Tectal-derived Interneurons Contribute to Phasic and Tonic Inhibition in the Visual Thalamus

Overview

Journal Nat Commun

Specialty Biology

Date 2016 Dec 9

PMID 27929058

Citations 31

Authors

Polona Jager

Zhiwen Ye

Xiao Yu

Laskaro Zagoraiou

Hong-Ting Prekop

Juha Partanen

Thomas M Jessell

William Wisden

Stephen G Brickley

Alessio Delogu

Affiliations

Soon will be listed here.

Abstract

The release of GABA from local interneurons in the dorsal lateral geniculate nucleus (dLGN-INs) provides inhibitory control during visual processing within the thalamus. It is commonly assumed that this important class of interneurons originates from within the thalamic complex, but we now show that during early postnatal development Sox14/Otx2-expressing precursor cells migrate from the dorsal midbrain to generate dLGN-INs. The unexpected extra-diencephalic origin of dLGN-INs sets them apart from GABAergic neurons of the reticular thalamic nucleus. Using optogenetics we show that at increased firing rates tectal-derived dLGN-INs generate a powerful form of tonic inhibition that regulates the gain of thalamic relay neurons through recruitment of extrasynaptic high-affinity GABA receptors. Therefore, by revising the conventional view of thalamic interneuron ontogeny we demonstrate how a previously unappreciated mesencephalic population controls thalamic relay neuron excitability.

Citing Articles

Development of the early fetal human thalamus: from a protomap to emergent thalamic nuclei.

Alhesain M, Alzubi A, Sankar N, Smith C, Kerwin J, Laws R Front Neuroanat. 2025; 19:1530236.

PMID: 39990522 PMC: 11842364. DOI: 10.3389/fnana.2025.1530236.

Retinal Input Is Required for the Maintenance of Neuronal Laminae in the Ventrolateral Geniculate Nucleus.

Stebbins K, Somaiya R, Sabbagh U, Khaksar P, Liang Y, Su J eNeuro. 2024; 11(9).

PMID: 39160068 PMC: 11373735. DOI: 10.1523/ENEURO.0022-24.2024.

A novel developmental critical period of orexinergic signaling in the primary visual thalamus.

Sanetra A, Jeczmien-Lazur J, Pradel K, Klich J, Palus-Chramiec K, Janik M iScience. 2024; 27(7):110352.

PMID: 39055917 PMC: 11269934. DOI: 10.1016/j.isci.2024.110352.

A molecular and cellular perspective on human brain evolution and tempo.

Lindhout F, Krienen F, Pollard K, Lancaster M Nature. 2024; 630(8017):596-608.

PMID: 38898293 DOI: 10.1038/s41586-024-07521-x.

The type of inhibition provided by thalamic interneurons alters the input selectivity of thalamocortical neurons.

Djama D, Zirpel F, Ye Z, Moore G, Chue C, Edge C Curr Res Neurobiol. 2024; 6:100130.

PMID: 38694514 PMC: 11061260. DOI: 10.1016/j.crneur.2024.100130.

References

Chen C, Regehr W . Developmental remodeling of the retinogeniculate synapse. Neuron. 2001; 28(3):955-66. DOI: 10.1016/s0896-6273(00)00166-5. View

Akerman C, Cline H . Refining the roles of GABAergic signaling during neural circuit formation. Trends Neurosci. 2007; 30(8):382-9. DOI: 10.1016/j.tins.2007.06.002. View

Golding B, Pouchelon G, Bellone C, Murthy S, Di Nardo A, Govindan S . Retinal input directs the recruitment of inhibitory interneurons into thalamic visual circuits. Neuron. 2014; 81(5):1057-1069. DOI: 10.1016/j.neuron.2014.01.032. View

Wafford K, van Niel M, Ma Q, Horridge E, Herd M, Peden D . Novel compounds selectively enhance delta subunit containing GABA A receptors and increase tonic currents in thalamus. Neuropharmacology. 2008; 56(1):182-9. DOI: 10.1016/j.neuropharm.2008.08.004. View

