TY - JOUR
T1 - The Synaptic Organization of Layer 6 Circuits Reveals Inhibition as a Major Output of a Neocortical Sublamina
AU - Frandolig, Jaclyn Ellen
AU - Matney, Chanel Joylae
AU - Lee, Kihwan
AU - Kim, Juhyun
AU - Chevée, Maxime
AU - Kim, Su Jeong
AU - Bickert, Aaron Andrew
AU - Brown, Solange Pezon
N1 - Funding Information:
The authors thank K. Deisseroth and the Stanford Neuroscience Gene Vector and Virus Core, S. Hestrin for Igor Pro routines, and J.Y. Cohen for thoughtful input. This work was supported by the National Institutes of Neurological Diseases ( RO1 NS085121 and P30NS050274 ) and the National Science Foundation (NSF; 1656592 ). C.J.M. was supported by an NSF Predoctoral Fellowship and an NIH Training Grant ( 5T32EY017203 ). J.K. was supported by a National Research Foundation of Korea Fellowship ( NRF-2011-357-E00005 ). M.C. was supported by a Boehringer Ingelheim Fonds Fellowship . A.A.B. was supported by a Johns Hopkins Provost’s Undergraduate Research Award . S.P.B. was supported by a Klingenstein-Simons Fellowship in the Neurosciences .
Funding Information:
The authors thank K. Deisseroth and the Stanford Neuroscience Gene Vector and Virus Core, S. Hestrin for Igor Pro routines, and J.Y. Cohen for thoughtful input. This work was supported by the National Institutes of Neurological Diseases (RO1 NS085121 and P30NS050274) and the National Science Foundation (NSF; 1656592). C.J.M. was supported by an NSF Predoctoral Fellowship and an NIH Training Grant (5T32EY017203). J.K. was supported by a National Research Foundation of Korea Fellowship (NRF-2011-357-E00005). M.C. was supported by a Boehringer Ingelheim Fonds Fellowship. A.A.B. was supported by a Johns Hopkins Provost's Undergraduate Research Award. S.P.B. was supported by a Klingenstein-Simons Fellowship in the Neurosciences. S.P.B. C.J.M. and J.E.F. conceived the study. C.J.M. K.L. J.K. M.C. and S.-J.K. performed the experiments. J.E.F. analyzed the data with assistance from C.J.M. K.L. J.K. S.-J.K. M.C. A.A.B. and S.P.B. S.P.B. wrote the manuscript with input from all of the authors. The authors declare no competing interests.
Publisher Copyright:
© 2019 The Authors
PY - 2019/9/17
Y1 - 2019/9/17
N2 - The canonical cortical microcircuit has principally been defined by interlaminar excitatory connections among the six layers of the neocortex. However, excitatory neurons in layer 6 (L6), a layer whose functional organization is poorly understood, form relatively rare synaptic connections with other cortical excitatory neurons. Here, we show that the vast majority of parvalbumin inhibitory neurons in a sublamina within L6 send axons through the cortical layers toward the pia. These interlaminar inhibitory neurons receive local synaptic inputs from both major types of L6 excitatory neurons and receive stronger input from thalamocortical afferents than do neighboring pyramidal neurons. The distribution of these interlaminar interneurons and their synaptic connectivity further support a functional subdivision within the standard six layers of the cortex. Positioned to integrate local and long-distance inputs in this sublayer, these interneurons generate an inhibitory interlaminar output. These findings call for a revision to the canonical cortical microcircuit.
AB - The canonical cortical microcircuit has principally been defined by interlaminar excitatory connections among the six layers of the neocortex. However, excitatory neurons in layer 6 (L6), a layer whose functional organization is poorly understood, form relatively rare synaptic connections with other cortical excitatory neurons. Here, we show that the vast majority of parvalbumin inhibitory neurons in a sublamina within L6 send axons through the cortical layers toward the pia. These interlaminar inhibitory neurons receive local synaptic inputs from both major types of L6 excitatory neurons and receive stronger input from thalamocortical afferents than do neighboring pyramidal neurons. The distribution of these interlaminar interneurons and their synaptic connectivity further support a functional subdivision within the standard six layers of the cortex. Positioned to integrate local and long-distance inputs in this sublayer, these interneurons generate an inhibitory interlaminar output. These findings call for a revision to the canonical cortical microcircuit.
KW - corticocortical neurons
KW - corticothalamic neurons
KW - fast-spiking interneurons
KW - layer 6
KW - neocortex
KW - parvalbumin interneurons
KW - thalamus
UR - http://www.scopus.com/inward/record.url?scp=85071975657&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85071975657&partnerID=8YFLogxK
U2 - 10.1016/j.celrep.2019.08.048
DO - 10.1016/j.celrep.2019.08.048
M3 - Article
C2 - 31533036
AN - SCOPUS:85071975657
SN - 2211-1247
VL - 28
SP - 3131-3143.e5
JO - Cell Reports
JF - Cell Reports
IS - 12
ER -