Development of Concurrent Retinotopic Maps in the Fly Motion Detection Circuit

Filipe Pinto-Teixeira, Clara Koo, Anthony Michael Rossi, Nathalie Neriec, Claire Bertet, Xin Li, Alberto Del-Valle-Rodriguez, Claude Desplan

Research output: Contribution to journalArticle

Abstract

Understanding how complex brain wiring is produced during development is a daunting challenge. In Drosophila, information from 800 retinal ommatidia is processed in distinct brain neuropiles, each subdivided into 800 matching retinotopic columns. The lobula plate comprises four T4 and four T5 neuronal subtypes. T4 neurons respond to bright edge motion, whereas T5 neurons respond to dark edge motion. Each is tuned to motion in one of the four cardinal directions, effectively establishing eight concurrent retinotopic maps to support wide-field motion. We discovered a mode of neurogenesis where two sequential Notch-dependent divisions of either a horizontal or a vertical progenitor produce matching sets of two T4 and two T5 neurons retinotopically coincident with pairwise opposite direction selectivity. We show that retinotopy is an emergent characteristic of this neurogenic program and derives directly from neuronal birth order. Our work illustrates how simple developmental rules can implement complex neural organization. The circuit for motion perception emerges out of the developmental program that specifies the identity of neurons.

Original languageEnglish (US)
Pages (from-to)485-498.e11
JournalCell
Volume173
Issue number2
DOIs
StatePublished - Apr 5 2018

Fingerprint

Neurons
Networks (circuits)
Brain
Motion Perception
Birth Order
Neuropil
Neurogenesis
Electric wiring
Drosophila
Direction compound

Keywords

  • Drosophila
  • Notch
  • direction selective neurons
  • neural connectivity
  • neural development
  • optic lobe
  • pattern formation
  • retinotopy

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Pinto-Teixeira, F., Koo, C., Rossi, A. M., Neriec, N., Bertet, C., Li, X., ... Desplan, C. (2018). Development of Concurrent Retinotopic Maps in the Fly Motion Detection Circuit. Cell, 173(2), 485-498.e11. https://doi.org/10.1016/j.cell.2018.02.053

Development of Concurrent Retinotopic Maps in the Fly Motion Detection Circuit. / Pinto-Teixeira, Filipe; Koo, Clara; Rossi, Anthony Michael; Neriec, Nathalie; Bertet, Claire; Li, Xin; Del-Valle-Rodriguez, Alberto; Desplan, Claude.

In: Cell, Vol. 173, No. 2, 05.04.2018, p. 485-498.e11.

Research output: Contribution to journalArticle

Pinto-Teixeira, F, Koo, C, Rossi, AM, Neriec, N, Bertet, C, Li, X, Del-Valle-Rodriguez, A & Desplan, C 2018, 'Development of Concurrent Retinotopic Maps in the Fly Motion Detection Circuit', Cell, vol. 173, no. 2, pp. 485-498.e11. https://doi.org/10.1016/j.cell.2018.02.053
Pinto-Teixeira F, Koo C, Rossi AM, Neriec N, Bertet C, Li X et al. Development of Concurrent Retinotopic Maps in the Fly Motion Detection Circuit. Cell. 2018 Apr 5;173(2):485-498.e11. https://doi.org/10.1016/j.cell.2018.02.053
Pinto-Teixeira, Filipe ; Koo, Clara ; Rossi, Anthony Michael ; Neriec, Nathalie ; Bertet, Claire ; Li, Xin ; Del-Valle-Rodriguez, Alberto ; Desplan, Claude. / Development of Concurrent Retinotopic Maps in the Fly Motion Detection Circuit. In: Cell. 2018 ; Vol. 173, No. 2. pp. 485-498.e11.
@article{6acbf16e035748e8bdc4abe7a65f41e7,
title = "Development of Concurrent Retinotopic Maps in the Fly Motion Detection Circuit",
abstract = "Understanding how complex brain wiring is produced during development is a daunting challenge. In Drosophila, information from 800 retinal ommatidia is processed in distinct brain neuropiles, each subdivided into 800 matching retinotopic columns. The lobula plate comprises four T4 and four T5 neuronal subtypes. T4 neurons respond to bright edge motion, whereas T5 neurons respond to dark edge motion. Each is tuned to motion in one of the four cardinal directions, effectively establishing eight concurrent retinotopic maps to support wide-field motion. We discovered a mode of neurogenesis where two sequential Notch-dependent divisions of either a horizontal or a vertical progenitor produce matching sets of two T4 and two T5 neurons retinotopically coincident with pairwise opposite direction selectivity. We show that retinotopy is an emergent characteristic of this neurogenic program and derives directly from neuronal birth order. Our work illustrates how simple developmental rules can implement complex neural organization. The circuit for motion perception emerges out of the developmental program that specifies the identity of neurons.",
keywords = "Drosophila, Notch, direction selective neurons, neural connectivity, neural development, optic lobe, pattern formation, retinotopy",
author = "Filipe Pinto-Teixeira and Clara Koo and Rossi, {Anthony Michael} and Nathalie Neriec and Claire Bertet and Xin Li and Alberto Del-Valle-Rodriguez and Claude Desplan",
year = "2018",
month = "4",
day = "5",
doi = "10.1016/j.cell.2018.02.053",
language = "English (US)",
volume = "173",
pages = "485--498.e11",
journal = "Cell",
issn = "0092-8674",
publisher = "Cell Press",
number = "2",

