Cofilin1 controls transcolumnar plasticity in dendritic spines in adult barrel cortex.
During sensory deprivation, the barrel cortex undergoes expansion of a functional column representing spared inputs (spared column), into the neighboring deprived columns (representing deprived inputs) which are in turn shrunk. As a result, the neurons in a deprived column simultaneously increase and decrease their responses to spared and deprived inputs, respectively. Previous studies revealed that dendritic spines are remodeled during this barrel map plasticity. Because cofilin1, a predominant regulator of actin filament turnover, governs both the expansion and shrinkage of the dendritic spine structure in vitro, it hypothetically regulates both responses in barrel map plasticity. However, this hypothesis remains untested. Using lentiviral vectors, we knocked down cofilin1 locally within layer 2/3 neurons in a deprived column. Cofilin1-knocked-down neurons were optogenetically labeled using channelrhodopsin-2, and electrophysiological recordings were targeted to these knocked-down neurons. We showed that cofilin1 knockdown impaired response increases to spared inputs but preserved response decreases to deprived inputs, indicating that cofilin1 dependency is dissociated in these two types of barrel map plasticity. To explore the structural basis of this dissociation, we then analyzed spine densities on deprived column dendritic branches, which were supposed to receive dense horizontal transcolumnar projections from the spared column. We found that spine number increased in a cofilin1-dependent manner selectively in the distal part of the supragranular layer, where most of the transcolumnar projections existed. Our findings suggest that cofilin1-mediated actin dynamics regulate functional map plasticity in an input-specific manner through the dendritic spine remodeling that occurs in the horizontal transcolumnar circuits. These new mechanistic insights into transcolumnar plasticity in adult rats may have a general significance for understanding reorganization of neocortical circuits that have more sophisticated columnar organization than the rodent neocortex, such as the primate neocortex.
Department of Physiology, The University of Tokyo School of Medicine, Tokyo, Japan.
Tadashi
T
Tsubota
Department of Biochemistry, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama, Toyama, Japan; Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Saitama, Japan.
Reiko
R
Okubo-Suzuki
Department of Physiology, The University of Tokyo School of Medicine, Tokyo, Japan.
Yohei
Y
Ohashi
Department of Physiology, The University of Tokyo School of Medicine, Tokyo, Japan.
Keita
K
Tamura
Department of Physiology, The University of Tokyo School of Medicine, Tokyo, Japan.
Koshin
K
Ogata
Department of Physiology, The University of Tokyo School of Medicine, Tokyo, Japan.
Masae
M
Yaguchi
Department of Physiology, The University of Tokyo School of Medicine, Tokyo, Japan.
Makoto
M
Matsuyama
Department of Biochemistry, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama, Toyama, Japan; Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Saitama, Japan.
Kaoru
K
Inokuchi
Department of Physiology, The University of Tokyo School of Medicine, Tokyo, Japan; Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Saitama, Japan.
Yasushi
Y
Miyashita
D000199:Actins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D000200:Action Potentials / Q000502:physiology; D000818:Animals; D000075402:Channelrhodopsins; D051338:Cofilin 1 / Q000037:antagonists & inhibitors / Q000235:genetics* / Q000378:metabolism; D049229:Dendritic Spines / Q000235:genetics / Q000378:metabolism* / Q000648:ultrastructure; D015870:Gene Expression; D055785:Gene Knockdown Techniques; D005822:Genetic Vectors; D057809:HEK293 Cells; D006801:Humans; D016086:Lentivirus / Q000235:genetics / Q000378:metabolism; D008297:Male; D019579:Neocortex / Q000378:metabolism* / Q000648:ultrastructure; D009473:Neuronal Plasticity / Q000502:physiology*; D062308:Optogenetics; D016716:PC12 Cells; D051381:Rats; D017208:Rats, Wistar; D012683:Sensory Deprivation / Q000502:physiology; D013003:Somatosensory Cortex / Q000378:metabolism* / Q000648:ultrastructure; D013569:Synapses / Q000235:genetics / Q000378:metabolism* / Q000648:ultrastructure
D000199:Actins; C495812:Cfl1 protein, rat; D000075402:Channelrhodopsins; D051338:Cofilin 1