Parvalbumin interneurons provide spillover to newborn and mature dentate granule cells

Abstract

Parvalbumin-expressing interneurons (PVs) in the dentate gyrus provide activity-dependent regulation of adult neurogenesis as well as maintain inhibitory control of mature neurons. In mature neurons, PVs evoke GABAA postsynaptic currents (GPSCs) with fast rise and decay phases that allow precise control of spike timing, yet synaptic currents with fast kinetics do not appear in adult-born neurons until several weeks after cell birth. Here we used mouse hippocampal slices to address how PVs signal to newborn neurons prior to the appearance of fast GPSCs. Whereas PV-evoked currents in mature neurons exhibit hallmark fast rise and decay phases, newborn neurons display slow GPSCs with characteristics of spillover signaling. We also unmasked slow spillover currents in mature neurons in the absence of fast GPSCs. Our results suggest that PVs mediate slow spillover signaling in addition to conventional fast synaptic signaling, and that spillover transmission mediates activity-dependent regulation of early events in adult neurogenesis.

Emergence of non-canonical parvalbumin-containing interneurons in hippocampus of a murine model of type I lissencephaly

“…Similar to prior analyses, we recovered Bistratified, Fast-spiking and Axo-axonic subsets of PV+INTs. Additionally, a minor population of Nos1 + cells clearly segregated, which represents putative dentate gyrus-expressed PV+INTs ( Vaden et al, 2020 ; Shen et al, 2019 ; Jinno and Kosaka, 2002 ).…”

Adult Neurogenesis: A Story Ranging from Controversial New Neurogenic Areas and Human Adult Neurogenesis to Molecular Regulation

“…Furthermore, the structural organization of the DG neurogenic niche suggests extensive cross-talk between niche cell types and adult-born DG cells and between position NSCs and adult-born DG cells; hence, adult-born DG cells serve as integrators of diverse signals from the niche. Additionally, AHN is a highly regulated process that leads from a quiescent state to neuronal differentiation [76] and is also an activity-dependent process that enables the formation of a new neural network [77]. In this regard, AHN initially produces rapidly proliferating precursor cells, followed by differentiation along the neurogenic trajectory, as the newborn cells exit the cell cycle and become immature neurons, and finally, the neurons survive and mature to become fully functional granule cells that are then integrated into the neural network [78].…”

Structural and Functional Modulation of Perineuronal Nets: In Search of Important Players with Highlight on Tenascins

“…Namely, optogenetic activation of PV + neurons promoted cell survival, while suppression of their activity reduced the survival of newborn cells. PV-expressing interneurons provide GABA signalization with two distinct spatiotemporal profiles: they evoke fast postsynaptic currents in mature GC, while in both mature and newborn GC they can elicit slow postsynaptic currents [109]. During synapse maturation slow postsynaptic responses transform into faster ones, while the formation of synapses between newborn GC and GABAergic PV + interneurons is considered to take place around 6-8 weeks [110].…”