Stochastic Interaction Between Neural Activity and Molecular Cues in the Formation of Topographic Maps

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2015 Sep 25

PMID 26402608

Citations 19

Authors

Melinda T Owens

David A Feldheim

Michael P Stryker

Jason W Triplett

Affiliations

Soon will be listed here.

Abstract

Topographic maps in visual processing areas maintain the spatial order of the visual world. Molecular cues and neuronal activity both play critical roles in map formation, but their interaction remains unclear. Here, we demonstrate that when molecular- and activity-dependent cues are rendered nearly equal in force, they drive topographic mapping stochastically. The functional and anatomical representation of azimuth in the superior colliculus of heterozygous Islet2-EphA3 knockin (Isl2(EphA3/+)) mice is variable: maps may be single, duplicated, or a combination of the two. This heterogeneity is not due to genetic differences, since map organizations in individual mutant animals often differ between colliculi. Disruption of spontaneous waves of retinal activity resulted in uniform map organization in Isl2(EphA3/+) mice, demonstrating that correlated spontaneous activity is required for map heterogeneity. Computational modeling replicates this heterogeneity, revealing that molecular- and activity-dependent forces interact simultaneously and stochastically during topographic map formation.

Citing Articles

Reanalysis of EphA3 Knock-In Double Maps in Mouse Suggests That Stochasticity in Topographic Map Formation Acts at the Retina Rather than between Competing Mechanisms at the Colliculus.

Willshaw D, Gale N eNeuro. 2023; 10(11).

PMID: 37852780 PMC: 10668230. DOI: 10.1523/ENEURO.0135-23.2023.

Postsynaptic NMDA Receptor Expression Is Required for Visual Corticocollicular Projection Refinement in the Mouse Superior Colliculus.

Johnson K, Harel L, Triplett J J Neurosci. 2023; 43(8):1310-1320.

PMID: 36717228 PMC: 9987568. DOI: 10.1523/JNEUROSCI.1473-22.2022.

Segregation of Multimodal Inputs Into Discrete Midbrain Compartments During an Early Critical Period.

Weakley J, Kavusak E, Carroll J, Gabriele M Front Neural Circuits. 2022; 16:882485.

PMID: 35463204 PMC: 9021614. DOI: 10.3389/fncir.2022.882485.

Wiring subcortical image-forming centers: Topography, laminar targeting, and map alignment.

Johnson K, Triplett J Curr Top Dev Biol. 2021; 142:283-317.

PMID: 33706920 PMC: 9116472. DOI: 10.1016/bs.ctdb.2020.10.004.

New insights on the modeling of the molecular mechanisms underlying neural maps alignment in the midbrain.

Savier E, Dunbar J, Cheung K, Reber M Elife. 2020; 9.

PMID: 32996883 PMC: 7527235. DOI: 10.7554/eLife.59754.

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