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The role of paralemniscal circuits in cortical plasticity and perception

English title The role of paralemniscal circuits in cortical plasticity and perception
Applicant Holtmaat Anthony
Number 173125
Funding scheme Project funding (Div. I-III)
Research institution Dépt des Neurosciences Fondamentales Faculté de Médecine Université de Genève
Institution of higher education University of Geneva - GE
Main discipline Neurophysiology and Brain Research
Start/End 01.10.2017 - 30.09.2021
Approved amount 1'008'000.00
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All Disciplines (2)

Discipline
Neurophysiology and Brain Research
Cellular Biology, Cytology

Keywords (6)

barrel cortex; paralemniscal circuits; synaptic plasticity; sensory perception; long-term potentiation; 2-photon microscopy

Lay Summary (French)

Lead
Le projet fournira des informations importantes sur la façon dont les systèmes de rétroaction du thalamus contribuent à la plasticité corticale et à l'apprentissage perceptuel sensoriel.
Lay summary

Au cours d’un apprentissage sensoriel, on pense que les neurones du cortex cérébral modifient la force de leurs connexions synaptiques. Malgré la pléthore de connaissances sur les aspects cellulaires de ces changements, il y a une pénurie d’information sur les circuits neuronaux qui les contrôlent.

Les aires corticales sensorielles reçoivent des informations à partir des organes sensoriels via le thalamus, puis les traites avant de les envoyer vers d'autres zones corticales afin d’être intégrées et générer un comportement. La dissémination d'information à d'autres zones corticales se produit en partie grâce à des connexions rétroactives qui repassent par le thalamus.

Nous étudierons le rôle de l'un de ces systèmes de rétroaction dans le système somatosensoriel (une modalité sensorielle qui traite le toucher) dans la plasticité corticale. Ce système s'appelle la voie extra-lemniscale (VEL), par opposition à la voie lemniscale (VL), qui traite les principales informations sensorielles entrantes.

Nous surveillerons l'activité de la VEL lors de l'apprentissage sensoriel en utilisant l'imagerie à travers des fenêtres crâniennes chez la souris. Cela nous révélera potentiellement les signaux instructifs de ce système pendant la phase d'apprentissage.

Nous examinerons également le rôle de la VEL sur la plasticité synaptique ex vivo dans le cortex, en enregistrant des neurones corticaux tout en combinant l'activation artificielle de la VL et de la VEL.

Au total, ce projet fournira des informations importantes sur la façon dont la VEL contribue à la plasticité corticale et à l'apprentissage perceptuel sensoriel, ce qui est essentiel pour faire progresser notre compréhension des mécanismes d'apprentissage et peut finalement aider à concevoir des traitements du traumatisme cérébral.
Direct link to Lay Summary Last update: 14.06.2017

Responsible applicant and co-applicants

Employees

Project partner

Natural persons


Name Institute

Publications

Publication
Dynamic perceptual feature selectivity in primary somatosensory cortex upon reversal learning
Chéreau Ronan, Bawa Tanika, Fodoulian Leon, Carleton Alan, Pagès Stéphane, Holtmaat Anthony (2020), Dynamic perceptual feature selectivity in primary somatosensory cortex upon reversal learning, in Nature Communications, 11, 3245.
Temporal Sharpening of Sensory Responses by Layer V in the Mouse Primary Somatosensory Cortex
Vecchia Dania, Beltramo Riccardo, Vallone Fabio, Chéreau Ronan, Forli Angelo, Molano-Mazón Manuel, Bawa Tanika, Binini Noemi, Moretti Claudio, Holtmaat Anthony, Panzeri Stefano, Fellin Tommaso (2020), Temporal Sharpening of Sensory Responses by Layer V in the Mouse Primary Somatosensory Cortex, in Current Biology, 30(9), 1589-1599.e10.
The mesoSPIM initiative: open-source light-sheet microscopes for imaging cleared tissue
Voigt Fabian F., Kirschenbaum Daniel, Platonova Evgenia, Pagès Stéphane, Campbell Robert A. A., Kastli Rahel, Schaettin Martina, Egolf Ladan, van der Bourg Alexander, Bethge Philipp, Haenraets Karen, Frézel Noémie, Topilko Thomas, Perin Paola, Hillier Daniel, Hildebrand Sven, Schueth Anna, Roebroeck Alard, Roska Botond, Stoeckli Esther T., Pizzala Roberto, Renier Nicolas, Zeilhofer Hanns Ulrich, Karayannis Theofanis, et al. (2019), The mesoSPIM initiative: open-source light-sheet microscopes for imaging cleared tissue, in Nature Methods, 16(11), 1105-1108.
Higher-Order Thalamocortical Inputs Gate Synaptic Long-Term Potentiation via Disinhibition
Williams Leena E., Holtmaat Anthony (2019), Higher-Order Thalamocortical Inputs Gate Synaptic Long-Term Potentiation via Disinhibition, in Neuron, 101(1), 91-102.e4.

