Critical periods in Drosophila neural network development: Importance to network tuning and therapeutic potential

Critical periods are phases of heightened plasticity that occur during the development of neural networks. Beginning with pioneering work of Hubel and Wiesel, which identified a critical period for the formation of ocular dominance in mammalian visual network connectivity, critical periods have been...

Full description

Saved in:
Bibliographic Details
Published inFrontiers in physiology Vol. 13; p. 1073307
Main Authors Coulson, Bramwell, Hunter, Iain, Doran, Sarah, Parkin, Jill, Landgraf, Matthias, Baines, Richard A
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 02.12.2022
Subjects
Online AccessGet full text

Cover

Loading…
Abstract Critical periods are phases of heightened plasticity that occur during the development of neural networks. Beginning with pioneering work of Hubel and Wiesel, which identified a critical period for the formation of ocular dominance in mammalian visual network connectivity, critical periods have been identified for many circuits, both sensory and motor, and across phyla, suggesting a universal phenomenon. However, a key unanswered question remains why these forms of plasticity are restricted to specific developmental periods rather than being continuously present. The consequence of this temporal restriction is that activity perturbations during critical periods can have lasting and significant functional consequences for mature neural networks. From a developmental perspective, critical period plasticity might enable reproducibly robust network function to emerge from ensembles of cells, whose properties are necessarily variable and fluctuating. Critical periods also offer significant clinical opportunity. Imposed activity perturbation during these periods has shown remarkable beneficial outcomes in a range of animal models of neurological disease including epilepsy. In this review, we spotlight the recent identification of a locomotor critical period in larva and describe how studying this model organism, because of its simplified nervous system and an almost complete wired connectome, offers an attractive prospect of understanding how activity during a critical period impacts a neuronal network.
AbstractList Critical periods are phases of heightened plasticity that occur during the development of neural networks. Beginning with pioneering work of Hubel and Wiesel, which identified a critical period for the formation of ocular dominance in mammalian visual network connectivity, critical periods have been identified for many circuits, both sensory and motor, and across phyla, suggesting a universal phenomenon. However, a key unanswered question remains why these forms of plasticity are restricted to specific developmental periods rather than being continuously present. The consequence of this temporal restriction is that activity perturbations during critical periods can have lasting and significant functional consequences for mature neural networks. From a developmental perspective, critical period plasticity might enable reproducibly robust network function to emerge from ensembles of cells, whose properties are necessarily variable and fluctuating. Critical periods also offer significant clinical opportunity. Imposed activity perturbation during these periods has shown remarkable beneficial outcomes in a range of animal models of neurological disease including epilepsy. In this review, we spotlight the recent identification of a locomotor critical period in Drosophila larva and describe how studying this model organism, because of its simplified nervous system and an almost complete wired connectome, offers an attractive prospect of understanding how activity during a critical period impacts a neuronal network.
Critical periods are phases of heightened plasticity that occur during the development of neural networks. Beginning with pioneering work of Hubel and Wiesel, which identified a critical period for the formation of ocular dominance in mammalian visual network connectivity, critical periods have been identified for many circuits, both sensory and motor, and across phyla, suggesting a universal phenomenon. However, a key unanswered question remains why these forms of plasticity are restricted to specific developmental periods rather than being continuously present. The consequence of this temporal restriction is that activity perturbations during critical periods can have lasting and significant functional consequences for mature neural networks. From a developmental perspective, critical period plasticity might enable reproducibly robust network function to emerge from ensembles of cells, whose properties are necessarily variable and fluctuating. Critical periods also offer significant clinical opportunity. Imposed activity perturbation during these periods has shown remarkable beneficial outcomes in a range of animal models of neurological disease including epilepsy. In this review, we spotlight the recent identification of a locomotor critical period in larva and describe how studying this model organism, because of its simplified nervous system and an almost complete wired connectome, offers an attractive prospect of understanding how activity during a critical period impacts a neuronal network.
Critical periods are phases of heightened plasticity that occur during the development of neural networks. Beginning with pioneering work of Hubel and Wiesel, which identified a critical period for the formation of ocular dominance in mammalian visual network connectivity, critical periods have been identified for many circuits, both sensory and motor, and across phyla, suggesting a universal phenomenon. However, a key unanswered question remains why these forms of plasticity are restricted to specific developmental periods rather than being continuously present. The consequence of this temporal restriction is that activity perturbations during critical periods can have lasting and significant functional consequences for mature neural networks. From a developmental perspective, critical period plasticity might enable reproducibly robust network function to emerge from ensembles of cells, whose properties are necessarily variable and fluctuating. Critical periods also offer significant clinical opportunity. Imposed activity perturbation during these periods has shown remarkable beneficial outcomes in a range of animal models of neurological disease including epilepsy. In this review, we spotlight the recent identification of a locomotor critical period in Drosophila larva and describe how studying this model organism, because of its simplified nervous system and an almost complete wired connectome, offers an attractive prospect of understanding how activity during a critical period impacts a neuronal network.
