, 2018;Newman, 1999;Wei et al, 2018) and more specifically in the 89 production of courtship vocalizations in rodents and in songbirds (Alger and Riters, 2006;Bean 90 et al, 1981;Floody, 1989Floody, , 2009Floody et al, 1998;Fu and Brudzynski, 1994;Gao et al, 2019;91 Riters and Ball, 1999;Vandries et al, 2019). Within the amygdala, we observed dense inputs to 92 both PAG cell types from neurons spanning the most medial and rostral portions of the 93 amygdala (referred to here as the extended amygdala (EA), see below) continuing caudally to 94 the central amygdala (CeA) ( Fig.…”

Section: Inhibitory Neurons In the Hypothalamus And Amygdala Provide mentioning

confidence: 98%

Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization

Michael

Goffinet

Wang

et al. 2019

Preprint

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9Animals vocalize only in certain behavioral contexts, but the circuits and synapses through 10 which forebrain neurons trigger or suppress vocalization remain unknown. Here we used 11 transsynaptic tracing to identify two populations of inhibitory neurons that lie upstream of 12 neurons in the periaqueductal gray that gate the production of ultrasonic vocalizations in mice 13 (i.e., PAG-USV neurons). Activating PAG-projecting neurons in the preoptic hypothalamus 14 (POAPAG neurons) elicited USV production in the absence of social cues. In contrast, activating 15 PAG-projecting neurons in the extended amygdala (EAPAG neurons) transiently suppressed USV 16 production without disrupting non-vocal social behavior. Optogenetics-assisted circuit mapping 17 in brain slices revealed that POAPAG neurons directly inhibit PAG interneurons, which in turn 18 inhibit PAG-USV neurons, whereas EAPAG neurons directly inhibit PAG-USV neurons. These 19 experiments identify two major forebrain inputs to the PAG that trigger and suppress 20 vocalization, respectively, while also establishing the synaptic mechanisms through which these 21 neurons exert opposing behavioral effects. 22 23

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Neural control of sexually dimorphic social behaviors

Cited by 27 publications

References 69 publications

Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization

Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization

Characterization of mWake expression in the murine brain

Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization

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