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Extreme Compartmentalization in a Drosophila Amacrine Cell

2019; Elsevier BV; Volume: 29; Issue: 9 Linguagem: Inglês

10.1016/j.cub.2019.03.070

1879-0445

Matthias Meier, Alexander Borst,

Viral Infectious Diseases and Gene Expression in Insects

A neuron is conventionally regarded as a single processing unit. It receives input from one or several presynaptic cells, transforms these signals, and transmits one output signal to its postsynaptic partners. Exceptions exist: amacrine cells in the mammalian retina [1Euler T. Detwiler P.B. Denk W. Directionally selective calcium signals in dendrites of starburst amacrine cells.Nature. 2002; 418: 845-852Crossref PubMed Scopus (432) Google Scholar, 2Grimes W.N. Zhang J. Graydon C.W. Kachar B. Diamond J.S. Retinal parallel processors: more than 100 independent microcircuits operate within a single interneuron.Neuron. 2010; 65: 873-885Abstract Full Text Full Text PDF PubMed Scopus (106) Google Scholar, 3Masland R.H. The tasks of amacrine cells.Vis. Neurosci. 2012; 29: 3-9Crossref PubMed Scopus (90) Google Scholar] or interneurons in the locust mesothoracic ganglion [4Laurent G. Burrows M. Intersegmental interneurons can control the gain of reflexes in adjacent segments of the locust by their action on nonspiking local interneurons.J. Neurosci. 1989; 9: 3030-3039Crossref PubMed Google Scholar] are thought to represent many electrically isolated microcircuits within one neuron. An extreme case of such an amacrine cell has recently been described in the Drosophila visual system. This cell, called CT1, reaches into two neuropils of the optic lobe, where it visits each of 700 repetitive columns, thereby covering the whole visual field [5Shinomiya K. Takemura S.Y. Rivlin P.K. Plaza S.M. Scheffer L.K. Meinertzhagen I.A. A common evolutionary origin for the ON- and OFF-edge motion detection pathways of the Drosophila visual system.Front. Neural Circuits. 2015; 9: 33Crossref PubMed Scopus (21) Google Scholar, 6Takemura S.Y. Nern A. Chklovskii D.B. Scheffer L.K. Rubin G.M. Meinertzhagen I.A. The comprehensive connectome of a neural substrate for ‘ON’ motion detection in Drosophila.eLife. 2017; 6: e24394Crossref PubMed Scopus (112) Google Scholar]. Due to its unusual morphology, CT1 has been suspected to perform local computations [6Takemura S.Y. Nern A. Chklovskii D.B. Scheffer L.K. Rubin G.M. Meinertzhagen I.A. The comprehensive connectome of a neural substrate for ‘ON’ motion detection in Drosophila.eLife. 2017; 6: e24394Crossref PubMed Scopus (112) Google Scholar, 7Shinomiya K. Huang G. Lu Z. Parag T. Xu C.S. Aniceto R. Ansari N. Cheatham N. Lauchie S. Neace E. et al.Comparisons between the ON- and OFF-edge motion pathways in the Drosophila brain.eLife. 2019; 8: e40025Crossref PubMed Scopus (39) Google Scholar], but this has never been proven. Using 2-photon calcium imaging and visual stimulation, we find highly compartmentalized retinotopic response properties in neighboring terminals of CT1, with each terminal acting as an independent functional unit. Model simulations demonstrate that this extreme case of compartmentalization is at the biophysical limit of neural computation.