Methods: We recorded extracellular field potentials from the primary visual cortex (V1) of head-fixed awake FHM1 knock-in (n = 12) and wild type (n = 12) mice in response to square-wave gratings with different visual contrasts. Additionally, we reproduced in silico the obtained experimental results with a novel spiking neurons network model of mouse V1, by implementing in the model both the synaptic alterations characterizing the FHM1 genetic mouse model adopted.
Background: Migraine affects a significant fraction of the world population, yet its etiology is not completely understood. In vitro results highlighted thalamocortical and intra-cortical glutamatergic synaptic gain-of-function associated with a monogenic form of migraine (familial-hemiplegic-migraine-type-1: FHM1). However, how these alterations reverberate on cortical activity remains unclear. As altered responsivity to visual stimuli and abnormal processing of visual sensory information are common hallmarks of migraine, herein we investigated the effects of FHM1-driven synaptic alterations in the visual cortex of awake mice.
Synaptic alterations in visual cortex reshape contrast-dependent gamma oscillations and inhibition-excitation ratio in a genetic mouse model of migraine
Vannini Eleonora;Tantillo Elena;Caleo MatteoCo-ultimo
;
2022
Abstract
Background: Migraine affects a significant fraction of the world population, yet its etiology is not completely understood. In vitro results highlighted thalamocortical and intra-cortical glutamatergic synaptic gain-of-function associated with a monogenic form of migraine (familial-hemiplegic-migraine-type-1: FHM1). However, how these alterations reverberate on cortical activity remains unclear. As altered responsivity to visual stimuli and abnormal processing of visual sensory information are common hallmarks of migraine, herein we investigated the effects of FHM1-driven synaptic alterations in the visual cortex of awake mice.| Campo DC | Valore | Lingua |
|---|---|---|
| dc.authority.ancejournal | THE JOURNAL OF HEADACHE AND PAIN (TESTO STAMP.) | en |
| dc.authority.orgunit | Istituto di Neuroscienze - IN - | en |
| dc.authority.people | Meneghetti Nicolo | en |
| dc.authority.people | Cerri Chiara | en |
| dc.authority.people | Vannini Eleonora | en |
| dc.authority.people | Tantillo Elena | en |
| dc.authority.people | Tottene Angelita | en |
| dc.authority.people | Pietrobon Daniela | en |
| dc.authority.people | Caleo Matteo | en |
| dc.authority.people | Mazzoni Alberto | en |
| dc.collection.id.s | b3f88f24-048a-4e43-8ab1-6697b90e068e | * |
| dc.collection.name | 01.01 Articolo in rivista | * |
| dc.contributor.appartenenza | Istituto di Neuroscienze - IN - | * |
| dc.contributor.appartenenza.mi | 942 | * |
| dc.contributor.area | Non assegn | * |
| dc.date.accessioned | 2024/02/21 02:40:36 | - |
| dc.date.available | 2024/02/21 02:40:36 | - |
| dc.date.firstsubmission | 2025/02/20 10:26:23 | * |
| dc.date.issued | 2022 | - |
| dc.date.submission | 2025/02/20 11:23:07 | * |
| dc.description.abstract | Methods: We recorded extracellular field potentials from the primary visual cortex (V1) of head-fixed awake FHM1 knock-in (n = 12) and wild type (n = 12) mice in response to square-wave gratings with different visual contrasts. Additionally, we reproduced in silico the obtained experimental results with a novel spiking neurons network model of mouse V1, by implementing in the model both the synaptic alterations characterizing the FHM1 genetic mouse model adopted. | - |
