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

Abstract

The intrinsic vasopressin system of the olfactory bulb is involved in social odor processing and consists of glutamatergic vasopressin cells (VPCs) located at the medial border of the glomerular layer. To characterize VPCs in detail, we combined various electrophysiological, neuroanatomical, and two-photon Ca 2+ imaging techniques in acute bulb slices from juvenile transgenic rats with eGFP-labeled VPCs. VPCs showed regular non-bursting firing patterns, and displayed slower membrane time constants and higher input resistances versus other glutamatergic tufted cell types. VPC axons spread deeply into the external plexiform and superficial granule cell layer (GCL). Axonal projections fell into two subclasses, with either denser local columnar collaterals or longer-ranging single projections running laterally within the internal plexiform layer and deeper within the granule cell layer. VPCs always featured lateral dendrites and a tortuous apical dendrite that innervated a single glomerulus with a homogenously branching tuft. These tufts lacked Ca 2+ transients in response to single somatically-evoked action potentials and showed a moderate Ca 2+ increase upon prolonged action potential trains. Notably, electrical olfactory nerve stimulation did not result in synaptic excitation of VPCs, but triggered substantial GABA A receptor-mediated IPSPs that masked excitatory barrages with yet longer latency. Exogenous vasopressin application reduced those IPSPs, as well as olfactory nerve-evoked EPSPs recorded from external tufted cells. In summary, VPCs can be classified as non-bursting, vertical superficial tufted cells. Moreover, our findings imply that sensory input alone cannot trigger excitation of VPCs, arguing for specific additional pathways for excitation or disinhibition in social contexts.

Molecular characterization of projection neuron subtypes in the mouse olfactory bulb

“…For OB projection neurons, however, only little information about chemotypes is available at this point: Pcdh1 and Tbx21 (Haddad et al, 2013;Nagai et al, 2005) have been shown to be selectively expressed in a subset of OB projection neurons. CCK distinguishes a subset of TCs (superficial TCs, (Liu and Shipley, 1994;Seroogy et al, 1985;Short and Wachowiak, 2019;Sun et al, 2020); vasopressin expressing cells might constitute a further subset of superficial TCs (Lukas et al, 2019). Heterogeneous expression of both the GABAa receptor as well as voltage-gated potassium channel subunits have been observed (Padmanabhan and Urban, 2010;Panzanelli et al, 2005), albeit not linked to specific cell types.…”

Top-down acetylcholine contributes to social discrimination via enabling action potentials in olfactory bulb vasopressin cells

“…As we recently demonstrated [8] that ON stimulation alone primarily inhibits VPCs, we suggest that (1) olfactory social cues alone are insufficient to excite VPCs and (2) VPC excitation is driven or unlocked by non-olfactory, top-down social signals. To test this hypothesis, we chose urine as an isolated olfactory social cue [21] and a novel male juvenile rat as a complete social stimulus.…”

Subpopulations of Projection Neurons in the Olfactory Bulb

“…Within the OT, middle tufted cells project to the lateral portion, whereas the medial portion is preferentially innervated by mitral cells ( Igarashi et al, 2012 ). Although it was previously undetermined if external tufted cells project their axons outside the OB ( Schoenfeld et al, 1985 ; Tobin et al, 2010 ; Lukas et al, 2019 ), Hirata et al (2019) recently showed that at least a subpopulation of external tufted cells do target the anterolateral edge of the OT as well as the pars externa of the AON.…”

“…Thus, external tufted cells likely transmit the olfactory information to specific regions in the olfactory cortex with unique temporal patterns. On the other hand, vasopressin, a neuropeptide, is predominantly expressed by external tufted cells with secondary dendrites and some middle tufted cells, but not by mitral cells, in the rodent OB ( Tobin et al, 2010 ; Lukas et al, 2019 ). It is proposed that the vasopressin-positive external tufted cells are involved in mechanisms of social recognition via the odor signatures ( Dluzen et al, 1998a , b ; Tobin et al, 2010 ; Wacker et al, 2011 ).…”

“…It is proposed that the vasopressin-positive external tufted cells are involved in mechanisms of social recognition via the odor signatures ( Dluzen et al, 1998a , b ; Tobin et al, 2010 ; Wacker et al, 2011 ). However, recent studies showed that OSN stimulation primarily caused strong inhibition of the vasopressin-positive external tufted cells, suggesting that OSN axons do not directly activate them ( Lukas et al, 2019 ). Whether the vasopressin-positive external tufted cells form a distinct neural circuit/pathway from the other external tufted cells is needed to be further elucidated.…”