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Vasopressin Cells in the Rodent Olfactory Bulb Resemble Non-Bursting Superficial Tufted Cells and Are Primarily Inhibited Upon Olfactory Nerve Stimulation

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Vasopressin Cells in the Rodent Olfactory Bulb Resemble Non-Bursting Superficial Tufted Cells and Are Primarily Inhibited Upon Olfactory Nerve Stimulation This Accepted Manuscript has not been copyedited and formatted. The final version may differ from this version. Research Article: New Research | Sensory and Motor Systems Vasopressin cells in the rodent olfactory bulb resemble non-bursting superficial tufted cells and are primarily inhibited upon olfactory nerve stimulation Michael Lukas1, Hajime Suyama1 and Veronica Egger1 1Institute of Zoology, Neurophysiology, University of Regensburg, Regensburg, Germany https://doi.org/10.1523/ENEURO.0431-18.2019 Received: 5 November 2018 Revised: 24 May 2019 Accepted: 28 May 2019 Published: 19 June 2019 M.L. and V.E. designed research; M.L. and H.S. performed research; M.L., H.S., and V.E. analyzed data; M.L. and V.E. wrote the paper. Funding: Deutsche Forschungsgemeinschaft (DFG) LU 2164/1-1 EG 135/5-1 . Conflict of Interest: Authors report no conflict of interest The research was funded by the German research foundation (DFG LU 2164/1-1 and EG 135/5-1) Correspondence should be addressed to Michael Lukas at [email protected] Cite as: eNeuro 2019; 10.1523/ENEURO.0431-18.2019 Alerts: Sign up at www.eneuro.org/alerts to receive customized email alerts when the fully formatted version of this article is published. Accepted manuscripts are peer-reviewed but have not been through the copyediting, formatting, or proofreading process. Copyright © 2019 Lukas et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. 1 Vasopressin cells in the rodent olfactory bulb resemble non-bursting superficial tufted cells and are 2 primarily inhibited upon olfactory nerve stimulation 3 4 Vasopressin cells in the rodent olfactory bulb 5 6 Michael Lukas, Institute of Zoology, Neurophysiology, University of Regensburg, Regensburg, Germany 7 Hajime Suyama, Institute of Zoology, Neurophysiology, University of Regensburg, Regensburg, 8 Germany 9 Veronica Egger, Institute of Zoology, Neurophysiology, University of Regensburg, Regensburg, 10 Germany 11 12 Author Contributions: ML and VE designed research; ML and HS performed research; ML, HS, and VE 13 analyzed data; ML wrote the paper; VE revised the paper. 14 15 Correspondence should be addressed to Michael Lukas ([email protected]) 16 17 Number of Figures: 9 Number of words for Abstract: 245 18 Number of Tables: 2 Number of words for Significance 19 Number of Multimedia: 0 Statement: 120 20 Number of words for Introduction: 585 21 Number of words for Discussion: 2972 22 23 Acknowledgements 24 We wish to thank Anne Pietryga-Krieger. Dr. Wolfgang Bywalez and Dr. Vanessa Rupprecht for 25 experimental support as well as Dr. Mike Ludwig (University of Edinburgh) for providing the VP-eGFP 26 rats. Further, we want to thank Dr. Harold Gainer (NINDS, Bethesda) and Dr. Maurice Manning 27 (University of Toledo) for generously providing the vasopressin-neurophysin antibodies and the selective 28 vasopressin receptor antagonist, respectively. 29 30 Authors report no conflict of interest 31 32 Funding sources: 33 The research was funded by the German research foundation (DFG LU 2164/1-1 and EG 135/5-1) 1 34 Vasopressin cells in the rodent olfactory bulb resemble non-bursting superficial tufted cells and are 35 primarily inhibited upon olfactory nerve stimulation 36 37 Abstract: 38 The intrinsic vasopressin system of the olfactory bulb is involved in social odor processing and consists of 39 glutamatergic vasopressin cells (VPCs) located at the medial border of the glomerular layer. To 40 characterize VPCs in detail, we combined various electrophysiological, neuroanatomical and two-photon 41 Ca2+ imaging techniques in acute bulb slices from juvenile transgenic rats with eGFP-labelled VPCs. 42 VPCs showed regular non-bursting firing patterns, and displayed slower membrane time constants and 43 higher input resistances versus other glutamatergic tufted cell types. VPC axons spread deeply into the 44 external plexiform and superficial granule cell layer. Axonal projections fell into two subclasses, with 45 either denser local columnar collaterals or longer-ranging single projections running laterally within the 46 internal plexiform layer and deeper within the granule cell layer. VPCs always featured lateral dendrites 47 and a tortuous apical dendrite that innervated a single glomerulus with a homogenously branching tuft. 48 These tufts lacked Ca2+ transients in response to single somatically-evoked action potentials and showed 49 a moderate Ca2+ increase upon prolonged action potential trains. 