Synaptic Plasticity on Motoneurons After Axotomy: A Necessary Change in Paradigm.
Ia afferent synapses
astrocytes
axotomy
microglia
motoneuron
regeneration
sensorimotor integration
synaptic plasticity
Journal
Frontiers in molecular neuroscience
ISSN: 1662-5099
Titre abrégé: Front Mol Neurosci
Pays: Switzerland
ID NLM: 101477914
Informations de publication
Date de publication:
2020
2020
Historique:
received:
03
02
2020
accepted:
08
04
2020
entrez:
20
5
2020
pubmed:
20
5
2020
medline:
20
5
2020
Statut:
epublish
Résumé
Motoneurons axotomized by peripheral nerve injuries experience profound changes in their synaptic inputs that are associated with a neuroinflammatory response that includes local microglia and astrocytes. This reaction is conserved across different types of motoneurons, injuries, and species, but also displays many unique features in each particular case. These reactions have been amply studied, but there is still a lack of knowledge on their functional significance and mechanisms. In this review article, we compiled data from many different fields to generate a comprehensive conceptual framework to best interpret past data and spawn new hypotheses and research. We propose that synaptic plasticity around axotomized motoneurons should be divided into two distinct processes. First, a rapid cell-autonomous, microglia-independent shedding of synapses from motoneuron cell bodies and proximal dendrites that is reversible after muscle reinnervation. Second, a slower mechanism that is microglia-dependent and permanently alters spinal cord circuitry by fully eliminating from the ventral horn the axon collaterals of peripherally injured and regenerating sensory Ia afferent proprioceptors. This removes this input from cell bodies and throughout the dendritic tree of axotomized motoneurons as well as from many other spinal neurons, thus reconfiguring ventral horn motor circuitries to function after regeneration without direct sensory feedback from muscle. This process is modulated by injury severity, suggesting a correlation with poor regeneration specificity due to sensory and motor axons targeting errors in the periphery that likely render Ia afferent connectivity in the ventral horn nonadaptive. In contrast, reversible synaptic changes on the cell bodies occur only while motoneurons are regenerating. This cell-autonomous process displays unique features according to motoneuron type and modulation by local microglia and astrocytes and generally results in a transient reduction of fast synaptic activity that is probably replaced by embryonic-like slow GABA depolarizations, proposed to relate to regenerative mechanisms.
Identifiants
pubmed: 32425754
doi: 10.3389/fnmol.2020.00068
pmc: PMC7203341
doi:
Types de publication
Journal Article
Review
Langues
eng
Pagination
68Subventions
Organisme : NINDS NIH HHS
ID : R21 NS114839
Pays : United States
Organisme : NINDS NIH HHS
ID : F32 NS112556
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS111969