| dc.description.abstracteng | Background: Migraine affects a significant fraction of the world population, yet its etiology is not completely understood. In vitro results highlighted thalamocortical and intra-cortical glutamatergic synaptic gain-of-function associated with a monogenic form of migraine (familial-hemiplegic-migraine-type-1: FHM1). However, how these alterations reverberate on cortical activity remains unclear. As altered responsivity to visual stimuli and abnormal processing of visual sensory information are common hallmarks of migraine, herein we investigated the effects of FHM1-driven synaptic alterations in the visual cortex of awake mice. | - |
| dc.description.affiliations | Scuola Super Sant Anna; Scuola Super Sant Anna; Natl Res Council CNR; Fdn Umberto Veronesi; Univ Pisa; Fdn Pisana Sci Onlus FPS; Scuola Normale Super Pisa; Univ Padua; Univ Padua; CNR Inst Neurosci | - |
| dc.description.allpeople | Meneghetti, Nicolo; Cerri, Chiara; Vannini, Eleonora; Tantillo, Elena; Tottene, Angelita; Pietrobon, Daniela; Caleo, Matteo; Mazzoni, Alberto | - |
| dc.description.allpeopleoriginal | Meneghetti, Nicolo; Cerri, Chiara; Vannini, Eleonora; Tantillo, Elena; Tottene, Angelita; Pietrobon, Daniela; Caleo, Matteo; Mazzoni, Alberto | en |
| dc.description.fulltext | open | en |
| dc.description.numberofauthors | 8 | - |
| dc.identifier.doi | 10.1186/s10194-022-01495-9 | en |
| dc.identifier.isi | WOS:000861899200003 | en |
| dc.identifier.scopus | 2-s2.0-85138903577 | en |
| dc.identifier.uri | https://hdl.handle.net/20.500.14243/413480 | - |
| dc.language.iso | eng | en |
| dc.miur.last.status.update | 2025-01-07T12:14:44Z | * |
| dc.relation.issue | 1 | en |
| dc.relation.numberofpages | 18 | en |
| dc.relation.volume | 23 | en |
| dc.subject.keywordseng | Migraine | - |
| dc.subject.keywordseng | Visual cortex | - |
| dc.subject.keywordseng | Mice | - |
| dc.subject.keywordseng | Gamma oscillations | - |
| dc.subject.keywordseng | Spiking neurons networks | - |
| dc.subject.keywordseng | Familial-hemiplegic-type1-migraine | - |
| dc.subject.keywordseng | Mutual information | - |
| dc.subject.singlekeyword | Migraine | * |
| dc.subject.singlekeyword | Visual cortex | * |
| dc.subject.singlekeyword | Mice | * |
| dc.subject.singlekeyword | Gamma oscillations | * |
| dc.subject.singlekeyword | Spiking neurons networks | * |
| dc.subject.singlekeyword | Familial-hemiplegic-type1-migraine | * |
| dc.subject.singlekeyword | Mutual information | * |
| dc.title | Synaptic alterations in visual cortex reshape contrast-dependent gamma oscillations and inhibition-excitation ratio in a genetic mouse model of migraine | en |
| dc.type.driver | info:eu-repo/semantics/article | - |
| dc.type.full | 01 Contributo su Rivista::01.01 Articolo in rivista | it |
| dc.type.miur | 262 | - |
| dc.ugov.descaux1 | 477191 | - |
| iris.isi.extIssued | 2022 | - |
| iris.isi.extTitle | Synaptic alterations in visual cortex reshape contrast-dependent gamma oscillations and inhibition-excitation ratio in a genetic mouse model of migraine | - |
| iris.isi.ideLinkStatusDate | 2025/02/17 15:52:42 | * |
| iris.isi.ideLinkStatusMillisecond | 1739803962891 | * |
| iris.mediafilter.data | 2025/04/09 03:46:15 | * |
| iris.orcid.lastModifiedDate | 2025/02/20 11:51:01 | * |
| iris.orcid.lastModifiedMillisecond | 1740048661561 | * |
| iris.scopus.extIssued | 2022 | - |
| iris.scopus.extTitle | Synaptic alterations in visual cortex reshape contrast-dependent gamma oscillations and inhibition-excitation ratio in a genetic mouse model of migraine | - |
| iris.scopus.ideLinkStatusDate | 2025/02/17 15:52:41 | * |
| iris.scopus.ideLinkStatusMillisecond | 1739803961338 | * |
