Complementary roles for parvalbumin and somatostatin interneurons in the generation of hippocampal gamma oscillations

Abstract

11Gamma-frequency oscillations (30-120 Hz) can be separated into fast (>60 Hz) and slow oscillations, 12 with different roles in neuronal encoding and information transfer. While synaptic inhibition is 13 important for synchronization across the gamma-frequency range, the role of distinct interneuronal 14 subtypes in fast and slow gamma states remains unclear. Here, we used optogenetics to examine 15 the involvement of parvalbumin (PV+) and somatostatin (SST+) expressing interneurons in gamma 16 oscillations in the mouse hippocampal CA3 ex vivo. Disrupting either PV+ or STT+ interneuron 17 activity, via either photo-inhibition or photo-excitation, led to a decrease in the power of 18 cholinergically-induced slow gamma oscillations. Furthermore, photo-excitation of SST+ 19 interneurons induced fast gamma oscillations, which depended on both synaptic excitation and 20 inhibition. Our findings support a critical role for both PV+ and SST+ interneurons in slow 21 hippocampal gamma oscillations, and further suggest that STT+ interneurons are capable of 22 switching the network between slow and fast gamma states. 23 24 25 26 2

Dentate gyrus and CA3 GABAergic interneurons bidirectionally modulate signatures of internal and external drive to CA1

“…Specifically, suppressing PV + interneurons led to SWR and SG/FG modulation consistent with increased CA3 drive and decreased EC drive to CA1: SWRs seen during immobility had higher incidence, faster frequency, greater amplitude of coincident SWs and SG, and showed higher SG coherence across regions; SG during movement had greater power and coherence across regions, while FG during movement had reduced modulation by theta. These findings concur with two recent studies which modulated CA3 PV + interneurons in rats and ex vivo (Antonoudiou et al, 2020;Lo ´pez-Madrona et al, 2020). By contrast, suppressing SST + interneurons led to SWR and SG modulation consistent with decreased CA3 drive and increased EC drive to CA1: SWRs were less common and longer; SG during movement had reduced modulation by theta and FG during movement had greater power.…”

Development of parvalbumin-immunoreactive neurons in the postnatal human hippocampal formation

“…In fast spiking interneurons, cytosolic expression of PV has been correlated with their structural and functional maturation (Doischer et al, 2008). While we have to emphasize that PV immunohistochemistry is suitable to detect both axo-axonic cells and fast-spiking basket cells, the role of the latter in hippocampal-dependent memory formation due to their involvement in complex network operations indicates that the maturation of PV-immunoreactive neurons is reflected in learning and memory processes (Whittington et al, 1995;Ylinen et al, 1995;Tamas et al, 2000;Freund, 2003;Fuchs et al, 2007;Antonoudiou et al, 2020;Strüber et al, 2022). In harmony with the early hippocampal development reflected by the predominantly prenatal maturation of PV-immunoreactive neurons in non-human primates, hippocampaldependent form of recognition memory has been reported soon after birth.…”

“…Among the various GABAergic cell types calcium-binding protein Parvalbumin (PV)expressing cells, the major GABAergic component of the hippocampal intrinsic inhibitory circuitry, are powerful regulators of neuronal activity. Fast-spiking PV-immunoreactive neurons are involved in basic microcircuit functions such as feed-forward or feed-back inhibition, and in gamma frequency (30-80 Hz) oscillations 10.3389/fnana.2023.1058370 (Whittington et al, 1995;Ylinen et al, 1995;Tamas et al, 2000;Freund, 2003;Fuchs et al, 2007;Sohal et al, 2009;Antonoudiou et al, 2020). In addition, PV-immunoreactive neurons are cellular components of complex network operations, including modulation of place and grid field, pattern separations, phase precession, and gain modulation of sensory responses (Hu et al, 2014).…”

NMDAr Blocking by MK801 Alters Hippocampal and Prefrontal Cortex Oscillations and Impairs Spatial Working Memory in Mice

“…On the other hand, a similar manipulation of cholecystokinin (CCK+) interneurons specifically affected theta oscillations and spatial cognition (Del Pino et al, 2017;delPino et al, 2013). Scrutinizing the role of different interneuron types by means of opto-tagging and manipulating NMDAr activity during different conditions would help unveil the micro and macro circuits involved in oscillatory activity, cognition, and the link between both (Antonoudiou et al, 2020;Royer et al, 2012).…”