Pays : United States
Organisme : NINDS NIH HHS
ID : R56 NS099092
Pays : United States
Organisme : NINDS NIH HHS
ID : F31 NS095528
Pays : United States
Informations de copyright
Copyright © 2020 Alvarez, Rotterman, Akhter, Lane, English and Cope.
Références
PLoS One. 2013;8(3):e59647
pubmed: 23527240
J Cell Biol. 1997 Oct 20;139(2):397-415
pubmed: 9334344
Neuroreport. 2010 Aug 4;21(11):782-5
pubmed: 20577133
J Comp Neurol. 2010 Dec 1;518(23):4675-701
pubmed: 20963823
J Neurochem. 2016 Jan;136 Suppl 1:10-7
pubmed: 25693054
Cell Rep. 2019 Dec 3;29(10):3087-3100.e7
pubmed: 31801075
J Physiol. 1973 Nov;234(3):665-88
pubmed: 4764434
Brain Res. 1974 Jun 20;73(2):338-42
pubmed: 4364627
J Physiol. 2002 May 15;541(Pt 1):123-37
pubmed: 12015425
Proc Natl Acad Sci U S A. 2004 Dec 21;101(51):17843-8
pubmed: 15591351
Nature. 1971 Sep 24;233(5317):273-5
pubmed: 4938371
Hum Mol Genet. 2004 Feb 1;13(3):295-302
pubmed: 14662657
Exp Neurol. 2014 Apr;254:109-20
pubmed: 24468477
Exp Brain Res. 1974;20(3):307-10
pubmed: 4139036
J Neurosci Res. 1993 Jul 1;35(4):373-81
pubmed: 8360946
J Exp Biol. 2011 Mar 15;214(Pt 6):1007-16
pubmed: 21346129
Lancet. 1947 May 24;1(6456):704-7
pubmed: 20241152
J Physiol. 1958 Aug 29;143(1):11-40
pubmed: 13576457
J Peripher Nerv Syst. 2000 Jun;5(2):75-81
pubmed: 10905466
Cells Tissues Organs. 2011;193(5):298-309
pubmed: 21411964
J Physiol. 1975 Feb;245(1):91-135
pubmed: 165288
J Neurosci. 2007 Nov 21;27(47):12851-9
pubmed: 18032657
J Neurophysiol. 1995 Jul;74(1):113-21
pubmed: 7472315
J Neurosci. 1998 Feb 1;18(3):1142-7
pubmed: 9437034
Front Biosci (Schol Ed). 2011 Jun 01;3:857-68
pubmed: 21622237
Eur J Neurosci. 2005 Feb;21(3):669-78
pubmed: 15733085
J Neurosci. 2014 Nov 19;34(47):15779-92
pubmed: 25411505
Nat Commun. 2014 Jul 22;5:4486
pubmed: 25047355
J Comp Neurol. 1993 Sep 22;335(4):563-75
pubmed: 7693774
J Physiol. 1978 Jan;274:111-27
pubmed: 624988
Exp Brain Res. 1975;22(2):175-83
pubmed: 1126413
Neuropharmacology. 2015 Sep;96(Pt A):113-23
pubmed: 25445484
Exp Brain Res. 1976 Aug 27;26(1):73-87
pubmed: 964328
Brain Res. 1985 Sep;357(1):27-46
pubmed: 2412661
Muscle Nerve. 1997 Jan;20(1):29-37
pubmed: 8995580
Exp Brain Res. 1998 Jan;118(1):1-13
pubmed: 9547066
Hand Clin. 2016 May;32(2):103-17
pubmed: 27094884
J Cell Biol. 2017 Sep 4;216(9):2979-2989
pubmed: 28716844
Nat Neurosci. 2006 Oct;9(10):1294-301
pubmed: 16980967
J Chem Neuroanat. 2018 Mar;88:13-21
pubmed: 29113945
Int J Mol Sci. 2016 Dec 01;17(12):
pubmed: 27916956
Brain Res. 2016 Oct 15;1649(Pt A):90-101
pubmed: 27545667
Eur J Neurosci. 1995 Oct 1;7(10):2101-10
pubmed: 8542067
J Physiol. 1986 Jun;375:587-609
pubmed: 2948009
Exp Neurol. 1977 Dec;57(3):1026-41
pubmed: 923669
Trends Neurosci. 1998 Feb;21(2):81-8
pubmed: 9498304
Eur J Neurosci. 2016 Feb;43(3):336-50
pubmed: 26121368
J Physiol. 1989 Jan;408:345-72
pubmed: 2528632
J Peripher Nerv Syst. 2003 Dec;8(4):209-26
pubmed: 14641646
Dev Neurosci. 1997;19(3):247-54
pubmed: 9208208