Author Baines, Richard A
Doran, Sarah
Landgraf, Matthias
Hunter, Iain
Parkin, Jill
Coulson, Bramwell
AuthorAffiliation 1 Division of Neuroscience , School of Biological Sciences , Faculty of Biology , Medicine and Health , University of Manchester , Manchester Academic Health Science Centre , Manchester , United Kingdom
2 Department of Zoology , University of Cambridge , Cambridge , United Kingdom
AuthorAffiliation_xml – name: 1 Division of Neuroscience , School of Biological Sciences , Faculty of Biology , Medicine and Health , University of Manchester , Manchester Academic Health Science Centre , Manchester , United Kingdom
– name: 2 Department of Zoology , University of Cambridge , Cambridge , United Kingdom
Author_xml – sequence: 1
  givenname: Bramwell
  surname: Coulson
  fullname: Coulson, Bramwell
  organization: Division of Neuroscience, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, United Kingdom
– sequence: 2
  givenname: Iain
  surname: Hunter
  fullname: Hunter, Iain
  organization: Division of Neuroscience, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, United Kingdom
– sequence: 3
  givenname: Sarah
  surname: Doran
  fullname: Doran, Sarah
  organization: Division of Neuroscience, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, United Kingdom
– sequence: 4
  givenname: Jill
  surname: Parkin
  fullname: Parkin, Jill
  organization: Division of Neuroscience, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, United Kingdom
– sequence: 5
  givenname: Matthias
  surname: Landgraf
  fullname: Landgraf, Matthias
  organization: Department of Zoology, University of Cambridge, Cambridge, United Kingdom
– sequence: 6
  givenname: Richard A
  surname: Baines
  fullname: Baines, Richard A
  organization: Division of Neuroscience, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, United Kingdom
BackLink https://www.ncbi.nlm.nih.gov/pubmed/36531164$$D View this record in MEDLINE/PubMed
BookMark eNpVkU1v3CAQhlGVKEmT_IEeKo697IYvG7uHStX2a6VIvbRSbwjDeJfUBgdwovz7stntKuECmpn3mRnet-jEBw8IvaNkyXnT3vTT9iktGWFsSYnknMg36ILWtVgQwf6cvHifo-uU7kg5gjBC6Bk653XFKa3FBbpfRZed0QOeILpgE3Yef4khhWnrBo09zLEkPeTHEP9iCw8whGkEnz_i9TiFmLU3gHM4luTZO7_B2luctxD1BHNpgKeQi8jp4Qqd9npIcH24L9Hvb19_rX4sbn9-X68-3y6MqJu8qBvak8ZozjspNbe94LSXXDdNbaQoYdsbYRpGKmq1JWUhkLRtRStETziX_BKt91wb9J2aoht1fFJBO_UcCHGjdCyTDaBAGga85qyxosi7llV9p2nVtbbStCOF9WnPmuZuBGvKJuVXXkFfZ7zbqk14UK2spGhZAXw4AGK4nyFlNbpkYBi0hzAnxWRVNaQm1W5uti81xYUUoT-2oUTtrFfP1qud9epgfRG9fzngUfLfaP4PRiav2A
CitedBy_id crossref_primary_10_37349_en_2024_00034
crossref_primary_10_7554_eLife_91599
crossref_primary_10_1038_s41598_024_59942_3
crossref_primary_10_7554_eLife_91599_3
Cites_doi 10.1017/S0952523818000020
10.1126/science.abf5273
10.1098/rstb.1977.0050
10.1038/s41598-021-99868-8
10.1038/nn.3933
10.1111/j.1460-9568.2010.07261.x
10.1016/j.neuron.2006.08.028
10.1098/rspb.2021.1025
10.1074/jbc.M111.270967
10.1016/j.neuron.2004.08.019
10.1016/j.cub.2021.10.005
10.1038/s41586-021-03441-2
10.1523/JNEUROSCI.18-12-04673.1998
10.1534/genetics.116.199083
10.1016/j.neuron.2016.06.031
10.1126/science.1091032
10.7554/eLife.13253
10.1111/j.1528-1167.2007.01458.x
10.1038/nature14297
10.1113/JP275814
10.1523/JNEUROSCI.1787-15.2016
10.1038/35004582
10.1152/jn.00616.2016
10.1523/JNEUROSCI.2223-18.2019
10.1016/S0070-2153(05)69008-4
10.1038/416174a
10.1523/JNEUROSCI.0346-11.2011
10.1016/j.cub.2011.12.002
10.1523/JNEUROSCI.2463-21.2022
10.3389/fncir.2022.875873
10.1523/JNEUROSCI.17-24-09642.1997
10.7554/eLife.51781
10.1038/s41467-019-10695-y
10.1242/dev.026773
10.1126/scitranslmed.aao0498
10.1111/j.1460-9568.2006.05273.x
10.1371/journal.pbio.0060260
10.3389/fncel.2018.00253
10.1038/nm.4225
10.3389/fnsys.2013.00102
10.1016/j.celrep.2021.110145
10.1126/science.282.5393.1504
10.1016/j.ejpn.2016.07.007
10.1371/journal.pbio.0000041
10.1016/j.cub.2021.08.022
10.1016/j.conb.2016.09.014
10.1089/ars.2009.2721
10.1016/j.cub.2015.09.040
10.1046/j.1471-4159.2003.01554.x
10.2174/157340612799278577
10.1016/B978-0-444-63327-9.00001-1
10.3390/ijms22052434
10.1371/journal.pone.0062199
10.1038/srep05799
10.1016/j.biopsych.2016.05.011
10.1038/nm.3987
10.1002/neu.480220309
10.1016/j.seizure.2014.09.018
10.1113/jphysiol.1970.sp009022
10.1016/j.cell.2019.07.023
10.1152/jn.00808.2010
10.1016/j.neuron.2014.06.026
10.1016/j.cub.2017.06.056
10.1006/dbio.2000.9983
10.1016/j.tins.2012.03.005
10.1016/j.conb.2008.05.009
ContentType Journal Article
Copyright Copyright © 2022 Coulson, Hunter, Doran, Parkin, Landgraf and Baines.
Copyright © 2022 Coulson, Hunter, Doran, Parkin, Landgraf and Baines. 2022 Coulson, Hunter, Doran, Parkin, Landgraf and Baines
Copyright_xml – notice: Copyright © 2022 Coulson, Hunter, Doran, Parkin, Landgraf and Baines.