Datasets

Higher-Order Thalamocortical Inputs Gate Synaptic Long-Term Potentiation via Disinhibition

Author Williams, Leena E.; Holtmaat, Anthony
Publication date 01.01.2019
Persistent Identifier (PID) 10.5281/zenodo.3922200
Repository Data set for "Higher-Order Thalamocortical Inputs Gate Synaptic Long-Term Potentiation via Disinhibition"
Abstract
This repository contains the data used to generate the figures

Dynamic perceptual feature selectivity in primary somatosensory cortex upon reversal learning

Author Chéreau, Ronan; Bawa, Tanika; Fodoulian, Leon; Carleton, Alan; Pagès, Stéphane; Holtmaat, Anthony
Publication date 26.12.2020
Persistent Identifier (PID) 10.5281/zenodo.3824493
Repository Data set for "Dynamic perceptual feature selectivity in primary somatosensory cortex upon reversal learning"
Abstract
This repository contains the data used to generate the figures and well as the main codes that were used for analyses.

Collaboration

Group / person Country
Types of collaboration
Helmchen lab at Brain Research Institute Zurich Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Fellin lab at IIT Genova, Italy Italy (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Excitatory Synapses and Brain Function GRC 2019 Talk given at a conference Context-Dependent Dynamics of Functional Selectivity in Somatosensory Cortex 09.06.2020 Manchester, NH, United States of America Holtmaat Anthony;
Seminar series Center for Brain Discovery Research, University of Edinburgh Individual talk (Dys)functional Somatosensory Cortical Circuits 26.02.2020 Edinburgh, Great Britain and Northern Ireland Williams Leena;
Seminar Series University Manchester Individual talk (Dys)functional Somatosensory Cortical Circuits 25.02.2020 Manchester, Great Britain and Northern Ireland Williams Leena;
Swiss Society for Neuroscience annual meeting 2020 Poster Input specific dendritic integration by barrel cortex supragranular pyramidal cells 22.02.2020 Bern, Switzerland Brandalise Federico;
Thalamocortical Interactions GRC Talk given at a conference Higher-Order Thalamocortical Projections and Cortical Plasticity 16.02.2020 Ventura, CA, United States of America Holtmaat Anthony;
Swisskers Meeting 2020 at Uni Bern Talk given at a conference Dendritic integration of long-range inputs by barrel cortex pyramidal cells 28.01.2020 Bern, Switzerland Brandalise Federico; Holtmaat Anthony;
EMBL Volume EM by Automated Serial SEM Workshop Talk given at a conference Flashtalk: CLEM of synpases in L1 of the mouse somatosensensory cortex 20.10.2019 Heidelberg, Germany Lee Kok Sin;
Giessbach Neuroscience meeting 2019 Talk given at a conference Talk by Ronan Chereau: Dynamic perceptual feature selectivity in primary somatosensory cortex upon reversal learning 23.05.2019 Giessbach, Switzerland Holtmaat Anthony;
Lemanic Neuroscience Doctoral School Annual Meeting 2019 Poster Morphological characterisation of synpases from long-range connections in L1 of the mouse somatosensensory cortex 03.05.2019 Les Diablerets, Switzerland Holtmaat Anthony; Lee Kok Sin;
Lemanic Neuroscience Doctoral School Annual Meeting 2019 Poster Functional and anatomical characterisation of the higher-order thalamic nucleus POm 02.05.2019 Les Diablerets, Switzerland Bawa Tanika Kaur; Holtmaat Anthony;
Dendritic Mechanisms in Neuronal Plasticity, Computation, Learning and Behavior GRC 2019 Poster Plateau potentials driven by higher-order thalamus mediate cortical map reorganization 31.03.2019 Ventura, CA, United States of America Holtmaat Anthony;
Swisskers Meeting 2019 at the FMI Talk given at a conference Talk by Ronan Chereau: Stimulus value-mediated tuning of neuronal activity in somatosensory cortex during perceptual learning 15.02.2019 Basel, Switzerland Bawa Tanika Kaur; Holtmaat Anthony;
Swiss Society for Neurosciences annual meeting 2019 Poster Higher-order thalamocortical inputs gate synaptic LTP via disinhibition 01.02.2019 Geneva, Switzerland Holtmaat Anthony; Williams Leena;
Swiss Society for Neuroscience annual meeting 2019 Poster Stimulus value-mediated tuning of neuronal activity in somatosensory cortex during perceptual learning 01.02.2019 Geneva, Switzerland Bawa Tanika Kaur; Holtmaat Anthony;
Young Swiss Society for Neurosciences Talk given at a conference Higher-Order Thalamocortical Inputs Gate Synaptic LTP via Disinhibition. 31.01.2019 Geneva, Switzerland Williams Leena;
Institutional Seminar Series DEPARTAMENTO DE ANATOMIA, HISTOLOGIA Y NEUROCIENCIA Individual talk The role of higher-order thalamocortical input in cortical synaptic plasticity 18.01.2019 Madrid, Spain Holtmaat Anthony;
Cajal School 2018 Linking Neural Circuits and Behaviour Individual talk Synaptic and circuit mechanisms for cortical plasticity 08.10.2018 Bordeaux, France Holtmaat Anthony;
Institutional Seminar Series IIT Genova Individual talk The role of higher-order thalamocortical feedback in cortical synaptic plasticity 24.09.2018 Genova, Italy Holtmaat Anthony;
FENS forum 2018 Berlin Poster Higher-Order Thalamocortical Inputs Gate LTP via Disinhibition 07.07.2018 Berlin, Germany Williams Leena;
Symposium of Neuroscience at CityU Hong Kong Individual talk Synaptic and circuit mechanisms for cortical plasticity 08.06.2018 Hong Kong, Hongkong Holtmaat Anthony;
Neuroplasticity and Maladaptation of Sensory Systems GRC Hong Kong Poster The role of higher-order thalamocortical feedback in cortical synaptic plasticity 03.06.2018 Hong Kong, Hongkong Williams Leena; Holtmaat Anthony; Bawa Tanika Kaur;
20th International Neuroscience Winter Conference Talk given at a conference Circuit mechanisms underlying cortical plasticity 11.04.2018 Sölden, Australia Holtmaat Anthony;
Development, Function and Dysfunction of Thalamocortical Networks GRC 2018 Poster Diverse coding of higher-order thalamocortical projections during sensory perception - poster by Chereau 18.02.2018 Lucca (Barga), Italy Bawa Tanika Kaur; Holtmaat Anthony;
6th European Synapse Meeting Talk given at a conference Circuit mechanisms for cortical synaptic plasticity 04.12.2017 Milano, Italy Holtmaat Anthony;