J Physiol. 1983 Oct;343:135-45
pubmed: 6644615
Exp Neurol. 1998 Apr;150(2):282-95
pubmed: 9527898
J Comp Neurol. 1996 Aug 26;372(3):465-85
pubmed: 8873872
J Physiol. 1976 Feb;255(1):67-79
pubmed: 130483
Exp Neurol. 2016 Jan;275 Pt 1:25-37
pubmed: 26431741
Brain Res Rev. 2008 Jan;57(1):77-85
pubmed: 17920131
Exp Brain Res. 1986;61(2):272-9
pubmed: 3005014
Eur J Neurosci. 2001 Feb;13(3):521-8
pubmed: 11168559
J Neurotrauma. 2006 Dec;23(12):1857-73
pubmed: 17184194
Z Zellforsch Mikrosk Anat. 1968;85(2):145-57
pubmed: 5706753
Cells. 2019 May 21;8(5):
pubmed: 31117227
J Cell Sci. 2005 Mar 15;118(Pt 6):1267-77
pubmed: 15741237
Neuroscience. 1984 Nov;13(3):855-62
pubmed: 6098859
Physiol Rev. 1984 Jan;64(1):260-324
pubmed: 6320234
Neurosci Lett. 2009 Jan 2;449(1):28-33
pubmed: 18977278
Eur Arch Otorhinolaryngol. 1996;253(8):475-80
pubmed: 8950547
J Neurosci. 2013 Oct 9;33(41):16236-48
pubmed: 24107955
Exp Neurol. 2012 Sep;237(1):8-17
pubmed: 22721768
J Neurosci. 2005 Feb 9;25(6):1448-58
pubmed: 15703399
Brain Res Rev. 2007 Aug;55(1):89-96
pubmed: 17509690
Neuroscience. 1983 Sep;10(1):23-9
pubmed: 6646422
J Neurosci. 2011 Apr 13;31(15):5865-75
pubmed: 21490228
J Comp Neurol. 1973 Oct 1;151(3):255-80
pubmed: 4744474
Exp Neurol. 1975 Nov;49(2):406-17
pubmed: 1193196
Brain Res Bull. 2020 Feb;155:67-80
pubmed: 31756421
J Anat. 1999 Jan;194 ( Pt 1):1-14
pubmed: 10227662
J Comp Neurol. 1993 Apr 15;330(3):439-54
pubmed: 8468413
J Neurosci. 2010 Jun 16;30(24):8308-19
pubmed: 20554882
J Neurophysiol. 1989 Aug;62(2):325-33
pubmed: 2549206
Brain Res. 1975 Sep 23;95(2-3):265-79
pubmed: 1156875
J Physiol. 1981 Dec;321:65-96
pubmed: 6279826
J Neurocytol. 1973 Sep;2(3):315-28
pubmed: 9224494
J Neurosci. 2014 Mar 5;34(10):3475-92
pubmed: 24599449
Neuroscience. 1994 Jan;58(1):59-79
pubmed: 7512703
Brain Res Mol Brain Res. 2005 Apr 27;135(1-2):260-75
pubmed: 15857688
Neurochem Res. 2018 Feb;43(2):324-339
pubmed: 29164431
J Physiol. 1979 Jun;291:191-205
pubmed: 225473
J Neurosci. 2019 May 1;39(18):3412-3433
pubmed: 30833511
J Physiol. 1980 Dec;309:185-98
pubmed: 7252863
Brain Res. 1986 May 14;373(1-2):15-21
pubmed: 3719303
Neuroscience. 1997 Nov;81(2):457-78
pubmed: 9300434
Neuron. 2013 Jan 9;77(1):10-8
pubmed: 23312512
J Comp Neurol. 1992 Apr 8;318(2):188-208
pubmed: 1583159
Exp Neurol. 2019 Sep;319:112817
pubmed: 30176220
Neuroscience. 2003;117(1):139-46
pubmed: 12605900
Neurosci Lett. 1984 Sep 28;51(1):67-72
pubmed: 6514233
J Physiol. 1975 Nov;252(2):429-63
pubmed: 1206535
Exp Neurol. 2006 Aug;200(2):468-79
pubmed: 16696973
Exp Brain Res. 1977 Nov 24;30(2-3):313-21
pubmed: 202476
J Neurophysiol. 2011 Nov;106(5):2450-70
pubmed: 21832035
Prog Neurobiol. 2007 Jul;82(4):163-201
pubmed: 17643733
Annu Rev Neurosci. 2012;35:369-89
pubmed: 22715882
Exp Brain Res. 1999 Mar;125(1):19-27
pubmed: 10100972
J Comp Neurol. 1985 Mar 22;233(4):421-8
pubmed: 3980778
J Anat. 2015 Aug;227(2):221-30
pubmed: 26047324
Neuron. 2009 Oct 15;64(1):40-5
pubmed: 19840547