– notice: Copyright © 2022 Coulson, Hunter, Doran, Parkin, Landgraf and Baines. 2022 Coulson, Hunter, Doran, Parkin, Landgraf and Baines
DBID NPM
AAYXX
CITATION
7X8
5PM
DOA
DOI 10.3389/fphys.2022.1073307
DatabaseName PubMed
CrossRef
MEDLINE - Academic
PubMed Central (Full Participant titles)
Directory of Open Access Journals
DatabaseTitle PubMed
CrossRef
MEDLINE - Academic
DatabaseTitleList
PubMed

CrossRef
Database_xml – sequence: 1
  dbid: DOA
  name: Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
DocumentTitleAlternate Coulson et al
EISSN 1664-042X
EndPage 1073307
ExternalDocumentID oai_doaj_org_article_e7c2e36328d444fb925fba15b9d5a1b0
10_3389_fphys_2022_1073307
36531164
Genre Journal Article
Review
GrantInformation_xml – fundername: ;
GroupedDBID 53G
5VS
9T4
AAFWJ
AAKDD
ACGFO
ACGFS
ACXDI
ADBBV
ADRAZ
AENEX
AFPKN
ALMA_UNASSIGNED_HOLDINGS
AOIJS
BCNDV
DIK
EMOBN
F5P
GROUPED_DOAJ
GX1
HYE
IAO
IEA
IHR
IHW
IPNFZ
ISR
KQ8
M48
M~E
NPM
O5R
O5S
OK1
PGMZT
RIG
RNS
RPM
AAYXX
CITATION
7X8
5PM
ID FETCH-LOGICAL-c468t-681f08ca33b77a3df431f73a886c74a33dfc4c82051dad0653e71994944f03373
IEDL.DBID RPM
ISSN 1664-042X
IngestDate Tue Oct 22 15:15:31 EDT 2024
Tue Sep 17 21:33:10 EDT 2024
Thu Oct 24 23:55:10 EDT 2024
Thu Nov 21 22:31:56 EST 2024
Sat Sep 28 08:18:01 EDT 2024
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Keywords neuron
homeostasis
development
critical period
Drosophila
network
Language English
License Copyright © 2022 Coulson, Hunter, Doran, Parkin, Landgraf and Baines.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c468t-681f08ca33b77a3df431f73a886c74a33dfc4c82051dad0653e71994944f03373
Notes ObjectType-Article-2
SourceType-Scholarly Journals-1
ObjectType-Feature-3
content type line 23
ObjectType-Review-1
This article was submitted to Invertebrate Physiology, a section of the journal Frontiers in Physiology
Milena Damulewicz, Jagiellonian University, Kraków, Poland
Edited by: Jean-René Martin, UMR9197 Institut des Neurosciences Paris Saclay (Neuro-PSI), France
These authors have contributed equally to this work
Reviewed by: Tihana Jovanic, UMR9197 Institut des Neurosciences Paris Saclay (Neuro-PSI), France
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9757492/
PMID 36531164
PQID 2755806057
PQPubID 23479
PageCount 1
ParticipantIDs doaj_primary_oai_doaj_org_article_e7c2e36328d444fb925fba15b9d5a1b0
pubmedcentral_primary_oai_pubmedcentral_nih_gov_9757492
proquest_miscellaneous_2755806057
crossref_primary_10_3389_fphys_2022_1073307
pubmed_primary_36531164
PublicationCentury 2000
PublicationDate 2022-12-02
PublicationDateYYYYMMDD 2022-12-02
PublicationDate_xml – month: 12
  year: 2022
  text: 2022-12-02
  day: 02
PublicationDecade 2020
PublicationPlace Switzerland
PublicationPlace_xml – name: Switzerland
PublicationTitle Frontiers in physiology
PublicationTitleAlternate Front Physiol
PublicationYear 2022
Publisher Frontiers Media S.A
Publisher_xml – name: Frontiers Media S.A
References Marley (B46) 2011; 106
Marley (B47) 2014; 4
Wong-Riley (B62) 2021; 288
Gibel-Russo (B22) 2022; 16
Sink (B56) 1991; 22
Crisp (B11) 2011; 31
Crisp (B10) 2008; 135
Cunliffe (B12) 2015; 24
Hensch (B28) 2018; 35
Blumenfeld (B6) 2008; 49
Calabrese (B7) 2009; 11
Fushiki (B15) 2013; 8
Asiminas (B2) 2019; 11
Giachello (B21) 2022; 42
Horne (B30) 2017; 205
Kiral (B36) 2021; 37
Kuppers (B38) 2003; 84
Larsson (B41) 2004; 43
Golovin (B23) 2016; 116
Zeng (B64) 2021; 31
Avitan (B3) 2017; 27
Hoang (B29) 2001; 229
Marguet (B44) 2015; 21
Baroncelli (B5) 2016; 36
Gervain (B17) 2013; 7
Fagiolini (B13) 2004; 303
Zwart (B66) 2016; 91
Ismail (B34) 2017; 21
Kohsaka (B37) 2019; 10
Fagiolini (B14) 2000; 404
Jin (B35) 2011; 286
Hensch (B27) 1998; 282
Golovin (B24) 2019; 39
Hubel (B33) 1970; 206
Giachello (B20) 2021; 11
Mukherjee (B50) 2019; 178
Takesian (B59) 2013; 207
Meredith (B48) 2012; 35
Zarin (B63) 2019; 8
Fushiki (B16) 2016; 5
Ribot (B53) 2021; 373
Landgraf (B40) 2003; 1
Gomez-Diaz (B25) 2018; 12
Luan (B43) 2006; 52
Silingardi (B55) 2010; 31
Carreira-Rosario (B8) 2021; 31
Hubel (B32) 1977; 278
Schwarzkopf (B54) 2007; 25
Warp (B61) 2012; 22
Zhang (B65) 2018; 596
Hrncic (B31) 2012; 8
Noebels (B51) 2015; 18
Suster (B58) 2002; 416
Morishita (B49) 2008; 18
Stork (B57) 2014; 83
Lee (B42) 2017; 81
Giachello (B18) 2015; 25
Giachello (B19) 2017; 43
Marin (B45) 2016; 22
Baines (B4) 1998; 18
Carulli (B9) 2021; 22
Ohyama (B52) 2015; 520
Hensch (B26) 2005; 69
Landgraf (B39) 1997; 17
Tripodi (B60) 2008; 6
Ackerman (B1) 2021; 592
References_xml – volume: 35
  start-page: E024
  year: 2018
  ident: B28
  article-title: Perspective Critical periods in amblyopia-Corrigendum
  publication-title: Vis. Neurosci.
