Tectal-derived interneurons contribute to phasic and tonic inhibition in the visual thalamus

Jager, Polona; Z, Ye; Yu, Xiao; Zagoraiou, Laskaro; Prekop, Hong-Ting; Partanen, Juha; Jessell, Thomas M.; Wisden, William; Brickley, Stephen G.; Delogu, Alessio

doi:10.1038/ncomms13579

Cited by 55 publications

(105 citation statements)

References 67 publications

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“…The arrival of these interneurons occurs postnatally, after retinal inputs have targeted dLGN, formed immature connections, and begun to undergo activity-dependent refinement (Jones & Rubenstein, 2004; Singh et al, 2012; Golding et al, 2014; Jager et al, 2016). The precise origin of these interneurons is currently under debate, with studies suggesting they arise from a rostral progenitor domain within the thalamus (i.e., prosomer 3) or from tectum (Virolainen et al, 2012; Golding et al, 2014; Jager et al, 2016). Evidence is also emerging that dLGN interneurons are not a homogeneous population in mice, and can instead be divided into at least two classes based on soma size, membrane capacitance, and neuronal nitric oxide synthase (nNOS) expression (Leist et al, 2016).…”

Section: Cytoarchitectural Organization Of Retinorecipient Thalamic Nmentioning

confidence: 99%

Not a one-trick pony: Diverse connectivity and functions of the rodent lateral geniculate complex

2017

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Often mislabeled as a simple relay of sensory information, the thalamus is a complicated structure with diverse functions. This diversity is exemplified by roles visual thalamus plays in processing and transmitting light-derived stimuli. Such light-derived signals are transmitted to the thalamus by retinal ganglion cells (RGCs), the sole projection neurons of the retina. Axons from RGCs innervate more than ten distinct nuclei within thalamus, including those of the lateral geniculate complex. Nuclei within the lateral geniculate complex of nocturnal rodents, which include the dorsal lateral geniculate nucleus (dLGN), ventral lateral geniculate nucleus (vLGN), and intergeniculate leaflet (IGL), are each densely innervated by retinal projections, yet, exhibit distinct cytoarchitecture and connectivity. These features suggest that each nucleus within this complex plays a unique role in processing and transmitting light-derived signals. Here, we review the diverse cytoarchitecture and connectivity of these nuclei in nocturnal rodents, in an effort to highlight roles for dLGN in vision and for vLGN and IGL in visuomotor, vestibular, ocular, and circadian function.

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Section: Cytoarchitectural Organization Of Retinorecipient Thalamic Nmentioning

confidence: 99%

Not a one-trick pony: Diverse connectivity and functions of the rodent lateral geniculate complex

2017

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“…How could these differences arise as part of species-specific ontogenesis of thalamic interneurons? We have previously shown that in the mouse, interneurons in the FO visual thalamus, the dorsal lateral geniculate nucleus (dLGN), originate in the midbrain from an En1 + Gata2 + Otx2 + Sox14 + lineage (Jager et al, 2016). On the other hand, earlier work in humans has suggested the Dlx1/2 -expressing ganglionic eminences (GE) in the telencephalon as the source of interneurons for the HO thalamic nuclei-the mediodorsal nucleus and the pulvinar (Rakić and Sidman, 1969; Letinić and Kostović, 1997; Letinic and Rakic, 2001).…”

Section: Introductionmentioning

confidence: 99%

Dual midbrain and forebrain origins of thalamic inhibitory interneurons

Jager

Moore

Calpin

et al. 2019

Preprint

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12The proportion and distribution of local inhibitory neurons (interneurons) in the thalamus 13 varies widely across mammals. This is reflected in the structure of thalamic local circuits, 14which is more complex in primates compared to smaller-brained mammals like rodents. 15An increase in the number of thalamic interneurons could arise from addition of novel 16 interneuron types or from elaboration of a plesiomorphic ontogenetic program, common to 17 all mammals. The former has been proposed for the human brain, with migration of 18 interneurons from the ventral telencephalon into higher order thalamus as one of its unique 19 features (Letinic and Rakic, 2001). 20Here, we identify a larger than expected complexity and distribution of interneurons across 21 the mouse thalamus. All thalamic interneurons can be traced back to two developmental 22 programs: one specified in the midbrain and the other in the forebrain. Interneurons migrate 23 to functionally distinct thalamic nuclei, where the midbrain-derived cells populate the sensory 24 thalamus, and forebrain-generated interneurons only the higher order regions. The latter 25 interneuron type may be homologous to the one previously considered to be human-specific, 26while we also observe that markers for the midbrain-born class are abundantly expressed in 27 the primate thalamus. These data therefore point to a shared ontogenetic organization of 28 thalamic interneurons across mammals. 29 30

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“…However, spillover of GABA onto these δ subunit-containing extrasynaptic GABA A Rs occurs onto VB relay neurons in response to stimulated burst firing of the nRT (Herd et al, 2013). Similarly, we recently reported that DS-2 application resulted in a slowing of ChR2-evoked IPSCs that are driven by optogenetic GABA release from dLGN interneurons (Jager et al, 2016). These results are not contradictory if the magnitude of the GABA transient associated with spontaneous release were much less than the GABA transient associated with evoked release.…”

Section: Discussionmentioning

confidence: 55%

Fast and Slow Inhibition in the Visual Thalamus Is Influenced by Allocating GABAA Receptors with Different γ Subunits

Houston

et al. 2017

Front. Cell. Neurosci.

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Cell-type specific differences in the kinetics of inhibitory postsynaptic conductance changes (IPSCs) are believed to impact upon network dynamics throughout the brain. Much attention has focused on how GABAA receptor (GABAAR) α and β subunit diversity will influence IPSC kinetics, but less is known about the influence of the γ subunit. We have examined whether GABAAR γ subunit heterogeneity influences IPSC properties in the thalamus. The γ2 subunit gene was deleted from GABAARs selectively in the dorsal lateral geniculate nucleus (dLGN). The removal of the γ2 subunit from the dLGN reduced the overall spontaneous IPSC (sIPSC) frequency across all relay cells and produced an absence of IPSCs in a subset of relay neurons. The remaining slower IPSCs were both insensitive to diazepam and zinc indicating the absence of the γ2 subunit. Because these slower IPSCs were potentiated by methyl-6,7-dimethoxy-4-ethyl-β-carboline-3-carboxylate (DMCM), we propose these IPSCs involve γ1 subunit-containing GABAAR activation. Therefore, γ subunit heterogeneity appears to influence the kinetics of GABAAR-mediated synaptic transmission in the visual thalamus in a cell-selective manner. We suggest that activation of γ1 subunit-containing GABAARs give rise to slower IPSCs in general, while faster IPSCs tend to be mediated by γ2 subunit-containing GABAARs.

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Tectal-derived interneurons contribute to phasic and tonic inhibition in the visual thalamus

Cited by 55 publications

References 67 publications

Not a one-trick pony: Diverse connectivity and functions of the rodent lateral geniculate complex

Not a one-trick pony: Diverse connectivity and functions of the rodent lateral geniculate complex

Dual midbrain and forebrain origins of thalamic inhibitory interneurons

Fast and Slow Inhibition in the Visual Thalamus Is Influenced by Allocating GABAA Receptors with Different γ Subunits

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