Strategies for assembling columns and layers in the  Drosophila  visual system

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Abstract

A striking feature of neural circuit structure is the arrangement of neurons into regularly spaced ensembles (i.e. columns) and neural connections into parallel layers. These patterns of organization are thought to underlie precise synaptic connectivity and provide a basis for the parallel processing of information. In this article we discuss in detail specific findings that contribute to a framework for understanding how columns and layers are assembled in the Drosophila visual system, and discuss their broader implications.

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Most cited references 98

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An olfactory sensory map in the fly brain.

L B Vosshall, A M Wong, R. Axel (2000)

We have isolated the "complete" repertoire of genes encoding the odorant receptors in Drosophila and employ these genes to provide a molecular description of the organization of the peripheral olfactory system. The repertoire of Drosophila odorant receptors is encoded by 57 genes. Individual sensory neurons are likely to express only a single receptor gene. Neurons expressing a given gene project axons to one or two spatially invariant glomeruli in the antennal lobe. The insect brain therefore retains a two-dimensional map of receptor activation such that the quality of an odor may be encoded by different spatial patterns of activity in the antennal lobe.

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Design principles of insect and vertebrate visual systems.

Joshua Sanes, S Lawrence Zipursky (2010)

A century ago, Cajal noted striking similarities between the neural circuits that underlie vision in vertebrates and flies. Over the past few decades, structural and functional studies have provided strong support for Cajal's view. In parallel, genetic studies have revealed some common molecular mechanisms controlling development of vertebrate and fly visual systems and suggested that they share a common evolutionary origin. Here, we review these shared features, focusing on the first several layers-retina, optic tectum (superior colliculus), and lateral geniculate nucleus in vertebrates; and retina, lamina, and medulla in fly. We argue that vertebrate and fly visual circuits utilize common design principles and that taking advantage of this phylogenetic conservation will speed progress in elucidating both functional strategies and developmental mechanisms, as has already occurred in other areas of neurobiology ranging from electrical signaling and synaptic plasticity to neurogenesis and axon guidance. Copyright 2010 Elsevier Inc. All rights reserved.

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The cortical column: a structure without a function.

D. Adams, Jonathan Horton (2005)

This year, the field of neuroscience celebrates the 50th anniversary of Mountcastle's discovery of the cortical column. In this review, we summarize half a century of research and come to the disappointing realization that the column may have no function. Originally, it was described as a discrete structure, spanning the layers of the somatosensory cortex, which contains cells responsive to only a single modality, such as deep joint receptors or cutaneous receptors. Subsequently, examples of columns have been uncovered in numerous cortical areas, expanding the original concept to embrace a variety of different structures and principles. A "column" now refers to cells in any vertical cluster that share the same tuning for any given receptive field attribute. In striate cortex, for example, cells with the same eye preference are grouped into ocular dominance columns. Unaccountably, ocular dominance columns are present in some species, but not others. In principle, it should be possible to determine their function by searching for species differences in visual performance that correlate with their presence or absence. Unfortunately, this approach has been to no avail; no visual faculty has emerged that appears to require ocular dominance columns. Moreover, recent evidence has shown that the expression of ocular dominance columns can be highly variable among members of the same species, or even in different portions of the visual cortex in the same individual. These observations deal a fatal blow to the idea that ocular dominance columns serve a purpose. More broadly, the term "column" also denotes the periodic termination of anatomical projections within or between cortical areas. In many instances, periodic projections have a consistent relationship with some architectural feature, such as the cytochrome oxidase patches in V1 or the stripes in V2. These tissue compartments appear to divide cells with different receptive field properties into distinct processing streams. However, it is unclear what advantage, if any, is conveyed by this form of columnar segregation. Although the column is an attractive concept, it has failed as a unifying principle for understanding cortical function. Unravelling the organization of the cerebral cortex will require a painstaking description of the circuits, projections and response properties peculiar to cells in each of its various areas.

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Author and article information

Contributors

S. Sean Millard:

ORCID: http://orcid.org/0000-0001-8573-4625

s.millard@uq.edu.au

Matthew Y. Pecot:

ORCID: http://orcid.org/0000-0001-8241-8002

Matthew_Pecot@hms.harvard.edu

Journal

Journal ID (nlm-ta): Neural Dev

Journal ID (iso-abbrev): Neural Dev

Title: Neural Development

Publisher: BioMed Central (London )

ISSN (Electronic): 1749-8104

Publication date (Electronic): 7 June 2018

Publication date PMC-release: 7 June 2018

Publication date Collection: 2018

Volume: 13

Electronic Location Identifier: 11

Affiliations

[1 ]ISNI 0000 0000 9320 7537, GRID grid.1003.2, School of Biomedical Sciences, , The University of Queensland, ; Brisbane, QLD 4072 Australia

[2 ]ISNI 000000041936754X, GRID grid.38142.3c, Department of Neurobiology, , Harvard Medical School, ; Boston, MA 02115 USA

Author information

S. Sean Millard http://orcid.org/0000-0001-8573-4625

Matthew Y. Pecot http://orcid.org/0000-0001-8241-8002

Article

Publisher ID: 106

DOI: 10.1186/s13064-018-0106-9

PMC ID: 5991427

PubMed ID: 29875010

SO-VID: 16443d33-2bd3-4c2c-af39-2d0f25a0a530

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 9 November 2017

Date accepted : 24 April 2018

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000025, National Institute of Mental Health;

Award ID: K01 NS094545

Funded by: FundRef http://dx.doi.org/10.13039/501100000925, National Health and Medical Research Council;

Award ID: APP1105792

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ScienceOpen disciplines: Neurosciences

Keywords: drosophila visual system,layers,columns,columnar restriction,layer specificity,synaptic specificity

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ScienceOpen disciplines: Neurosciences

Keywords: drosophila visual system, layers, columns, columnar restriction, layer specificity, synaptic specificity

Strategies for assembling columns and layers in the Drosophila visual system

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Most cited references 98

An olfactory sensory map in the fly brain.

Design principles of insect and vertebrate visual systems.

The cortical column: a structure without a function.

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