TY - JOUR
T1 - Morning and Evening Circadian Pacemakers Independently Drive Premotor Centers via a Specific Dopamine Relay
AU - Liang, Xitong
AU - Ho, Margaret C.W.
AU - Zhang, Yajun
AU - Li, Yulong
AU - Wu, Mark N.
AU - Holy, Timothy E.
AU - Taghert, Paul H.
N1 - Funding Information:
We thank Cody Greer for building the OCPI-2 microscope, the Holy and Taghert laboratories for advice, and the Washington University Center for Cellular Imaging (WUCCI) for technical support. Heather Dionne, Gerry Rubin, Aljoscha Nern, and Francois Rouyer kindly shared unpublished fly stocks and information. Orie Shafer, Michael Rosbash, the Bloomington Stock Center, and Janelia Research Center provided fly stocks and reagents. The work was supported by the Washington University McDonnell Center for Cellular and Molecular Neurobiology and by NIH grants, United States R01 NS068409 and R01 DP1 DA035081 (T.E.H.), R01 NS099332 and R01 GM127508 (P.H.T.), and R24 NS086741 (T.E.H. and P.H.T.); NIH Training Grant, United States T32HL110952 (M.C.W.H.) and R01NS079584 (M.N.W.); National Basic Research Program of China , China (973 Program; grant 2015CB856402 to Y.L.); the General Program of National Natural Science Foundation of China , China (project 31671118 to Y.L.); NIH BRAIN Initiative grant, United States U01NS103558 (Y.L.); and a Peking University Postdoctoral Fellowship , China (Y.Z.).
Funding Information:
We thank Cody Greer for building the OCPI-2 microscope, the Holy and Taghert laboratories for advice, and the Washington University Center for Cellular Imaging (WUCCI) for technical support. Heather Dionne, Gerry Rubin, Aljoscha Nern, and Francois Rouyer kindly shared unpublished fly stocks and information. Orie Shafer, Michael Rosbash, the Bloomington Stock Center, and Janelia Research Center provided fly stocks and reagents. The work was supported by the Washington University McDonnell Center for Cellular and Molecular Neurobiology and by NIH grants, United States R01 NS068409 and R01 DP1 DA035081 (T.E.H.), R01 NS099332 and R01 GM127508 (P.H.T.), and R24 NS086741 (T.E.H. and P.H.T.); NIH Training Grant, United States T32HL110952 (M.C.W.H.) and R01NS079584 (M.N.W.); National Basic Research Program of China, China (973 Program; grant 2015CB856402 to Y.L.); the General Program of National Natural Science Foundation of China, China (project 31671118 to Y.L.); NIH BRAIN Initiative grant, United States U01NS103558 (Y.L.); and a Peking University Postdoctoral Fellowship, China (Y.Z.). X.L. M.N.W. T.E.H. and P.H.T. conceived the experiments; X.L. performed and analyzed all experiments; M.C.W.H. generated and characterized the dopamine-related transgenic fly lines; Y.Z. and Y.L. generated the dopamine sensor GRAB
Publisher Copyright:
© 2019 Elsevier Inc.
PY - 2019/5/22
Y1 - 2019/5/22
N2 - Many animals exhibit morning and evening peaks of locomotor behavior. In Drosophila, two corresponding circadian neural oscillators—M (morning) cells and E (evening) cells—exhibit a corresponding morning or evening neural activity peak. Yet we know little of the neural circuitry by which distinct circadian oscillators produce specific outputs to precisely control behavioral episodes. Here, we show that ring neurons of the ellipsoid body (EB-RNs) display spontaneous morning and evening neural activity peaks in vivo: these peaks coincide with the bouts of locomotor activity and result from independent activation by M and E pacemakers. Further, M and E cells regulate EB-RNs via identified PPM3 dopaminergic neurons, which project to the EB and are normally co-active with EB-RNs. These in vivo findings establish the fundamental elements of a circadian neuronal output pathway: distinct circadian oscillators independently drive a common pre-motor center through the agency of specific dopaminergic interneurons. Liang et al. describe neural outputs from the Drosophila circadian pacemaker network regulating locomotor rhythms: via a specific dopamine relay, the network forms parallel connections to the central complex, the pre-motor area dictating the balance between rest and activity.
AB - Many animals exhibit morning and evening peaks of locomotor behavior. In Drosophila, two corresponding circadian neural oscillators—M (morning) cells and E (evening) cells—exhibit a corresponding morning or evening neural activity peak. Yet we know little of the neural circuitry by which distinct circadian oscillators produce specific outputs to precisely control behavioral episodes. Here, we show that ring neurons of the ellipsoid body (EB-RNs) display spontaneous morning and evening neural activity peaks in vivo: these peaks coincide with the bouts of locomotor activity and result from independent activation by M and E pacemakers. Further, M and E cells regulate EB-RNs via identified PPM3 dopaminergic neurons, which project to the EB and are normally co-active with EB-RNs. These in vivo findings establish the fundamental elements of a circadian neuronal output pathway: distinct circadian oscillators independently drive a common pre-motor center through the agency of specific dopaminergic interneurons. Liang et al. describe neural outputs from the Drosophila circadian pacemaker network regulating locomotor rhythms: via a specific dopamine relay, the network forms parallel connections to the central complex, the pre-motor area dictating the balance between rest and activity.
UR - http://www.scopus.com/inward/record.url?scp=85065236854&partnerID=8YFLogxK
U2 - 10.1016/j.neuron.2019.03.028
DO - 10.1016/j.neuron.2019.03.028
M3 - Article
C2 - 30981533
AN - SCOPUS:85065236854
SN - 0896-6273
VL - 102
SP - 843-857.e4
JO - Neuron
JF - Neuron
IS - 4
ER -