| iris.sitodocente.maxattempts | 1 | - |
| iris.unpaywall.bestoahost | publisher | * |
| iris.unpaywall.bestoaversion | publishedVersion | * |
| iris.unpaywall.doi | 10.1186/s10194-022-01495-9 | * |
| iris.unpaywall.hosttype | publisher | * |
| iris.unpaywall.isoa | true | * |
| iris.unpaywall.journalisindoaj | true | * |
| iris.unpaywall.landingpage | https://doi.org/10.1186/s10194-022-01495-9 | * |
| iris.unpaywall.license | cc-by | * |
| iris.unpaywall.metadataCallLastModified | 01/05/2026 05:38:57 | - |
| iris.unpaywall.metadataCallLastModifiedMillisecond | 1777606737665 | - |
| iris.unpaywall.oastatus | gold | * |
| iris.unpaywall.pdfurl | https://thejournalofheadacheandpain.biomedcentral.com/counter/pdf/10.1186/s10194-022-01495-9 | * |
| isi.authority.ancejournal | THE JOURNAL OF HEADACHE AND PAIN###1129-2369 | * |
| isi.category | RT | * |
| isi.category | RU | * |
| isi.contributor.affiliation | Scuola Superiore Sant'Anna | - |
| isi.contributor.affiliation | Natl Res Council CNR | - |
| isi.contributor.affiliation | Natl Res Council CNR | - |
| isi.contributor.affiliation | Natl Res Council CNR | - |
| isi.contributor.affiliation | University of Padua | - |
| isi.contributor.affiliation | University of Padua | - |
| isi.contributor.affiliation | Natl Res Council CNR | - |
| isi.contributor.affiliation | Scuola Superiore Sant'Anna | - |
| isi.contributor.country | Italy | - |
| isi.contributor.country | Italy | - |
| isi.contributor.country | Italy | - |
| isi.contributor.country | Italy | - |
| isi.contributor.country | Italy | - |
| isi.contributor.country | Italy | - |
| isi.contributor.country | Italy | - |
| isi.contributor.country | Italy | - |
| isi.contributor.name | Nicolo | - |
| isi.contributor.name | Chiara | - |
| isi.contributor.name | Eleonora | - |
| isi.contributor.name | Elena | - |
| isi.contributor.name | Angelita | - |
| isi.contributor.name | Daniela | - |
| isi.contributor.name | Matteo | - |
| isi.contributor.name | Alberto | - |
| isi.contributor.researcherId | HTP-5224-2023 | - |
| isi.contributor.researcherId | FZB-3639-2022 | - |
| isi.contributor.researcherId | P-2303-2018 | - |
| isi.contributor.researcherId | DWV-4976-2022 | - |
| isi.contributor.researcherId | GJU-8072-2022 | - |
| isi.contributor.researcherId | JUF-4037-2023 | - |
| isi.contributor.researcherId | DWG-9653-2022 | - |
| isi.contributor.researcherId | A-5433-2018 | - |
| isi.contributor.subaffiliation | Biorobot Inst | - |
| isi.contributor.subaffiliation | Neurosci Inst | - |
| isi.contributor.subaffiliation | Neurosci Inst | - |
| isi.contributor.subaffiliation | Neurosci Inst | - |
| isi.contributor.subaffiliation | Dept Biomed Sci | - |
| isi.contributor.subaffiliation | Dept Biomed Sci | - |
| isi.contributor.subaffiliation | Neurosci Inst | - |
| isi.contributor.subaffiliation | Biorobot Inst | - |
| isi.contributor.surname | Meneghetti | - |
| isi.contributor.surname | Cerri | - |
| isi.contributor.surname | Vannini | - |
| isi.contributor.surname | Tantillo | - |
| isi.contributor.surname | Tottene | - |
| isi.contributor.surname | Pietrobon | - |
| isi.contributor.surname | Caleo | - |
| isi.contributor.surname | Mazzoni | - |
| isi.date.issued | 2022 | * |