  doi: 10.1017/S0952523818000020
  contributor:
    fullname: Hensch
– volume: 373
  start-page: 77
  year: 2021
  ident: B53
  article-title: Astrocytes close the mouse critical period for visual plasticity
  publication-title: Science
  doi: 10.1126/science.abf5273
  contributor:
    fullname: Ribot
– volume: 278
  start-page: 377
  year: 1977
  ident: B32
  article-title: Plasticity of ocular dominance columns in monkey striate cortex
  publication-title: Philos. Trans. R. Soc. Lond. B Biol. Sci.
  doi: 10.1098/rstb.1977.0050
  contributor:
    fullname: Hubel
– volume: 11
  start-page: 20286
  year: 2021
  ident: B20
  article-title: Nitric oxide mediates activity-dependent change to synaptic excitation during a critical period in Drosophila
  publication-title: Sci. Rep.
  doi: 10.1038/s41598-021-99868-8
  contributor:
    fullname: Giachello
– volume: 18
  start-page: 344
  year: 2015
  ident: B51
  article-title: Pathway-driven discovery of epilepsy genes
  publication-title: Nat. Neurosci.
  doi: 10.1038/nn.3933
  contributor:
    fullname: Noebels
– volume: 31
  start-page: 2185
  year: 2010
  ident: B55
  article-title: Epigenetic treatments of adult rats promote recovery from visual acuity deficits induced by long-term monocular deprivation
  publication-title: Eur. J. Neurosci.
  doi: 10.1111/j.1460-9568.2010.07261.x
  contributor:
    fullname: Silingardi
– volume: 52
  start-page: 425
  year: 2006
  ident: B43
  article-title: Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression
  publication-title: Neuron
  doi: 10.1016/j.neuron.2006.08.028
  contributor:
    fullname: Luan
– volume: 288
  start-page: 20211025
  year: 2021
  ident: B62
  article-title: The critical period: Neurochemical and synaptic mechanisms shared by the visual cortex and the brain stem respiratory system
  publication-title: Proc. Biol. Sci.
  doi: 10.1098/rspb.2021.1025
  contributor:
    fullname: Wong-Riley
– volume: 286
  start-page: 33190
  year: 2011
  ident: B35
  article-title: Nitric oxide inhibits nociceptive transmission by differentially regulating glutamate and glycine release to spinal dorsal horn neurons
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M111.270967
  contributor:
    fullname: Jin
– volume: 43
  start-page: 703
  year: 2004
  ident: B41
  article-title: Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction
  publication-title: Neuron
  doi: 10.1016/j.neuron.2004.08.019
  contributor:
    fullname: Larsson
– volume: 31
  start-page: 5327
  year: 2021
  ident: B64
  article-title: An electrically coupled pioneer circuit enables motor development via proprioceptive feedback in Drosophila embryos
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2021.10.005
  contributor:
    fullname: Zeng
– volume: 592
  start-page: 414
  year: 2021
  ident: B1
  article-title: Astrocytes close a motor circuit critical period
  publication-title: Nature
  doi: 10.1038/s41586-021-03441-2
  contributor:
    fullname: Ackerman
– volume: 18
  start-page: 4673
  year: 1998
  ident: B4
  article-title: Electrophysiological development of central neurons in the Drosophila embryo
  publication-title: J. Neurosci.
  doi: 10.1523/JNEUROSCI.18-12-04673.1998
  contributor:
    fullname: Baines
– volume: 205
  start-page: 1261
  year: 2017
  ident: B30
  article-title: Julius seizure, a Drosophila mutant, defines a neuronal population underlying epileptogenesis
  publication-title: Genetics
  doi: 10.1534/genetics.116.199083
  contributor:
    fullname: Horne
– volume: 91
  start-page: 615
  year: 2016
  ident: B66
  article-title: Selective inhibition mediates the sequential recruitment of motor pools
  publication-title: Neuron
  doi: 10.1016/j.neuron.2016.06.031
  contributor:
    fullname: Zwart
– volume: 303
  start-page: 1681
  year: 2004
  ident: B13
  article-title: Specific GABAA circuits for visual cortical plasticity
  publication-title: Science
  doi: 10.1126/science.1091032
  contributor:
    fullname: Fagiolini
– volume: 5
  start-page: e13253
  year: 2016
  ident: B16
  article-title: A circuit mechanism for the propagation of waves of muscle contraction in Drosophila
  publication-title: Elife
  doi: 10.7554/eLife.13253
  contributor:
    fullname: Fushiki
– volume: 49
  start-page: 400
  year: 2008
  ident: B6
  article-title: Early treatment suppresses the development of spike-wave epilepsy in a rat model
  publication-title: Epilepsia
  doi: 10.1111/j.1528-1167.2007.01458.x
  contributor:
    fullname: Blumenfeld
– volume: 520
  start-page: 633
  year: 2015
  ident: B52
  article-title: A multilevel multimodal circuit enhances action selection in Drosophila
  publication-title: Nature
  doi: 10.1038/nature14297
  contributor:
    fullname: Ohyama
– volume: 596
  start-page: 4511
  year: 2018
  ident: B65
  article-title: Uncovering a critical period of synaptic imbalance during postnatal development of the rat visual cortex: Role of brain-derived neurotrophic factor
  publication-title: J. Physiol.
