Physiological features of parvalbumin-expressing GABAergic interneurons contributing to high-frequency oscillations in the cerebral cortex

• Published in: Current research in neurobiology Vol. 6; p. 100121
• Main Authors: Milicevic, Katarina D., Barbeau, Brianna L., Lovic, Darko D., Patel, Aayushi A., Ivanova, Violetta O., Antic, Srdjan D.
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 2024
• Subjects: Axon initial segment; Dendritic integration; Electrical synapse; Gamma oscillations; GEVI; Myelinated axon; I–O; Dendritic integration; AD; OPC; PV; IPSP; TZ; EPSP; Tau; CNS; Axon initial segment; VB; FS; AP; Ra; GEVI; Electrical synapse; HCN; PC; LFP; Gamma oscillations; Rm; Myelinated axon
• ISSN: 2665-945X; 2665-945X
• DOI: 10.1016/j.crneur.2023.100121

Parvalbumin-expressing (PV+) inhibitory interneurons drive gamma oscillations (30–80 Hz), which underlie higher cognitive functions. In this review, we discuss two groups/aspects of fundamental properties of PV+ interneurons. In the first group (dubbed Before Axon), we list properties representing optimal synaptic integration in PV+ interneurons designed to support fast oscillations. For example: [i] Information can neither enter nor leave the neocortex without the engagement of fast PV+ -mediated inhibition; [ii] Voltage responses in PV+ interneuron dendrites integrate linearly to reduce impact of the fluctuations in the afferent drive; and [iii] Reversed somatodendritic Rm gradient accelerates the time courses of synaptic potentials arriving at the soma. In the second group (dubbed After Axon), we list morphological and biophysical properties responsible for (a) short synaptic delays, and (b) efficient postsynaptic outcomes. For example: [i] Fast-spiking ability that allows PV+ interneurons to outpace other cortical neurons (pyramidal neurons). [ii] Myelinated axon (which is only found in the PV+ subclass of interneurons) to secure fast-spiking at the initial axon segment; and [iii] Inhibitory autapses – autoinhibition, which assures brief biphasic voltage transients and supports postinhibitory rebounds. Recent advent of scientific tools, such as viral strategies to target PV cells and the ability to monitor PV cells via in vivo imaging during behavior, will aid in defining the role of PV cells in the CNS. Given the link between PV+ interneurons and cognition, in the future, it would be useful to carry out physiological recordings in the PV+ cell type selectively and characterize if and how psychiatric and neurological diseases affect initiation and propagation of electrical signals in this cortical sub-circuit. Voltage imaging may allow fast recordings of electrical signals from many PV+ interneurons simultaneously. [Display omitted] •PV+ interneurons intercept and filter cortical input, and then intercept and filter cortical outputs. Information can neither enter nor leave the neocortex without strong engagement of fast PV + cell-mediated inhibition..•Predominantly linear voltage responses in dendrites of PV + interneurons are used to reduce impact of the fluctuations in the afferent drive, which in turn promotes PV + interneuron network synchrony.•PV + interneurons use fast spiking to outpace other excitable cells in the cortex and sculpt the ongoing electrical rhythm.•Electrical synapses (void of synaptic delays and high metabolic demands) are formed between PV + interneurons to allow the PV + interneuronal network to multiply its strength, outpace, and overcome other competing networks in the cortex. We envision the cerebral cortex as consisting of two competing cortical networks: one constituted by slow and numerous pyramidal cells releasing glutamate, and the other network composed of fast yet scarce interneurons releasing GABA.•The vast majority of cortical excitatory pyramidal cells have myelin wraps around their axons. However, among the cortical inhibitory interneurons, only the PV + subclass has myelinated axons, which are used to secure fast spiking in the initial axon segment (first), and then shorten time delays between the PV + interneuron action potential and synaptic releases of GABA at the PV + axon terminals (second).