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 human neocortical tissue resected in deep-brain surgery, and in mice as control. 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 self-inhibition 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 is common in both human and mouse pvBCs of supragranular neocortex, where they efficiently control discharge of the pvBCs.
Data availability
All data generated or analyzed during this study are included in the manuscript and supporting files.
Article and author information
Author details
Funding
NKFIH (National Brain Research Programme)
- Viktor Szegedi
- Melinda Paizs
- Karri Lamsa
ERC (INTERIMPACT)
- Gabor Tamas
Hungarian Academy of Sciences
- Viktor Szegedi
- Gábor Molnár
University of Szeged Open Access Fund (4373)
- Viktor Szegedi
- Karri Lamsa
Eotvos Lorand Research Network
- Gabor Tamas
National Research, Development and Innovation Office of Hungary (GINOP-2.3.2-15-2016-00018)
- Gabor Tamas
National Research, Development and Innovation Office (OTKA K128863)
- Gábor Molnár
- Gabor Tamas
- Karri Lamsa
Ministry of Human Capacities Hungary (20391-3/2018/FEKUSTRAT)
- Gabor Tamas
- Karri Lamsa
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- John Huguenard, Stanford University School of Medicine, United States
Ethics
Animal experimentation: All procedures were performed with the approval of theUniversity of Szeged (no. I-74-8/2016) and in accordance withthe Guide for the Care and Use of Laboratory Animals (2011)(http://grants.nih.gov/grants/olaw/guide-for-the-care-and-use-oflaboratory-animals.pdf).
Human subjects: All procedures were performed according to the Declaration of Helsinki with the approval of the University of Szeged Ethical Committee and Regional Human Investigation Review Board (ref. 75/2014). For all human tissue material, written consent was obtained from patients prior to surgery. Tissue obtained from underage patients was provided with agreement from a parent or guardian.
Version history
- Received: September 6, 2019
- Accepted: January 8, 2020
- Accepted Manuscript published: January 9, 2020 (version 1)
- Version of Record published: January 27, 2020 (version 2)
Copyright
© 2020, Szegedi et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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- Neuroscience
Probing memory of a complex visual image within a few hundred milliseconds after its disappearance reveals significantly greater fidelity of recall than if the probe is delayed by as little as a second. Classically interpreted, the former taps into a detailed but rapidly decaying visual sensory or ‘iconic’ memory (IM), while the latter relies on capacity-limited but comparatively stable visual working memory (VWM). While iconic decay and VWM capacity have been extensively studied independently, currently no single framework quantitatively accounts for the dynamics of memory fidelity over these time scales. Here, we extend a stationary neural population model of VWM with a temporal dimension, incorporating rapid sensory-driven accumulation of activity encoding each visual feature in memory, and a slower accumulation of internal error that causes memorized features to randomly drift over time. Instead of facilitating read-out from an independent sensory store, an early cue benefits recall by lifting the effective limit on VWM signal strength imposed when multiple items compete for representation, allowing memory for the cued item to be supplemented with information from the decaying sensory trace. Empirical measurements of human recall dynamics validate these predictions while excluding alternative model architectures. A key conclusion is that differences in capacity classically thought to distinguish IM and VWM are in fact contingent upon a single resource-limited WM store.
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- Neuroscience
Our ability to recall details from a remembered image depends on a single mechanism that is engaged from the very moment the image disappears from view.