  doi: 10.1113/JP275814
  contributor:
    fullname: Zhang
– volume: 36
  start-page: 3430
  year: 2016
  ident: B5
  article-title: Experience affects Critical Period plasticity in the visual cortex through an epigenetic regulation of histone post-translational modifications
  publication-title: J. Neurosci.
  doi: 10.1523/JNEUROSCI.1787-15.2016
  contributor:
    fullname: Baroncelli
– volume: 404
  start-page: 183
  year: 2000
  ident: B14
  article-title: Inhibitory threshold for critical-period activation in primary visual cortex
  publication-title: Nature
  doi: 10.1038/35004582
  contributor:
    fullname: Fagiolini
– volume: 116
  start-page: 2730
  year: 2016
  ident: B23
  article-title: Developmental experience-dependent plasticity in the first synapse of the Drosophila olfactory circuit
  publication-title: J. Neurophysiol.
  doi: 10.1152/jn.00616.2016
  contributor:
    fullname: Golovin
– volume: 39
  start-page: 2995
  year: 2019
  ident: B24
  article-title: Activity-dependent remodeling of Drosophila olfactory sensory neuron brain innervation during an early-life Critical Period
  publication-title: J. Neurosci.
  doi: 10.1523/JNEUROSCI.2223-18.2019
  contributor:
    fullname: Golovin
– volume: 69
  start-page: 215
  year: 2005
  ident: B26
  article-title: Critical period mechanisms in developing visual cortex
  publication-title: Curr. Top. Dev. Biol.
  doi: 10.1016/S0070-2153(05)69008-4
  contributor:
    fullname: Hensch
– volume: 416
  start-page: 174
  year: 2002
  ident: B58
  article-title: Embryonic assembly of a central pattern generator without sensory input
  publication-title: Nature
  doi: 10.1038/416174a
  contributor:
    fullname: Suster
– volume: 31
  start-page: 10445
  year: 2011
  ident: B11
  article-title: Endogenous patterns of activity are required for the maturation of a motor network
  publication-title: J. Neurosci.
  doi: 10.1523/JNEUROSCI.0346-11.2011
  contributor:
    fullname: Crisp
– volume: 22
  start-page: 93
  year: 2012
  ident: B61
  article-title: Emergence of patterned activity in the developing zebrafish spinal cord
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2011.12.002
  contributor:
    fullname: Warp
– volume: 42
  start-page: 6724
  year: 2022
  ident: B21
  article-title: Electrophysiological validation of monosynaptic connectivity between premotor interneurons and the aCC motoneuron in the Drosophila larval CNS
  publication-title: J. Neurosci.
  doi: 10.1523/JNEUROSCI.2463-21.2022
  contributor:
    fullname: Giachello
– volume: 16
  start-page: 875873
  year: 2022
  ident: B22
  article-title: Non-cell-autonomous factors implicated in parvalbumin interneuron maturation and critical periods
  publication-title: Front. Neural Circuits
  doi: 10.3389/fncir.2022.875873
  contributor:
    fullname: Gibel-Russo
– volume: 17
  start-page: 9642
  year: 1997
  ident: B39
  article-title: The origin, location, and projections of the embryonic abdominal motorneurons of Drosophila
  publication-title: J. Neurosci.
  doi: 10.1523/JNEUROSCI.17-24-09642.1997
  contributor:
    fullname: Landgraf
– volume: 8
  start-page: e51781
  year: 2019
  ident: B63
  article-title: A multilayer circuit architecture for the generation of distinct locomotor behaviors in Drosophila
  publication-title: Elife
  doi: 10.7554/eLife.51781
  contributor:
    fullname: Zarin
– volume: 10
  start-page: 2654
  year: 2019
  ident: B37
  article-title: Regulation of forward and backward locomotion through intersegmental feedback circuits in Drosophila larvae
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-019-10695-y
  contributor:
    fullname: Kohsaka
– volume: 135
  start-page: 3707
  year: 2008
  ident: B10
  article-title: The development of motor coordination in Drosophila embryos
  publication-title: Development
  doi: 10.1242/dev.026773
  contributor:
    fullname: Crisp
– volume: 11
  start-page: eaao0498
  year: 2019
  ident: B2
  article-title: Sustained correction of associative learning deficits after brief, early treatment in a rat model of Fragile X Syndrome
  publication-title: Sci. Transl. Med.
  doi: 10.1126/scitranslmed.aao0498
  contributor:
    fullname: Asiminas
– volume: 25
  start-page: 270
  year: 2007
  ident: B54
  article-title: Brief daily binocular vision prevents monocular deprivation effects in visual cortex
  publication-title: Eur. J. Neurosci.
  doi: 10.1111/j.1460-9568.2006.05273.x
  contributor:
    fullname: Schwarzkopf
– volume: 6
  start-page: e260
  year: 2008
  ident: B60
  article-title: Structural homeostasis: Compensatory adjustments of dendritic arbor geometry in response to variations of synaptic input
  publication-title: PLoS Biol.
  doi: 10.1371/journal.pbio.0060260
  contributor:
    fullname: Tripodi
– volume: 12
  start-page: 253
  year: 2018
  ident: B25
  article-title: The two main olfactory receptor families in Drosophila, ORs and IRs: A comparative approach
  publication-title: Front. Cell. Neurosci.
  doi: 10.3389/fncel.2018.00253
  contributor:
    fullname: Gomez-Diaz
– volume: 22
  start-page: 1229
  year: 2016
  ident: B45
  article-title: Developmental timing and critical windows for the treatment of psychiatric disorders
  publication-title: Nat. Med.