50 Notably, electrical olfactory nerve stimulation did not result in synaptic excitation of VPCs, but triggered 51 substantial GABAA receptor-mediated IPSPs that masked excitatory barrages with yet longer latency. 52 Exogenous vasopressin application reduced those IPSPs, as well as olfactory-nerve evoked EPSPs 53 recorded from external tufted cells. 54 In summary, VPCs can be classified as non-bursting, vertical superficial tufted cells. Moreover, our 55 findings imply that sensory input alone cannot trigger excitation of VPCs, arguing for specific additional 56 pathways for excitation or disinhibition in social contexts. 2 57 Significance statement: 58 Efficient sensing of conspecific odor signatures is essential for most rodent social behavior. Although 59 olfactory bulb vasopressin was shown to be a potent facilitator of social odor processing, little is known 60 on the cellular substrate of the intrinsic vasopressin system. Here we provide a detailed characterization 61 of the anatomical and electrophysiological properties of the bulbar vasopressin cells. While we also 62 identify several targets of vasopressin action, we find that stimulation of the sensory inputs to the bulb 63 results primarily in vasopressin cell inhibition, implying that excitation of the bulbar vasopressin system 64 requires additional still unknown excitatory or dis-inhibitory inputs which might confer social specificity. 65 These insights may complement the knowledge on vasopressinergic modulation of social stimuli in limbic 66 brain structures. 67 3 68 Introduction 69 The neuropeptide vasopressin (VP) is primarily synthesized in neurons located within the supraoptic, 70 paraventricular, and suprachiasmatic nuclei of the hypothalamus (Ludwig and Leng, 2006). These 71 neurons release VP from their axonal projections to the neurohypophysis into the bloodstream to exert 72 its peripheral physiological functions as a neurohormone, e.g. water retention in the kidney (Ondrasek, 73 2016). In the central nervous system, VP is known as a key modulator of social behavior and cognition in 74 mammals, including rodents and humans (Meyer-Lindenberg et al., 2011; Lukas and Neumann, 2013; 75 Lukas and de Jong, 2016). In this context, relevant VP release was shown to occur from somata and 76 dendrites of the above mentioned VP cells (VPCs) in the hypothalamus as well as from hypothalamic and 77 extra-hypothalamic fibers that target the components of the social behavior network throughout the 78 mammalian brain, e.g. the lateral septum, the medial extended amygdala, the anterior and ventromedial 79 hypothalamus, and the periaqueductal gray (Sterba, 1974; Buijs et al., 1983; Ondrasek, 2016). The extra- 80 hypothalamic brain regions that also synthesize and release VP during social interactions are the bed 81 nucleus of stria terminalis, the medial amygdala, and the olfactory bulb (OB), i.e. the first center of 82 olfactory processing (De Vries and Buijs, 1983; Tobin et al., 2010; Lukas and de Jong, 2016). 83 Olfactory processing is an essential component of mammalian social communication, in rodents, sheep, 84 and even humans (Porter et al., 1986; Brennan and Kendrick, 2006). Especially in rodents, the olfactory 85 system is regarded as the main sensory pathway for mediating recognition and discrimination of 86 individual con-specifics (Camats Perna and Engelmann, 2017). Several pharmacological studies suggest 87 that endogenous VP release within the OB facilitates the discrimination of known and new individuals via 88 their odor signatures (e.g. Dluzen et al., 1998b; Dluzen et al., 1998a; Tobin et al., 2010). The source of 89 this VP release are bulbar VPCs, a subpopulation of glutamatergic tufted cells with lateral dendrites 90 (Macrides and Schneider, 1982; Hamilton et al., 2005), that resides at the border between the 91 glomerular layer and the external plexiform layer (EPL) in both the accessory OB (AOB) and the main OB 4 92 (MOB, Tobin et al., 2010; Wacker et al., 2011). The presence of VPCs in both pathways for odorant 93 detection (volatile/MOB and non-volatile/AOB) is in line with the view that volatile odor signals are 94 especially important for the coding of individual body odor signatures (Brennan and Kendrick, 2006) and 95 thus the AOB and MOB play complementary roles in processing social odor recognition (Baum and 96 Kelliher, 2009; Stowers and Kuo, 2016). 97 As mentioned above, VP enhances social recognition of individuals on the level of the OB, but what could 98 be the cellular mechanisms that are responsible for this facilitation of social odor processing? As a first 99 step towards resolving these questions, here we provide a detailed investigation of basic 100 electrophysiological and neuroanatomical properties of the OB VPCs, including their axonal projections. 101 We also set out to identify synaptic inputs to VPCs, which turns out to be a challenging
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