TY - JOUR
T1 - Emergence of functional subnetworks in layer 2/3 cortex induced by sequential spikes in vivo
AU - Kim, Taekeun
AU - Oh, Won Chan
AU - Choi, Joon Ho
AU - Kwon, Hyung Bae
N1 - Funding Information:
We thank all members of the H.B.-K. laboratory. We also thank D. Fitzpatrick, B. L. Sabatini, R. Yasuda, H. Taniguchi, N. X. Tritsch, and B. Sakmann for their constructive comments on the initial manuscripts. We thank J. Schummers and L. Yan for help in setting up in vivo animal surgeries and with the two-photon microscope setup. GCaMP6f virus was available from the Genetically-Encoded Neuronal Indicator and Effector (GENIE) Project and the Janelia Farm Research Campus, especially V. Jayaraman, R. A. Kerr, D. S. Kim, L. L. Looger, and K. Svoboda. This work was supportive by funding from the Max Planck Florida Institute for Neuroscience (to H.-B.K.) and R01 MH107460 (to H.-B.K.).
PY - 2016/3/8
Y1 - 2016/3/8
N2 - During cortical circuit development in the mammalian brain, groups of excitatory neurons that receive similar sensory information form microcircuits. However, cellular mechanisms underlying cortical microcircuit development remain poorly understood. Here we implemented combined two-photon imaging and photolysis in vivo to monitor and manipulate neuronal activities to study the processes underlying activity-dependent circuit changes. We found that repeated triggering of spike trains in a randomly chosen group of layer 2/3 pyramidal neurons in the somatosensory cortex triggered long-term plasticity of circuits (LTPc), resulting in the increased probability that the selected neurons would fire when action potentials of individual neurons in the group were evoked. Significant firing pattern changes were observed more frequently in the selected group of neurons than in neighboring control neurons, and the induction was dependent on the time interval between spikes, N-methyl-D-aspartate (NMDA) receptor activation, and Calcium/calmodulin-dependent protein kinase II (CaMKII) activation. In addition, LTPc was associated with an increase of activity from a portion of neighboring neurons with different probabilities. Thus, our results demonstrate that the formation of functional microcircuits requires broad network changes and that its directionality is nonrandom, which may be a general feature of cortical circuit assembly in the mammalian cortex.
AB - During cortical circuit development in the mammalian brain, groups of excitatory neurons that receive similar sensory information form microcircuits. However, cellular mechanisms underlying cortical microcircuit development remain poorly understood. Here we implemented combined two-photon imaging and photolysis in vivo to monitor and manipulate neuronal activities to study the processes underlying activity-dependent circuit changes. We found that repeated triggering of spike trains in a randomly chosen group of layer 2/3 pyramidal neurons in the somatosensory cortex triggered long-term plasticity of circuits (LTPc), resulting in the increased probability that the selected neurons would fire when action potentials of individual neurons in the group were evoked. Significant firing pattern changes were observed more frequently in the selected group of neurons than in neighboring control neurons, and the induction was dependent on the time interval between spikes, N-methyl-D-aspartate (NMDA) receptor activation, and Calcium/calmodulin-dependent protein kinase II (CaMKII) activation. In addition, LTPc was associated with an increase of activity from a portion of neighboring neurons with different probabilities. Thus, our results demonstrate that the formation of functional microcircuits requires broad network changes and that its directionality is nonrandom, which may be a general feature of cortical circuit assembly in the mammalian cortex.
KW - Layer 2/3 cortex
KW - Neuronal connectivity
KW - Spike timing-dependent plasticity
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U2 - 10.1073/pnas.1513410113
DO - 10.1073/pnas.1513410113
M3 - Article
C2 - 26903616
AN - SCOPUS:84960370190
SN - 0027-8424
VL - 113
SP - E1372-E1381
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 10
ER -