  doi: 10.1038/nm.4225
  contributor:
    fullname: Marin
– volume: 7
  start-page: 102
  year: 2013
  ident: B17
  article-title: Valproate reopens critical-period learning of absolute pitch
  publication-title: Front. Syst. Neurosci.
  doi: 10.3389/fnsys.2013.00102
  contributor:
    fullname: Gervain
– volume: 37
  start-page: 110145
  year: 2021
  ident: B36
  article-title: Brain connectivity inversely scales with developmental temperature in Drosophila
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2021.110145
  contributor:
    fullname: Kiral
– volume: 282
  start-page: 1504
  year: 1998
  ident: B27
  article-title: Local GABA circuit control of experience-dependent plasticity in developing visual cortex
  publication-title: Science
  doi: 10.1126/science.282.5393.1504
  contributor:
    fullname: Hensch
– volume: 21
  start-page: 23
  year: 2017
  ident: B34
  article-title: Cerebral plasticity: Windows of opportunity in the developing brain
  publication-title: Eur. J. Paediatr. Neurol.
  doi: 10.1016/j.ejpn.2016.07.007
  contributor:
    fullname: Ismail
– volume: 1
  start-page: E41
  year: 2003
  ident: B40
  article-title: Embryonic origins of a motor system: Motor dendrites form a myotopic map in Drosophila
  publication-title: PLoS Biol.
  doi: 10.1371/journal.pbio.0000041
  contributor:
    fullname: Landgraf
– volume: 31
  start-page: 5341
  year: 2021
  ident: B8
  article-title: Mechanosensory input during circuit formation shapes Drosophila motor behavior through patterned spontaneous network activity
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2021.08.022
  contributor:
    fullname: Carreira-Rosario
– volume: 43
  start-page: 1
  year: 2017
  ident: B19
  article-title: Regulation of motoneuron excitability and the setting of homeostatic limits
  publication-title: Curr. Opin. Neurobiol.
  doi: 10.1016/j.conb.2016.09.014
  contributor:
    fullname: Giachello
– volume: 11
  start-page: 2717
  year: 2009
  ident: B7
  article-title: Nitric oxide in cell survival: A janus molecule
  publication-title: Antioxid. Redox Signal.
  doi: 10.1089/ars.2009.2721
  contributor:
    fullname: Calabrese
– volume: 25
  start-page: 2964
  year: 2015
  ident: B18
  article-title: Inappropriate neural activity during a sensitive period in embryogenesis results in persistent seizure-like behavior
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2015.09.040
  contributor:
    fullname: Giachello
– volume: 84
  start-page: 939
  year: 2003
  ident: B38
  article-title: In developing Drosophila neurones the production of gamma-amino butyric acid is tightly regulated downstream of glutamate decarboxylase translation and can be influenced by calcium
  publication-title: J. Neurochem.
  doi: 10.1046/j.1471-4159.2003.01554.x
  contributor:
    fullname: Kuppers
– volume: 8
  start-page: 59
  year: 2012
  ident: B31
  article-title: Inhibition of the neuronal nitric oxide synthase potentiates homocysteine thiolactone-induced seizures in adult rats
  publication-title: Med. Chem.
  doi: 10.2174/157340612799278577
  contributor:
    fullname: Hrncic
– volume: 207
  start-page: 3
  year: 2013
  ident: B59
  article-title: Balancing plasticity/stability across brain development
  publication-title: Prog. Brain Res.
  doi: 10.1016/B978-0-444-63327-9.00001-1
  contributor:
    fullname: Takesian
– volume: 22
  start-page: 2434
  year: 2021
  ident: B9
  article-title: An extracellular perspective on CNS maturation: Perineuronal nets and the control of plasticity
  publication-title: Int. J. Mol. Sci.
  doi: 10.3390/ijms22052434
  contributor:
    fullname: Carulli
– volume: 8
  start-page: e62199
  year: 2013
  ident: B15
  article-title: Role of sensory experience in functional development of Drosophila motor circuits
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0062199
  contributor:
    fullname: Fushiki
– volume: 4
  start-page: 5799
  year: 2014
  ident: B47
  article-title: Cryptochrome-dependent magnetic field effect on seizure response in Drosophila larvae
  publication-title: Sci. Rep.
  doi: 10.1038/srep05799
  contributor:
    fullname: Marley
– volume: 81
  start-page: 838
  year: 2017
  ident: B42
  article-title: Excitation/inhibition imbalance in animal models of autism spectrum disorders
  publication-title: Biol. Psychiatry
  doi: 10.1016/j.biopsych.2016.05.011
  contributor:
    fullname: Lee
– volume: 21
  start-page: 1436
  year: 2015
  ident: B44
  article-title: Treatment during a vulnerable developmental period rescues a genetic epilepsy
  publication-title: Nat. Med.
  doi: 10.1038/nm.3987
  contributor:
    fullname: Marguet
– volume: 22
  start-page: 298
  year: 1991
  ident: B56
  article-title: Location and connectivity of abdominal motoneurons in the embryo and larva of Drosophila melanogaster
  publication-title: J. Neurobiol.
  doi: 10.1002/neu.480220309
  contributor:
    fullname: Sink
– volume: 24
  start-page: 44
  year: 2015
  ident: B12
  article-title: Epilepsy research methods update: Understanding the causes of epileptic seizures and identifying new treatments using non-mammalian model organisms
  publication-title: Seizure
  doi: 10.1016/j.seizure.2014.09.018
  contributor:
    fullname: Cunliffe
– volume: 206
  start-page: 419
  year: 1970
  ident: B33
  article-title: The period of susceptibility to the physiological effects of unilateral eye closure in kittens
  publication-title: J. Physiol.