Awards

Title Year
2019 NARSAD Young Investigator Grant 2019

Associated projects

Number Title Start Funding scheme
153448 Activity-dependent functional and structural plasticity in the somatosensory cortex in vivo 01.04.2014 Project funding (Div. I-III)
153448 Activity-dependent functional and structural plasticity in the somatosensory cortex in vivo 01.04.2014 Project funding (Div. I-III)
154453 Function and structure of neuromodulatory inputs to the cerebral cortex 01.01.2015 Sinergia

Abstract

Sensory perception depends on the integration of multisensory information. The cerebral cortex plays a critical role in this process in order to produce a relevant (behavioral) response. The cortex receives information from and sends information back to the thalamus, which is composed of various nuclei that interact with the cortex in a hierarchical order. Some nuclei primarily transmit incoming sensory information directly to the cortex, others primarily receive information from the cortex in order to return and disseminate it again over a large array of other cortical targets. The latter structures are often referred to as higher-order thalamic nuclei. Similarities in their anatomical layout and connectivity pattern across various sensory modalities suggest that higher-order thalamic nuclei share similar roles among all types of perception. However, how their output affects cortical activity and ultimately how it relates to sensory perception and learning remains poorly understood.In the current proposal we aim at investigating the role of the paralemniscal pathway, a higher-order thalamocortical circuit in the somatosensory system, in cortical plasticity and sensory perception. In contrast to the lemniscal pathway, the paralemniscal pathway receives most of its inputs from cortex, and in turn is thought to send modulatory input back into the primary somatosensory cortex (S1). The project is divided into three aims. First we will investigate how activity in the thalamocortical paralemniscal pathway shapes cortical plasticity in S1. This project stems from earlier work in which we had observed that the paralemniscal drive is essential for sensory-evoked synaptic long-term potentiation in the cortex. We will follow up on this work by investigating the circuit mechanisms of paralameniscal pathway-facilitated plasticity, and we will study how perturbing the activity of this circuit affects cortical plasticity in S1 over days to weeks in vivo. Second, we will investigate the relationship between paralemniscal input activity in S1 and reward-based sensory discrimination. We will correlate activity patterns in thalamocortical projections with particular aspects of the sensory percept and behavioral outcomes of a whisker-mediated texture-discrimination task. We will also study the effects of reducing paralemniscal activity on the discrimination performance in this task and the learning process leading up to it. Third, we will relate the aforementioned functions of the paralemniscal pathway to the anatomy of their synaptic connections in S1. We will characterize their morphology and dissect synaptic connectivity within local microcircuits that may be of importance for the presumed gating function of this pathway in layer 1 of S1. These aspects will be studied by utilizing optogenetic and chemogenetic tools, in vitro and in vivo electrophysiology, texture-discrimination tasks, two-photon laser scanning microscopy of neuronal activity (Ca2+ imaging) and neuronal structure, and focused ion beam scanning electron microscopy. Together, the proposal will reveal important information about the function of the paralemniscal system, and how it contributes to cortical plasticity and somatosensory perception, which is essential for advancing our understanding of the mechanisms underlying perceptual learning.
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