Acta Neurochir Suppl. 1996;66:103-6
pubmed: 8780806
Exp Neurol. 1993 Mar;120(1):123-31
pubmed: 8477825
J Neurophysiol. 1994 Feb;71(2):817-20
pubmed: 8176445
Ann N Y Acad Sci. 2010 Jun;1198:231-41
pubmed: 20536938
Exp Brain Res. 1993;96(1):19-27
pubmed: 8243580
Biol Open. 2018 Aug 6;7(8):
pubmed: 30082274
J Physiol. 1981;313:121-40
pubmed: 7277213
Philos Trans R Soc Lond B Biol Sci. 1974 Sep 12;269(896):95-108
pubmed: 4154464
J Comp Neurol. 1991 May 8;307(2):259-80
pubmed: 1856325
J Cereb Blood Flow Metab. 2001 Jan;21(1):69-76
pubmed: 11149670
J Neurophysiol. 1993 Nov;70(5):1787-96
pubmed: 8294953
Neurosci Res. 1988 Apr;5(4):338-46
pubmed: 2836765
J Neurosci. 2009 Jan 14;29(2):575-87
pubmed: 19144857
J Comp Neurol. 1981 Nov 1;202(3):357-64
pubmed: 7298903
J Comp Neurol. 2004 May 3;472(3):257-80
pubmed: 15065123
J Comp Neurol. 1999 Nov 29;414(4):454-68
pubmed: 10531539
J Physiol. 1983 Oct;343:117-33
pubmed: 6644614
J Neuroinflammation. 2012 Oct 23;9:240
pubmed: 23092428
eNeuro. 2019 Oct 16;6(5):
pubmed: 31541001
Neuron. 1998 Sep;21(3):505-20
pubmed: 9768838
J Comp Neurol. 1992 Apr 22;318(4):439-51
pubmed: 1578011
Exp Brain Res. 1990;79(1):65-74
pubmed: 2311704
J Neurophysiol. 1967 Sep;30(5):1169-93
pubmed: 4293410
Acta Neuropathol. 1983;61(3-4):161-8
pubmed: 6196933
Glia. 1990;3(5):342-9
pubmed: 2146223
J Comp Neurol. 2001 Jul 23;436(2):182-201
pubmed: 11438923
Exp Neurol. 1986 Sep;93(3):662-7
pubmed: 3743712
Neuroscience. 2014 Oct 24;279:187-219
pubmed: 25168736
J Neurophysiol. 2011 Nov;106(5):2471-85
pubmed: 21832030
Curr Opin Neurobiol. 2007 Feb;17(1):43-52
pubmed: 17275284
Int Rev Neurobiol. 1971;14:49-124
pubmed: 4948651
J Neurocytol. 1986 Jun;15(3):363-73
pubmed: 3746351
Acta Neuropathol. 1993;86(2):179-81
pubmed: 8213072
J Neurophysiol. 1986 May;55(5):947-65
pubmed: 3711974
J Neurosci Res. 2002 Jun 15;68(6):691-702
pubmed: 12111830
Exp Neurol. 2006 Oct;201(2):461-9
pubmed: 16777094
J Comp Neurol. 2000 Sep 11;425(1):10-23
pubmed: 10940938
Brain Res. 1989 Jun 12;489(2):400-5
pubmed: 2743165
J Neurosci. 2010 Jan 20;30(3):973-84
pubmed: 20089906
Neuroscience. 1988 Jan;24(1):143-60
pubmed: 3368045
ASN Neuro. 2010 Oct 14;2(5):e00047
pubmed: 20967131
Exp Brain Res. 2007 Aug;181(2):377-93
pubmed: 17406860
J Comp Neurol. 1998 Sep 7;398(4):459-72
pubmed: 9717703
Neuroscience. 2005;136(1):147-60
pubmed: 16182453
J Neurobiol. 1998 Oct;37(1):131-45
pubmed: 9777737
Acta Physiol Scand Suppl. 1969;332:85-115
pubmed: 5386537
J Neuroimmunol. 1998 Nov 2;91(1-2):180-9
pubmed: 9846834
Neuron. 2011 Feb 10;69(3):453-67
pubmed: 21315257
J Neurosci. 2006 Dec 20;26(51):13297-310
pubmed: 17182780
Mol Immunol. 2009 Dec;47(2-3):302-9
pubmed: 19833392
Prog Neurobiol. 2012 Jul;98(1):16-37
pubmed: 22609046
Prog Brain Res. 2000;127:501-14
pubmed: 11142045
Neuroscience. 2005;134(3):889-99
pubmed: 15994018
J Physiol. 2011 Oct 15;589(Pt 20):4935-47
pubmed: 21788349
Neurosci Lett. 1994 Sep 26;179(1-2):157-61
pubmed: 7531312
Exp Neurol. 1975 Mar;46(3):605-15