  doi: 10.1113/jphysiol.1970.sp009022
  contributor:
    fullname: Hubel
– volume: 178
  start-page: 1387
  year: 2019
  ident: B50
  article-title: Long-lasting rescue of network and cognitive dysfunction in a genetic schizophrenia model
  publication-title: Cell
  doi: 10.1016/j.cell.2019.07.023
  contributor:
    fullname: Mukherjee
– volume: 106
  start-page: 18
  year: 2011
  ident: B46
  article-title: Increased persistent Na+ current contributes to seizure in the slamdance bang-sensitive Drosophila mutant
  publication-title: J. Neurophysiol.
  doi: 10.1152/jn.00808.2010
  contributor:
    fullname: Marley
– volume: 83
  start-page: 388
  year: 2014
  ident: B57
  article-title: Neuron-glia interactions through the Heartless FGF receptor signaling pathway mediate morphogenesis of Drosophila astrocytes
  publication-title: Neuron
  doi: 10.1016/j.neuron.2014.06.026
  contributor:
    fullname: Stork
– volume: 27
  start-page: 2407
  year: 2017
  ident: B3
  article-title: Spontaneous activity in the zebrafish tectum reorganizes over development and is influenced by visual experience
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2017.06.056
  contributor:
    fullname: Avitan
– volume: 229
  start-page: 55
  year: 2001
  ident: B29
  article-title: Single-cell analysis of Drosophila larval neuromuscular synapses
  publication-title: Dev. Biol.
  doi: 10.1006/dbio.2000.9983
  contributor:
    fullname: Hoang
– volume: 35
  start-page: 335
  year: 2012
  ident: B48
  article-title: Sensitive time-windows for susceptibility in neurodevelopmental disorders
  publication-title: Trends Neurosci.
  doi: 10.1016/j.tins.2012.03.005
  contributor:
    fullname: Meredith
– volume: 18
  start-page: 101
  year: 2008
  ident: B49
  article-title: Critical period revisited: Impact on vision
  publication-title: Curr. Opin. Neurobiol.
  doi: 10.1016/j.conb.2008.05.009
  contributor:
    fullname: Morishita
SSID ssj0000402001
Score 2.383587
SecondaryResourceType review_article
Snippet Critical periods are phases of heightened plasticity that occur during the development of neural networks. Beginning with pioneering work of Hubel and Wiesel,...
SourceID doaj
pubmedcentral
proquest
crossref
pubmed
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
StartPage 1073307
SubjectTerms critical period
development
Drosophila
homeostasis
network
neuron
Physiology
SummonAdditionalLinks – databaseName: Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1bS8MwFA6yJ19E8TZvRPBNytrc65u3MQV9crC3kjQJDmars_v_nqTb3ETwxdckJel3kuZ86cl3ELrgKnWeWg0LyeiEMc4S7RxLlHDMG8UtdYEoPj2LwZA9jvhoJdVXiAlr5YFb4HpOlsRRQYmyjMHjOeHe6Iyb3HKdmZatp2SFTMVvcKBFadbekgEWlvd8OCkAPkgIEFYJLF6u7URRsP83L_NnsOTK7tPfRltztxFft8PdQRuu2kUfizwFOMgV1_YTjyt8N42ZCcYTjYNWJVRWbaQ3tt_xQVf44S063mBy3NTLJs0sHJNgXVm8cjELv9dNCCrSkz007N-_3A6SeQqFpGRCNYlQmU9VqSk1UmpqPfgLXlKtlCglg2LrS1aCF8Azq23QqXUyqAXnAHVKqaT7qFPVlTtEOCfCWIBdyJIzAbRQe05NDu6ZT0srWRddLuAs3luljAIYRgC_iOAXAfxiDn4X3QTEly2DynUsANsXc9sXf9m-i84X9ipgVYRfHbpy9Qy6khxmIVA16Oigtd-yKwpvmQFL7CK5Ztm1sazXVOPXqLydSy5ZTo7-Y_DHaDMAEkNjyAnqNNOZOwUHpzFncS5_AZJW_J8
  priority: 102
  providerName: Directory of Open Access Journals
– databaseName: Scholars Portal Open Access Journals
  dbid: M48
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1LT9wwELYoXHqpQH0tj8qVeqvSJn4HCSGgRVCJnliJW2THdrvSksCSleDfd8bJLmxFb73ajjz57MnM54xnCPkkTR4i9xYUydlMCCkyG4LIjAoiOiM9D0gUL36qs7H4cSWv1sii3NEA4N2z1A7rSY1n0y_3tw-HoPAHyDjB3n6NeAgAVI8x4KIaCLp-QTYYWEYM8boY3P30ZUaylBf93Zl_PLpin1Ia_-d8z79DKJ_YpNNN8mpwJulRv_pbZC00r8ntonoBxSTGrb-jk4Z-m6V6BZOppZjBEjqbPv6b-seooX16fp2QgI1Au3Y5pJvj4Qm1jadPrmvRm7bDUCM7fUPGp98vT86yobBCVgtlukyZIuamtpw7rS33EbCKmltjVK0FNPtYixp8A1l46zF7bdCYQ7gUIuaca_6WrDdtE94TWjLlvHSl0rUUCsiijZK7Epy2mNdeixH5vICzuunzZ1TAOxD8KoFfIfjVAP6IHCPiy5GY-zo1tLNf1aBKVdA1C1xxZrwAgVzJZHS2ACG8tIXLR-TjYr0q0BX8AWKb0M5hKi1hbwKBg4ne9eu3nIrDWxbAHUdEr6zsiiyrPc3kd8rHXWqpRcm2_4fwO-QlApICZtguWe9m87AHbk_nPqS9_Ad5kgUg