| isi.description.abstracteng | Background: Migraine affects a significant fraction of the world population, yet its etiology is not completely understood. In vitro results highlighted thalamocortical and intra-cortical glutamatergic synaptic gain-of-function associated with a monogenic form of migraine (familial-hemiplegic-migraine-type-1: FHM1). However, how these alterations reverberate on cortical activity remains unclear. As altered responsivity to visual stimuli and abnormal processing of visual sensory information are common hallmarks of migraine, herein we investigated the effects of FHM1-driven synaptic alterations in the visual cortex of awake mice.Methods: We recorded extracellular field potentials from the primary visual cortex (V1) of head-fixed awake FHM1 knock-in (n = 12) and wild type (n = 12) mice in response to square-wave gratings with different visual contrasts. Additionally, we reproduced in silico the obtained experimental results with a novel spiking neurons network model of mouse V1, by implementing in the model both the synaptic alterations characterizing the FHM1 genetic mouse model adopted.Results: FHM1 mice displayed similar amplitude but slower temporal evolution of visual evoked potentials. Visual contrast stimuli induced a lower increase of multi-unit activity in FHM1 mice, while the amount of information content about contrast level remained, however, similar to WT.Spectral analysis of the local field potentials revealed an increase in the beta/low gamma range of WT mice following the abrupt reversal of contrast gratings. Such frequency range transitioned to the high y range in FHM1 mice. Despite this change in the encoding channel, these oscillations preserved the amount of information conveyed about visual contrast. The computational model showed how these network effects may arise from a combination of changes in thalamocortical and intra-cortical synaptic transmission, with the former inducing a lower cortical activity and the latter inducing the higher frequencies y oscillations.Conclusions: Contrast-driven gamma modulation in V1 activity occurs at a much higher frequency in FHM1. This is likely to play a role in the altered processing of visual information. Computational studies suggest that this shift is specifically due to enhanced cortical excitatory transmission. Our network model can help to shed light on the relationship between cellular and network levels of migraine neural alterations. | * |
| isi.description.allpeopleoriginal | Meneghetti, N; Cerri, C; Vannini, E; Tantillo, E; Tottene, A; Pietrobon, D; Caleo, M; Mazzoni, A; | * |
| isi.document.sourcetype | WOS.SCI | * |
| isi.document.type | Article | * |
| isi.document.types | Article | * |
| isi.identifier.doi | 10.1186/s10194-022-01495-9 | * |
| isi.identifier.eissn | 1129-2377 | * |
| isi.identifier.isi | WOS:000861899200003 | * |
| isi.journal.journaltitle | JOURNAL OF HEADACHE AND PAIN | * |
| isi.journal.journaltitleabbrev | J HEADACHE PAIN | * |
| isi.language.original | English | * |
| isi.publisher.place | CAMPUS, 4 CRINAN ST, LONDON N1 9XW, ENGLAND | * |
| isi.relation.issue | 1 | * |
| isi.relation.volume | 23 | * |
| isi.title | Synaptic alterations in visual cortex reshape contrast-dependent gamma oscillations and inhibition-excitation ratio in a genetic mouse model of migraine | * |
| scopus.authority.ancejournal | THE JOURNAL OF HEADACHE AND PAIN###1129-2369 | * |
| scopus.category | 2728 | * |
| scopus.category | 2703 | * |
| scopus.contributor.affiliation | Scuola Superiore Sant’Anna | - |
| scopus.contributor.affiliation | University of Pisa | - |
| scopus.contributor.affiliation | Fondazione Umberto Veronesi | - |
| scopus.contributor.affiliation | Scuola Normale Superiore | - |
| scopus.contributor.affiliation | University of Padova | - |
| scopus.contributor.affiliation | CNR Institute of Neuroscience | - |
| scopus.contributor.affiliation | University of Padova | - |
| scopus.contributor.affiliation | Scuola Superiore Sant’Anna | - |
