Development of asymmetric inhibition underlying direction selectivity in the retina
- PMID: 21131947
- PMCID: PMC3974627
- DOI: 10.1038/nature09600
Development of asymmetric inhibition underlying direction selectivity in the retina
Abstract
Establishing precise synaptic connections is crucial to the development of functional neural circuits. The direction-selective circuit in the retina relies upon highly selective wiring of inhibitory inputs from starburst amacrine cells (SACs) onto four subtypes of ON-OFF direction-selective ganglion cells (DSGCs), each preferring motion in one of four cardinal directions. It has been reported in rabbit that the SACs on the 'null' sides of DSGCs form functional GABA (γ-aminobutyric acid)-mediated synapses, whereas those on the preferred sides do not. However, it is not known how the asymmetric wiring between SACs and DSGCs is established during development. Here we report that in transgenic mice with cell-type-specific labelling, the synaptic connections from SACs to DSGCs were of equal strength during the first postnatal week, regardless of whether the SAC was located on the preferred or null side of the DSGC. However, by the end of the second postnatal week, the strength of the synapses made from SACs on the null side of a DSGC significantly increased whereas those made from SACs located on the preferred side remained constant. Blocking retinal activity by intraocular injections of muscimol or gabazine during this period did not alter the development of direction selectivity. Hence, the asymmetric inhibition between the SACs and DSGCs is achieved by a developmental program that specifically strengthens the GABA-mediated inputs from SACs located on the null side, in a manner not dependent on neural activity.
Conflict of interest statement
The authors declare no competing financial interests.
Figures




Comment in
-
Developmental neuroscience: asymmetric inhibition.Nat Rev Neurosci. 2011 Feb;12(2):64. doi: 10.1038/nrn2982. Nat Rev Neurosci. 2011. PMID: 21309095 No abstract available.
Similar articles
-
An Asymmetric Increase in Inhibitory Synapse Number Underlies the Development of a Direction Selective Circuit in the Retina.J Neurosci. 2015 Jun 24;35(25):9281-6. doi: 10.1523/JNEUROSCI.0670-15.2015. J Neurosci. 2015. PMID: 26109653 Free PMC article.
-
Symmetric synaptic patterns between starburst amacrine cells and direction selective ganglion cells in the rabbit retina.J Comp Neurol. 2008 May 1;508(1):175-83. doi: 10.1002/cne.21677. J Comp Neurol. 2008. PMID: 18306383
-
Excitatory synaptic inputs to mouse on-off direction-selective retinal ganglion cells lack direction tuning.J Neurosci. 2014 Mar 12;34(11):3976-81. doi: 10.1523/JNEUROSCI.5017-13.2014. J Neurosci. 2014. PMID: 24623775 Free PMC article.
-
Synaptic physiology of direction selectivity in the retina.J Physiol. 2008 Sep 15;586(18):4371-6. doi: 10.1113/jphysiol.2008.159020. Epub 2008 Jul 10. J Physiol. 2008. PMID: 18617561 Free PMC article. Review.
-
New directions in retinal research.Trends Neurosci. 2003 Jul;26(7):379-85. doi: 10.1016/S0166-2236(03)00167-X. Trends Neurosci. 2003. PMID: 12850434 Review.
Cited by
-
Spatial relationships between GABAergic and glutamatergic synapses on the dendrites of distinct types of mouse retinal ganglion cells across development.PLoS One. 2013 Jul 26;8(7):e69612. doi: 10.1371/journal.pone.0069612. Print 2013. PLoS One. 2013. PMID: 23922756 Free PMC article.
-
Conserved circuits for direction selectivity in the primate retina.Curr Biol. 2022 Jun 6;32(11):2529-2538.e4. doi: 10.1016/j.cub.2022.04.056. Epub 2022 May 18. Curr Biol. 2022. PMID: 35588744 Free PMC article.
-
Asymmetric connections with starburst amacrine cells underlie the upward motion selectivity of J-type retinal ganglion cells.PLoS Biol. 2023 Sep 18;21(9):e3002301. doi: 10.1371/journal.pbio.3002301. eCollection 2023 Sep. PLoS Biol. 2023. PMID: 37721959 Free PMC article.
-
Stimulus-dependent engagement of neural mechanisms for reliable motion detection in the mouse retina.J Neurophysiol. 2018 Sep 1;120(3):1153-1161. doi: 10.1152/jn.00716.2017. Epub 2018 Jun 13. J Neurophysiol. 2018. PMID: 29897862 Free PMC article. Review.
-
Activity-Dependent Synaptic Refinement: New Insights from Drosophila.Front Syst Neurosci. 2017 Apr 21;11:23. doi: 10.3389/fnsys.2017.00023. eCollection 2017. Front Syst Neurosci. 2017. PMID: 28484377 Free PMC article. Review.
References
-
- Euler T, Detwiler PB, Denk W. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature. 2002;418:845–852. - PubMed
-
- Demb JB. Cellular mechanisms for direction selectivity in the retina. Neuron. 2007;55:179–186. - PubMed
-
- Fried SI, Munch TA, Werblin FS. Mechanisms and circuitry underlying directional selectivity in the retina. Nature. 2002;420:411–414. - PubMed
Publication types
MeSH terms
Substances
Grants and funding
LinkOut - more resources
Full Text Sources
Molecular Biology Databases
Miscellaneous