  priority: 102
  providerName: Scholars Portal
Title Critical periods in Drosophila neural network development: Importance to network tuning and therapeutic potential
URI https://www.ncbi.nlm.nih.gov/pubmed/36531164
https://search.proquest.com/docview/2755806057
https://pubmed.ncbi.nlm.nih.gov/PMC9757492
https://doaj.org/article/e7c2e36328d444fb925fba15b9d5a1b0
Volume 13
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3PT9swFLagp10mJhgrbMhI3FBoEv_MboMNAVKnHUDiFvnnqNQ6XZf-_3t2kq6dOO2Sg-PIznvP8fucz58RumAyd55YBQNJq4xSRjPlHM0kd9RrySxxEShOv_O7J_rwzJ73EBv2wiTSvtGzqzBfXIXZS-JWLhdmMvDEJj-mN5VgglblZB_tw_S7BdHT5zciorzoNsgAAKsmPi4SABQsS8CqAgC82JmEklb_awnmvzzJrYnn9gC97TNG_KXr2Tu058Ih-jUcUYCjUnFjf-NZwF9X6VCC2VzhKFMJN0NH8sb2LzXoM75fpJwbvI3bZlOlXccVEqyCxVt7svCyaSOfSM2P0NPtt8ebu6w_PSEzlMs247LwuTSKEC2EItZDquAFUVJyIygUW2-ogQSAFVbZKFHrRBQKrij1OSGCvEej0AT3AeGq5NoyXXFhGOWACJVnRFeQmfncWEHH6HIwZ73sRDJqABfR-HUyfh2NX_fGH6PraPFNzShwnQqa1c-6d3PthCkd4aSUlkKHdFUyr1UBnbBMFTofo_PBXzUMiPiXQwXXrKEpwSAAAaVBQ8ed_zZNEXjLAgDiGIkdz-70ZfcOxGAS3e5j7uS_nzxFb6IVEhWm_IhG7WrtPkFC0-qztBAA1ymVZymY_wAMGPzm
link.rule.ids 230,314,727,780,784,864,885,2102,24318,27924,27925,53791,53793
linkProvider National Library of Medicine
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lj9MwELaW5QAXBOJVnkbihrJNYju2ucHCqgvbFYddaW-Wn1CpdUpJ_z9jJykt4sTVduTJjB3P53z-jNBbJkofiNMwkYwuKGW00N7TQjSeBiOYIz4BxfllM7umX27YzRFi41mYTNq3ZnESl6uTuPiRuZXrlZ2OPLHpt_mp5IxTWU9voduMcFntgfT8AU6YqKz6IzIAweQ0pG0CAIN1DWiVA4TnB8tQVuv_V4r5N1Nyb-k5u4_uDTkj_tDb9gAd-fgQ_RwvKcBJq7h1v_Ai4k-bfC3BYqlxEqqEytjTvLH7Qw56j89XOeuGeOOu3TXptmmPBOvo8N6pLLxuu8Qo0stH6Prs89XprBjuTygsbURXNKIKpbCaEMO5Ji5AshA40UI0llModsFSCykAq5x2SaTW8yQVLCkNJSGcPEbHsY3-KcKyboxjRjbcMtoAJtSBESMhNwuldZxO0LvRnWrdy2QogBfJ-So7XyXnq8H5E_QxeXzXMklc54J2810NgVae29qThtTCUTDIyJoFoyswwjFdmXKC3ozxUjAl0n8OHX27ha44gyEIOA06etLHb9cVgbesACJOED-I7IEthzUwCrPs9jDqnv33k6_RndnV_EJdnF9-fY7uJo9kYkz9Ah13m61_CelNZ17lwfwbkhn-bA
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1LbxMxELagSIgLAvEK5WEkbmi7Dz-XG7RELdCqByr1ZvlZIiXekG7-P2PvJiSIE1fbK8_OjNfzeT_PIPSeycoH4jQsJKMLShkttPe0kNzTYCRzxCegeH7BT6_o12t2vVPqK5P2rZkdxfniKM5-Zm7lcmHLDU-svDw_bgUTtG3KpQvlXXSPEXCyHaCeP8IJF1X1cE0GYFhbhnRUAICwaQCxCoDxYm8ryhn7_xVm_s2W3Nl-po_QwzFuxJ8G-R6jOz4-Qb82hQpwylfcuVs8i_hklUsTzOYap2SV0BkHqjd2fwhCH_HZIkfeYHPcd9sh_Tqdk2AdHd65mYWXXZ9YRXr-FF1Nv_w4Pi3GGgqFpVz2BZd1qKTVhBghNHEBAoYgiJaSW0Gh2QVLLYQBrHbapUS1XqR0wS2loSJEkGfoIHbRv0C4bbhxzLRcWEY54EIdGDEtxGehsk7QCfqwUadaDqkyFECMpHyVla-S8tWo_An6nDS-HZnSXOeGbnWjRmMrL2zjCSeNdBQEMm3DgtE1COGYrk01Qe829lKwLNK_Dh19t4apBAM3BKwGEz0f7LedisBb1gATJ0jsWXZPlv0e8MScenv0vJf__eRbdP_yZKq-n118O0QPkkIyN6Z5hQ761dq_hginN2-yL_8GJhv_fw
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Critical+periods+in+Drosophila+neural+network+development%3A+Importance+to+network+tuning+and+therapeutic+potential&rft.jtitle=Frontiers+in+physiology&rft.au=Bramwell+Coulson&rft.au=Iain+Hunter&rft.au=Sarah+Doran&rft.au=Jill+Parkin&rft.date=2022-12-02&rft.pub=Frontiers+Media+S.A&rft.eissn=1664-042X&rft.volume=13&rft_id=info:doi/10.3389%2Ffphys.2022.1073307&rft.externalDBID=DOA&rft.externalDocID=oai_doaj_org_article_e7c2e36328d444fb925fba15b9d5a1b0
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1664-042X&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1664-042X&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1664-042X&client=summon