| scopus.contributor.afid | 60028039 | - |
| scopus.contributor.afid | 60028868 | - |
| scopus.contributor.afid | 112827354 | - |
| scopus.contributor.afid | 60030674 | - |
| scopus.contributor.afid | 60000481 | - |
| scopus.contributor.afid | 60021199 | - |
| scopus.contributor.afid | 60000481 | - |
| scopus.contributor.afid | 60028039 | - |
| scopus.contributor.auid | 57219463916 | - |
| scopus.contributor.auid | 57195284720 | - |
| scopus.contributor.auid | 54387638800 | - |
| scopus.contributor.auid | 57188755628 | - |
| scopus.contributor.auid | 6603490744 | - |
| scopus.contributor.auid | 7003670065 | - |
| scopus.contributor.auid | 6603589444 | - |
| scopus.contributor.auid | 25931530400 | - |
| scopus.contributor.country | Italy | - |
| scopus.contributor.country | Italy | - |
| scopus.contributor.country | Italy | - |
| scopus.contributor.country | Italy | - |
| scopus.contributor.country | Italy | - |
| scopus.contributor.country | Italy | - |
| scopus.contributor.country | Italy | - |
| scopus.contributor.country | Italy | - |
| scopus.contributor.dptid | 125235834 | - |
| scopus.contributor.dptid | 104458909 | - |
| scopus.contributor.dptid | - | |
| scopus.contributor.dptid | - | |
| scopus.contributor.dptid | 110785477 | - |
| scopus.contributor.dptid | - | |
| scopus.contributor.dptid | - | |
| scopus.contributor.dptid | 125235834 | - |
| scopus.contributor.name | Nicolò | - |
| scopus.contributor.name | Chiara | - |
| scopus.contributor.name | Eleonora | - |
| scopus.contributor.name | Elena | - |
| scopus.contributor.name | Angelita | - |
| scopus.contributor.name | Daniela | - |
| scopus.contributor.name | Matteo | - |
| scopus.contributor.name | Alberto | - |
| scopus.contributor.subaffiliation | Department of Excellence for Robotics and AI; | - |
| scopus.contributor.subaffiliation | Department of Pharmacy; | - |
| scopus.contributor.subaffiliation | - | |
| scopus.contributor.subaffiliation | - | |
| scopus.contributor.subaffiliation | Department of Biomedical Sciences; | - |
| scopus.contributor.subaffiliation | - | |
| scopus.contributor.subaffiliation | Padova Neuroscience Center; | - |
| scopus.contributor.subaffiliation | Department of Excellence for Robotics and AI; | - |
| scopus.contributor.surname | Meneghetti | - |
| scopus.contributor.surname | Cerri | - |
| scopus.contributor.surname | Vannini | - |
| scopus.contributor.surname | Tantillo | - |
| scopus.contributor.surname | Tottene | - |
| scopus.contributor.surname | Pietrobon | - |
| scopus.contributor.surname | Caleo | - |
| scopus.contributor.surname | Mazzoni | - |
| scopus.date.issued | 2022 | * |
| scopus.description.abstracteng | Background: Migraine affects a significant fraction of the world population, yet its etiology is not completely understood. In vitro results highlighted thalamocortical and intra-cortical glutamatergic synaptic gain-of-function associated with a monogenic form of migraine (familial-hemiplegic-migraine-type-1: FHM1). However, how these alterations reverberate on cortical activity remains unclear. As altered responsivity to visual stimuli and abnormal processing of visual sensory information are common hallmarks of migraine, herein we investigated the effects of FHM1-driven synaptic alterations in the visual cortex of awake mice. Methods: We recorded extracellular field potentials from the primary visual cortex (V1) of head-fixed awake FHM1 knock-in (n = 12) and wild type (n = 12) mice in response to square-wave gratings with different visual contrasts. Additionally, we reproduced in silico the obtained