Robust perisomatic GABAergic self-innervation inhibits basket cells in the human and mouse supragranular neocortex

Abstract

Inhibitory autapses are self-innervating synaptic connections in GABAergic interneurons in the brain. Autapses in neocortical layers have not been systematically investigated, and their function in different mammalian species and specific interneuron types is poorly known. We investigated GABAergic parvalbumin-expressing basket cells (pvBCs) in layer 2/3 (L2/3) in mice as well as in human neocortical tissue resected in deep-brain surgery. Most pvBCs showed robust GABAAR-mediated self-innervation in both species, but autapses were rare in nonfast spiking GABAergic interneurons. Light-and electron microscopy analyses revealed pvBC axons innervating their own soma and proximal dendrites. GABAergic selfinhibition conductance was similar in human and mouse pvBCs and comparable to that of synapses from pvBCs to other L2/3 neurons. Autaptic conductance prolonged somatic inhibition in pvBCs after a spike and inhibited repetitive firing. Perisomatic autaptic inhibition has evolved in pvBCs of various cortical layers and different mammalian species to control discharge of these interneurons.

Kcns3Deficiency Disrupts Parvalbumin Neuron Physiology in Mouse Prefrontal Cortex: Implications for the pathophysiology of schizophrenia

“…The variety of Kv channel genes expressed by PV neurons is highly conserved between mouse and human neocortex (Okaty et al, 2009;Enwright et al, 2018;Krienen et al, 2019)(http://interneuron.mccarrolllab.org/). These and other similarities in voltage-gated channel gene expression suggest that PV neurons from human neocortex display FS properties, as verified experimentally (Wang et al, 2016;Stedehouder et al, 2017;Szegedi et al, 2017;Stedehouder et al, 2019;Szegedi et al, 2020). Hence, Kcns3 deficiency may produce qualitatively similar electrophysiological changes in PV neurons whether from mouse or human cortex.…”

Differential effects of group III metabotropic glutamate receptors on spontaneous inhibitory synaptic currents in spine-innervating double bouquet and parvalbumin-expressing dendrite-targeting GABAergic interneurons in human neocortex

“…Parvalbumin-expressing interneurons include axo-axonic and basket cells in rats (Kawaguchi & Kubota, 1998; Hartwich et al, 2009) and primates (Zaitsev et al, 2005) including humans (Szegedi et al, 2020). The term ‘basket cell’ is often used loosely for PV-expressing multipolar cells without information if the cells so named form perisomatic baskets or terminate on somata at all.…”

“…Furthermore, several other types of GABAergic interneuron in rodents, cats and primates, particularly those expressing VIP and/or CCK, and/or CR (Freund et al, 1986;Condé et al, 1994;Kawaguchi & Kubota, 1996Meskenaite, 1997;Caputi et al, 2009), and some basket cells (Somogyi et al, 1983;DeFelipe et al, 1986;Kisvárday, 1992;Jiang et al, 2015) also have descending axon collaterals crossing several layers without forming a narrow bundle. In conclusion, the available evidence suggests that Parvalbumin-expressing interneurons include axo-axonic and basket cells in rats (Kawaguchi & Kubota, 1998;Hartwich et al, 2009) and primates (Zaitsev et al, 2005) including humans (Szegedi et al, 2020). The term 'basket cell' is often used loosely for PV-expressing multipolar cells without information if the cells so named form perisomatic baskets or terminate on somata at all.…”

Differential effects of group III metabotropic glutamate receptors on spontaneous inhibitory synaptic currents in spine-innervating double bouquet and parvalbumin-expressing dendrite-targeting GABAergic interneurons in human neocortex

“…Furthermore, several other types of GABAergic interneuron in rodents, cats and primates, particularly those expressing VIP and/or CCK, and/or CR (Freund et al, 1986;Condé et al, 1994;Kawaguchi & Kubota, 1996Meskenaite, 1997;Caputi et al, 2009), and some basket cells (Somogyi et al, 1983;DeFelipe et al, 1986;Kisvárday, 1992;Jiang et al, 2015) also have descending axon collaterals crossing several layers without forming a narrow bundle. In conclusion, the available evidence suggests that Parvalbumin-expressing interneurons include axo-axonic and basket cells in rats (Kawaguchi & Kubota, 1998;Hartwich et al, 2009) and primates (Zaitsev et al, 2005) including humans (Szegedi et al, 2020). The term 'basket cell' is often used loosely for PV-expressing multipolar cells without information if the cells so named form perisomatic baskets or terminate on somata at all.…”