pubmed: 1112295
Science. 1980 May 9;208(4444):603-5
pubmed: 7367884
Brain Res. 1989 Mar 6;481(2):368-72
pubmed: 2720389
J Neurobiol. 2005 Jul;64(1):58-74
pubmed: 15884002
Neuroscience. 2014 Dec 26;283:138-65
pubmed: 25168733
Cell. 2007 Dec 14;131(6):1164-78
pubmed: 18083105
J Neuropathol Exp Neurol. 1998 Oct;57(10):915-30
pubmed: 9786242
J Neurophysiol. 2003 Mar;89(3):1353-62
pubmed: 12612004
J Neurosci. 2005 May 11;25(19):4733-42
pubmed: 15888649
J Physiol. 1979 Nov;296:215-26
pubmed: 529088
Nat Commun. 2014 Jul 11;5:4294
pubmed: 25014177
J Neuroimmune Pharmacol. 2015 Dec;10(4):587-94
pubmed: 26148561
J Neurotrauma. 2004 Jan;21(1):95-108
pubmed: 14987469
Neurobiol Dis. 2009 Feb;33(2):290-300
pubmed: 19049875
J Histochem Cytochem. 1994 Apr;42(4):451-7
pubmed: 7510317
Mol Chem Neuropathol. 1995 Jan;24(1):53-68
pubmed: 7755847
J Gen Physiol. 1959 May 20;42(5):931-58
pubmed: 13654743
Synapse. 1998 Feb;28(2):176-84
pubmed: 9450518
J Neurocytol. 1988 Apr;17(2):209-20
pubmed: 2849645
Muscle Nerve. 2005 Feb;31(2):135-56
pubmed: 15736297
Eur J Neurosci. 2003 Jan;17(1):13-27
pubmed: 12534965
J Comp Neurol. 2000 Oct 16;426(2):229-42
pubmed: 10982465
Anat Embryol (Berl). 1984;169(3):303-7
pubmed: 6476403
J Physiol. 1959 Jan 28;145(1):204-20
pubmed: 13621430
Neuroscience. 2011 May 19;182:1-10
pubmed: 21435379
Acta Neurol Scand Suppl. 1984;100:55-67
pubmed: 6207702
Anat Rec. 1994 Feb;238(2):248-62
pubmed: 8154610
J Neuroinflammation. 2010 Nov 12;7:77
pubmed: 21073708
Exp Neurol. 2019 Aug;318:124-134
pubmed: 31039333
Physiol Rep. 2017 May;5(9):
pubmed: 28468849
J Physiol. 2008 Mar 1;586(5):1225-31
pubmed: 17947305
J Neurosci. 2014 Apr 30;34(18):6389-404
pubmed: 24790209
Brain Res Bull. 2000 Nov 15;53(5):553-60
pubmed: 11165791
J Neurosci. 2002 Jun 1;22(11):4412-7
pubmed: 12040048
J Comp Neurol. 2009 Dec 10;517(5):670-82
pubmed: 19827159
Brain Res Brain Res Rev. 2004 Mar;44(2-3):154-78
pubmed: 15003391
Prog Neurobiol. 1990;35(1):1-51
pubmed: 2217820
J Comp Neurol. 2017 Sep 1;525(13):2876-2889
pubmed: 28543879
J Neurophysiol. 2000 Nov;84(5):2709-14
pubmed: 11068014
Neuroreport. 1997 May 6;8(7):1711-6
pubmed: 9189919
Orthopedics. 2017 Jan 1;40(1):e141-e156
pubmed: 27783836
J Neurosci. 2000 Sep 1;20(17):6734-40
pubmed: 10964980
J Physiol. 2010 Sep 15;588(Pt 18):3425-43
pubmed: 20660560
J Physiol. 1953 Sep;121(3):492-516
pubmed: 13097388
J Comp Neurol. 1999 Mar 29;406(1):29-50
pubmed: 10100891
J Neuroimmunol. 1992 Sep;40(1):99-109
pubmed: 1517400
J Comp Neurol. 2011 Aug 15;519(12):2335-52
pubmed: 21456016
Acta Neuropathol. 1971;17(3):265-82
pubmed: 5552043
Brain Res. 1979 Jan 12;160(2):347-52
pubmed: 761069
J Comp Neurol. 1978 Feb 15;177(4):635-64
pubmed: 624794
Brain Res Bull. 2017 Mar;129:50-65
pubmed: 27612963
J Neurosci. 1999 Apr 15;19(8):3162-70
pubmed: 10191329
J Anat. 1994 Dec;185 ( Pt 3):537-42
pubmed: 7649789
Nature. 2008 Oct 16;455(7215):903-11
pubmed: 18923512
Acta Neuropathol. 1989;78(4):348-58
pubmed: 2782046
J Physiol. 1976 Jul;259(1):159-75