experimental results with a novel spiking neurons network model of mouse V1, by implementing in the model both the synaptic alterations characterizing the FHM1 genetic mouse model adopted. Results: FHM1 mice displayed similar amplitude but slower temporal evolution of visual evoked potentials. Visual contrast stimuli induced a lower increase of multi-unit activity in FHM1 mice, while the amount of information content about contrast level remained, however, similar to WT. Spectral analysis of the local field potentials revealed an increase in the β/low γ range of WT mice following the abrupt reversal of contrast gratings. Such frequency range transitioned to the high γ range in FHM1 mice. Despite this change in the encoding channel, these oscillations preserved the amount of information conveyed about visual contrast. The computational model showed how these network effects may arise from a combination of changes in thalamocortical and intra-cortical synaptic transmission, with the former inducing a lower cortical activity and the latter inducing the higher frequencies ɣ oscillations. Conclusions: Contrast-driven ɣ modulation in V1 activity occurs at a much higher frequency in FHM1. This is likely to play a role in the altered processing of visual information. Computational studies suggest that this shift is specifically due to enhanced cortical excitatory transmission. Our network model can help to shed light on the relationship between cellular and network levels of migraine neural alterations. Graphical Abstract: [Figure not available: see fulltext.]. | * |
| scopus.description.allpeopleoriginal | Meneghetti N.; Cerri C.; Vannini E.; Tantillo E.; Tottene A.; Pietrobon D.; Caleo M.; Mazzoni A. | * |
| scopus.differences | scopus.subject.keywords | * |
| scopus.differences | scopus.description.allpeopleoriginal | * |
| scopus.differences | scopus.description.abstracteng | * |
| scopus.differences | scopus.authority.ancejournal | * |
| scopus.document.type | ar | * |
| scopus.document.types | ar | * |
| scopus.funding.funders | 501100003407 - Ministero dell’Istruzione, dell’Università e della Ricerca; | * |
| scopus.funding.ids | 20178L7WRS; 2017ANP5L8; PRIN2017; | * |
| scopus.identifier.doi | 10.1186/s10194-022-01495-9 | * |
| scopus.identifier.eissn | 1129-2377 | * |
| scopus.identifier.pmid | 36175826 | * |
| scopus.identifier.pui | 2019356642 | * |
| scopus.identifier.scopus | 2-s2.0-85138903577 | * |
| scopus.journal.sourceid | 16714 | * |
| scopus.language.iso | eng | * |
| scopus.publisher.name | BioMed Central Ltd | * |
| scopus.relation.article | 125 | * |
| scopus.relation.issue | 1 | * |
| scopus.relation.volume | 23 | * |
| scopus.subject.keywords | Familial-hemiplegic-type1-migraine; Gamma oscillations; Mice; Migraine; Mutual information; Spiking neurons networks; Visual cortex; | * |
| scopus.title | Synaptic alterations in visual cortex reshape contrast-dependent gamma oscillations and inhibition-excitation ratio in a genetic mouse model of migraine | * |
| scopus.titleeng | Synaptic alterations in visual cortex reshape contrast-dependent gamma oscillations and inhibition-excitation ratio in a genetic mouse model of migraine | * |
| Appare nelle tipologie: | 01.01 Articolo in rivista | |
File in questo prodotto:
| File | Dimensione | Formato | |
|---|---|---|---|
|
Meneghetti et al., 2022 J of Headache and Pain.pdf
accesso aperto
Licenza:
Creative commons
Dimensione
8.13 MB
Formato
Adobe PDF
|
8.13 MB | Adobe PDF | Visualizza/Apri |
I documenti in IRIS sono protetti da copyright e tutti i diritti sono riservati, salvo diversa indicazione.