Puelles L, Rubenstein J . Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci. 2003; 26(9):469-76. DOI: 10.1016/S0166-2236(03)00234-0. View

Steriade M . Sleep, epilepsy and thalamic reticular inhibitory neurons. Trends Neurosci. 2005; 28(6):317-24. DOI: 10.1016/j.tins.2005.03.007. View

Fagiolini M, Hensch T . Inhibitory threshold for critical-period activation in primary visual cortex. Nature. 2000; 404(6774):183-6. DOI: 10.1038/35004582. View

McAlonan K, Cavanaugh J, Wurtz R . Guarding the gateway to cortex with attention in visual thalamus. Nature. 2008; 456(7220):391-4. PMC: 2713033. DOI: 10.1038/nature07382. View

Williams S, Turner J, Anderson C, Crunelli V . Electrophysiological and morphological properties of interneurones in the rat dorsal lateral geniculate nucleus in vitro. J Physiol. 1996; 490 ( Pt 1):129-47. PMC: 1158652. DOI: 10.1113/jphysiol.1996.sp021131. View

10.

Houser C, Vaughn J, Barber R, Roberts E . GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res. 1980; 200(2):341-54. DOI: 10.1016/0006-8993(80)90925-7. View

11.

Simon D, Prusky G, OLeary D, Constantine-Paton M . N-methyl-D-aspartate receptor antagonists disrupt the formation of a mammalian neural map. Proc Natl Acad Sci U S A. 1992; 89(22):10593-7. PMC: 50387. DOI: 10.1073/pnas.89.22.10593. View

12.

Fishell G, Rudy B . Mechanisms of inhibition within the telencephalon: "where the wild things are". Annu Rev Neurosci. 2011; 34:535-67. PMC: 3556485. DOI: 10.1146/annurev-neuro-061010-113717. View

13.

Hunt C, Pang D, Jones E . Distribution and density of GABA cells in intralaminar and adjacent nuclei of monkey thalamus. Neuroscience. 1991; 43(1):185-96. DOI: 10.1016/0306-4522(91)90426-o. View

14.

Song H, Lee B, Pyun D, Guimera J, Son Y, Yoon J . Ascl1 and Helt act combinatorially to specify thalamic neuronal identity by repressing Dlxs activation. Dev Biol. 2014; 398(2):280-91. DOI: 10.1016/j.ydbio.2014.12.003. View

15.

Jeong Y, Dolson D, Waclaw R, Matise M, Sussel L, Campbell K . Spatial and temporal requirements for sonic hedgehog in the regulation of thalamic interneuron identity. Development. 2011; 138(3):531-41. PMC: 3014638. DOI: 10.1242/dev.058917. View

16.

Herd M, Brown A, Lambert J, Belelli D . Extrasynaptic GABA(A) receptors couple presynaptic activity to postsynaptic inhibition in the somatosensory thalamus. J Neurosci. 2013; 33(37):14850-68. PMC: 6705167. DOI: 10.1523/JNEUROSCI.1174-13.2013. View

17.

Ralston 3rd H . Evidence for presynaptic dendrites and a proposal for their mechanism of action. Nature. 1971; 230(5296):585-7. DOI: 10.1038/230585a0. View

18.

Huang Z . Molecular regulation of neuronal migration during neocortical development. Mol Cell Neurosci. 2009; 42(1):11-22. DOI: 10.1016/j.mcn.2009.06.003. View

19.

Kataoka A, Shimogori T . Fgf8 controls regional identity in the developing thalamus. Development. 2008; 135(17):2873-81. DOI: 10.1242/dev.021618. View

20.

Altman J, Bayer S . Development of the rat thalamus: VI. The posterior lobule of the thalamic neuroepithelium and the time and site of origin and settling pattern of neurons of the lateral geniculate and lateral posterior nuclei. J Comp Neurol. 1989; 284(4):581-601. DOI: 10.1002/cne.902840407. View