pubmed: 957208
Glia. 1988;1(1):90-5
pubmed: 2976741
J Comp Neurol. 2000 Jun 26;422(2):172-80
pubmed: 10842225
J Neurophysiol. 1976 Jul;39(4):679-92
pubmed: 184256
J Comp Neurol. 1998 Oct 12;400(1):1-17
pubmed: 9762863
J Comp Neurol. 1979 Jul 15;186(2):189-211
pubmed: 87406
Neurology. 1987 Jun;37(6):985-92
pubmed: 2438594
Immunity. 2009 Nov 20;31(5):711-21
pubmed: 19836265
J Neurosci. 2011 Jul 27;31(30):10819-28
pubmed: 21795534
J Physiol. 1980 Sep;306:205-18
pubmed: 7463360
Prog Neurobiol. 1998 May;55(1):1-26
pubmed: 9602498
J Neurosci. 1995 May;15(5 Pt 2):3876-85
pubmed: 7751952
Prog Neurobiol. 2019 Feb;173:102-121
pubmed: 30579784
Mol Neurobiol. 2011 Feb;43(1):41-66
pubmed: 21190141
Mol Immunol. 2008 Sep;45(15):3865-77
pubmed: 18672287
J Comp Neurol. 1986 Feb 22;244(4):413-29
pubmed: 3958235
J Neurophysiol. 2017 Nov 1;118(5):2687-2701
pubmed: 28814636
Exp Neurol. 1997 Sep;147(1):18-27
pubmed: 9294399
Neurochem Int. 2017 Sep;108:332-342
pubmed: 28522413
Glia. 2008 Oct;56(13):1448-62
pubmed: 18512252
Exp Neurol. 2006 Aug;200(2):521-31
pubmed: 16631171
Neuroscientist. 2010 Dec;16(6):600-7
pubmed: 21239728
Neuroscience. 2000;100(1):171-81
pubmed: 10996467
Neural Plast. 2015;2015:392591
pubmed: 25918648
J Comp Neurol. 1994 Apr 1;342(1):35-44
pubmed: 8207127
Brain Res. 2012 Mar 29;1446:22-33
pubmed: 22325090
Exp Brain Res. 1997 Dec;117(3):453-6
pubmed: 9438713
Science. 1968 Apr 5;160(3823):96-8
pubmed: 4296007
J Cell Biol. 1970 Nov 1;47(2):319-31
pubmed: 19866734
Nature. 2010 Nov 11;468(7321):223-31
pubmed: 21068831
Neuroscience. 2017 Jan 6;340:188-200
pubmed: 27984178
Brain Res. 1981 Nov 9;224(1):165-9
pubmed: 7284832
J Biol Chem. 2002 Feb 15;277(7):4945-50
pubmed: 11733521
J Physiol. 1970 Nov;210(4):823-38
pubmed: 4322767
J Comp Neurol. 2004 Mar 29;471(2):201-18
pubmed: 14986313
Exp Brain Res. 1975 Mar 27;22(3):221-34
pubmed: 211046
Nat Neurosci. 2016 Jan;19(1):94-101
pubmed: 26642091
Rev Neurosci. 1996 Apr-Jun;7(2):115-49
pubmed: 8819206
Brain Res. 2006 Jun 20;1095(1):35-42
pubmed: 16714003
Neurosci Lett. 1988 Mar 10;85(3):317-21
pubmed: 3362421
Brain Res Mol Brain Res. 2000 Mar 29;76(2):325-35
pubmed: 10762708
Neuroscience. 1994 Aug;61(4):719-26
pubmed: 7530816
J Neurosci. 1996 May 15;16(10):3363-72
pubmed: 8627372
J Comp Neurol. 1984 Oct 10;229(1):121-8
pubmed: 6490973
J Neurosci Res. 1998 Jul 15;53(2):260-7
pubmed: 9671983
Eur J Neurosci. 1994 Oct 1;6(10):1615-8
pubmed: 7850025
J Comp Neurol. 1994 Jul 15;345(3):345-58
pubmed: 7929906
Eur J Neurosci. 2004 Oct;20(8):1984-94
pubmed: 15450077
J Comp Neurol. 2007 Jul 10;503(2):308-18
pubmed: 17492651
J Comp Neurol. 2000 Nov 20;427(3):370-90
pubmed: 11054700
J Neurosci. 2009 Oct 28;29(43):13503-15
pubmed: 19864563
J Neurocytol. 2000 Jul;29(7):509-23
pubmed: 11279366
Brain Res Rev. 2008 Jan;57(1):265-9
pubmed: 17764750
Exp Neurol. 2018 Jun;304:67-81
pubmed: 29522757
J Neurophysiol. 1995 Feb;73(2):662-73
pubmed: 7760125
Exp Brain Res. 1977 Aug 31;29(2):219-31
pubmed: 913516