Synaptic circuits and their variations within different columns in the visual system of Drosophila.
We reconstructed the synaptic circuits of seven columns in the second neuropil or medulla behind the fly's compound eye. These neurons embody some of the most stereotyped circuits in one of the most miniaturized of animal brains. The reconstructions allow us, for the first time to our knowledge, to study variations between circuits in the medulla's neighboring columns. This variation in the number of synapses and the types of their synaptic partners has previously been little addressed because methods that visualize multiple circuits have not resolved detailed connections, and existing connectomic studies, which can see such connections, have not so far examined multiple reconstructions of the same circuit. Here, we address the omission by comparing the circuits common to all seven columns to assess variation in their connection strengths and the resultant rates of several different and distinct types of connection error. Error rates reveal that, overall, <1% of contacts are not part of a consensus circuit, and we classify those contacts that supplement (E+) or are missing from it (E-). Autapses, in which the same cell is both presynaptic and postsynaptic at the same synapse, are occasionally seen; two cells in particular, Dm9 and Mi1, form ≥ 20-fold more autapses than do other neurons. These results delimit the accuracy of developmental events that establish and normally maintain synaptic circuits with such precision, and thereby address the operation of such circuits. They also establish a precedent for error rates that will be required in the new science of connectomics.
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Shin-ya
SY
Takemura
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
C Shan
CS
Xu
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147; Department of Psychology and Neuroscience, Dalhousie University, Halifax, NS, Canada B3H 4R2;
Zhiyuan
Z
Lu
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Patricia K
PK
Rivlin
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Toufiq
T
Parag
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Donald J
DJ
Olbris
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Stephen
S
Plaza
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Ting
T
Zhao
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
William T
WT
Katz
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Lowell
L
Umayam
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Charlotte
C
Weaver
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Harald F
HF
Hess
Department of Psychology and Neuroscience, Dalhousie University, Halifax, NS, Canada B3H 4R2;
Jane Anne
JA
Horne
Life Sciences Computation Centre, University of Melbourne, Carlton, VIC 3010, Australia;
Juan
J
Nunez-Iglesias
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Roxanne
R
Aniceto
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Lei-Ann
LA
Chang
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Shirley
S
Lauchie
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Ashley
A
Nasca
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Omotara
O
Ogundeyi
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Christopher
C
Sigmund
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Satoko
S
Takemura
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
Julie
J
Tran
Department of Psychology and Neuroscience, Dalhousie University, Halifax, NS, Canada B3H 4R2;
Carlie
C
Langille
Department of Psychology and Neuroscience, Dalhousie University, Halifax, NS, Canada B3H 4R2;
Kelsey
K
Le Lacheur
Department of Psychology and Neuroscience, Dalhousie University, Halifax, NS, Canada B3H 4R2;
Sari
S
McLin
Department of Psychology and Neuroscience, Dalhousie University, Halifax, NS, Canada B3H 4R2;
Aya
A
Shinomiya
Simons Center for Data Analysis, Simons Foundation, New York, NY 10010.
Dmitri B
DB
Chklovskii
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147; Department of Psychology and Neuroscience, Dalhousie University, Halifax, NS, Canada B3H 4R2;
Ian A
IA
Meinertzhagen
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147; schefferl@janelia.hhmi.org.
Louis K
LK
Scheffer
D000818:Animals; D004331:Drosophila melanogaster / Q000502:physiology*; D013569:Synapses / Q000502:physiology*; D014785:Vision, Ocular / Q000502:physiology*
biological error rates; neural circuits; reconstruction error rates; stereotypy