}

TY - JOUR

T1 - Development of Concurrent Retinotopic Maps in the Fly Motion Detection Circuit

AU - Pinto-Teixeira, Filipe

AU - Koo, Clara

AU - Rossi, Anthony Michael

AU - Neriec, Nathalie

AU - Bertet, Claire

AU - Li, Xin

AU - Del-Valle-Rodriguez, Alberto

AU - Desplan, Claude

PY - 2018/4/5

Y1 - 2018/4/5

N2 - Understanding how complex brain wiring is produced during development is a daunting challenge. In Drosophila, information from 800 retinal ommatidia is processed in distinct brain neuropiles, each subdivided into 800 matching retinotopic columns. The lobula plate comprises four T4 and four T5 neuronal subtypes. T4 neurons respond to bright edge motion, whereas T5 neurons respond to dark edge motion. Each is tuned to motion in one of the four cardinal directions, effectively establishing eight concurrent retinotopic maps to support wide-field motion. We discovered a mode of neurogenesis where two sequential Notch-dependent divisions of either a horizontal or a vertical progenitor produce matching sets of two T4 and two T5 neurons retinotopically coincident with pairwise opposite direction selectivity. We show that retinotopy is an emergent characteristic of this neurogenic program and derives directly from neuronal birth order. Our work illustrates how simple developmental rules can implement complex neural organization. The circuit for motion perception emerges out of the developmental program that specifies the identity of neurons.

AB - Understanding how complex brain wiring is produced during development is a daunting challenge. In Drosophila, information from 800 retinal ommatidia is processed in distinct brain neuropiles, each subdivided into 800 matching retinotopic columns. The lobula plate comprises four T4 and four T5 neuronal subtypes. T4 neurons respond to bright edge motion, whereas T5 neurons respond to dark edge motion. Each is tuned to motion in one of the four cardinal directions, effectively establishing eight concurrent retinotopic maps to support wide-field motion. We discovered a mode of neurogenesis where two sequential Notch-dependent divisions of either a horizontal or a vertical progenitor produce matching sets of two T4 and two T5 neurons retinotopically coincident with pairwise opposite direction selectivity. We show that retinotopy is an emergent characteristic of this neurogenic program and derives directly from neuronal birth order. Our work illustrates how simple developmental rules can implement complex neural organization. The circuit for motion perception emerges out of the developmental program that specifies the identity of neurons.

KW - Drosophila

KW - Notch

KW - direction selective neurons

KW - neural connectivity

KW - neural development

KW - optic lobe

KW - pattern formation

KW - retinotopy

UR - http://www.scopus.com/inward/record.url?scp=85044149428&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85044149428&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2018.02.053

DO - 10.1016/j.cell.2018.02.053

M3 - Article

C2 - 29576455

AN - SCOPUS:85044149428

VL - 173

SP - 485-498.e11

JO - Cell

JF - Cell

SN - 0092-8674

IS - 2

ER -