Supralinear dendritic integration in murine dendrite-targeting interneurons

Non-linear summation of synaptic inputs to the dendrites of pyramidal neurons has been proposed to increase the computation capacity of neurons through coincidence detection, signal amplification, and additional logic operations such as XOR. Supralinear dendritic integration has been documented exte...

Full description

Saved in:
Bibliographic Details
Main Authors: Simonas Griesius, Amy Richardson, Dimitri Michael Kullmann
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2025-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/100268
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1832576073393504256
author Simonas Griesius
Amy Richardson
Dimitri Michael Kullmann
author_facet Simonas Griesius
Amy Richardson
Dimitri Michael Kullmann
author_sort Simonas Griesius
collection DOAJ
description Non-linear summation of synaptic inputs to the dendrites of pyramidal neurons has been proposed to increase the computation capacity of neurons through coincidence detection, signal amplification, and additional logic operations such as XOR. Supralinear dendritic integration has been documented extensively in principal neurons, mediated by several voltage-dependent conductances. It has also been reported in parvalbumin-positive hippocampal basket cells, in dendrites innervated by feedback excitatory synapses. Whether other interneurons, which support feed-forward or feedback inhibition of principal neuron dendrites, also exhibit local non-linear integration of synaptic excitation is not known. Here, we use patch-clamp electrophysiology, and two-photon calcium imaging and glutamate uncaging, to show that supralinear dendritic integration of near-synchronous spatially clustered glutamate-receptor mediated depolarization occurs in NDNF-positive neurogliaform cells and oriens-lacunosum moleculare interneurons in the mouse hippocampus. Supralinear summation was detected via recordings of somatic depolarizations elicited by uncaging of glutamate on dendritic fragments, and, in neurogliaform cells, by concurrent imaging of dendritic calcium transients. Supralinearity was abolished by blocking NMDA receptors (NMDARs) but resisted blockade of voltage-gated sodium channels. Blocking L-type calcium channels abolished supralinear calcium signalling but only had a minor effect on voltage supralinearity. Dendritic boosting of spatially clustered synaptic signals argues for previously unappreciated computational complexity in dendrite-projecting inhibitory cells of the hippocampus.
format Article
id doaj-art-d1ba85a66a424517b6718a2b4417b6df
institution Kabale University
issn 2050-084X
language English
publishDate 2025-01-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj-art-d1ba85a66a424517b6718a2b4417b6df2025-01-31T12:01:04ZengeLife Sciences Publications LtdeLife2050-084X2025-01-011310.7554/eLife.100268Supralinear dendritic integration in murine dendrite-targeting interneuronsSimonas Griesius0https://orcid.org/0000-0002-2025-1064Amy Richardson1https://orcid.org/0000-0002-1552-2915Dimitri Michael Kullmann2https://orcid.org/0000-0001-6696-3545Department of Clinical Experimental and Epilepsy, UCL Queen Square Institute of Neurology, University College London, London, United KingdomDepartment of Clinical Experimental and Epilepsy, UCL Queen Square Institute of Neurology, University College London, London, United KingdomDepartment of Clinical Experimental and Epilepsy, UCL Queen Square Institute of Neurology, University College London, London, United KingdomNon-linear summation of synaptic inputs to the dendrites of pyramidal neurons has been proposed to increase the computation capacity of neurons through coincidence detection, signal amplification, and additional logic operations such as XOR. Supralinear dendritic integration has been documented extensively in principal neurons, mediated by several voltage-dependent conductances. It has also been reported in parvalbumin-positive hippocampal basket cells, in dendrites innervated by feedback excitatory synapses. Whether other interneurons, which support feed-forward or feedback inhibition of principal neuron dendrites, also exhibit local non-linear integration of synaptic excitation is not known. Here, we use patch-clamp electrophysiology, and two-photon calcium imaging and glutamate uncaging, to show that supralinear dendritic integration of near-synchronous spatially clustered glutamate-receptor mediated depolarization occurs in NDNF-positive neurogliaform cells and oriens-lacunosum moleculare interneurons in the mouse hippocampus. Supralinear summation was detected via recordings of somatic depolarizations elicited by uncaging of glutamate on dendritic fragments, and, in neurogliaform cells, by concurrent imaging of dendritic calcium transients. Supralinearity was abolished by blocking NMDA receptors (NMDARs) but resisted blockade of voltage-gated sodium channels. Blocking L-type calcium channels abolished supralinear calcium signalling but only had a minor effect on voltage supralinearity. Dendritic boosting of spatially clustered synaptic signals argues for previously unappreciated computational complexity in dendrite-projecting inhibitory cells of the hippocampus.https://elifesciences.org/articles/100268Brainsynapseinterneurondendrite
spellingShingle Simonas Griesius
Amy Richardson
Dimitri Michael Kullmann
Supralinear dendritic integration in murine dendrite-targeting interneurons
eLife
Brain
synapse
interneuron
dendrite
title Supralinear dendritic integration in murine dendrite-targeting interneurons
title_full Supralinear dendritic integration in murine dendrite-targeting interneurons
title_fullStr Supralinear dendritic integration in murine dendrite-targeting interneurons
title_full_unstemmed Supralinear dendritic integration in murine dendrite-targeting interneurons
title_short Supralinear dendritic integration in murine dendrite-targeting interneurons
title_sort supralinear dendritic integration in murine dendrite targeting interneurons
topic Brain
synapse
interneuron
dendrite
url https://elifesciences.org/articles/100268
work_keys_str_mv AT simonasgriesius supralineardendriticintegrationinmurinedendritetargetinginterneurons
AT amyrichardson supralineardendriticintegrationinmurinedendritetargetinginterneurons
AT dimitrimichaelkullmann supralineardendriticintegrationinmurinedendritetargetinginterneurons