Selective neuronal expression of the SoxE factor, Sox8, in direct pathway striatal projection neurons of the developing mouse brain

Merchan-Sala, Paloma; Nardini, Diana; Waclaw, Ronald R.; Campbell, Kenneth

doi:10.1002/cne.24232

Cited by 19 publications

(11 citation statements)

References 64 publications

(196 reference statements)

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“…Moreover, we show that many of the properties of mature D1 and D2 SPNs are already apparent by the first and second postnatal weeks, which is thought to be a period prior to much exploratory motor behaviour (Dehorter et al 2011) or exposure to structured input from the sensory periphery (Tobach et al 1971;Krug et al 2001;Akerman et al 2002;Ko et al 2013;Mowery et al 2015Mowery et al , 2016Mowery et al , 2017. This is consistent with the idea that neuronal specification can occur early in development (Lobo et al 2006(Lobo et al , 2008Arlotta et al 2008;Ehrman et al 2013;Lu et al 2014;Zhang et al 2016;Merchan-Sala et al 2017;Kelly et al 2018;Tinterri et al 2018;Xu et al 2018) with further postnatal development guided by, for example, neural activity (Zhang & Poo, 2001;Kozorovitskiy et al 2012;Peixoto et al 2016) and neuromodulation (Kozorovitskiy et al 2015;Lieberman et al 2018). Future work will be able to clarify the precise interaction of these factors during striatal development as well as their differential involvement in neurodevelopmental disorders (Graybiel & Rauch, 2000;Del Campo et al 2011;Langen et al 2011;McNaught & Mink, 2011;Shepherd, 2013;Albin, 2018).…”

Section: Local Inhibitory Synaptic Connections Between D1 and D2 Spnssupporting

confidence: 89%

Dynamic postnatal development of the cellular and circuit properties of striatal D1 and D2 spiny projection neurons

Krajeski

Macey-Dare

Heusden

et al. 2019

The Journal of Physiology

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Key points Imbalances in the activity of the D1‐expressing direct pathway and D2‐expressing indirect pathway striatal projection neurons (SPNs) are thought to contribute to many basal ganglia disorders, including early‐onset neurodevelopmental disorders such as obsessive–compulsive disorder, attention deficit hyperactivity disorder and Tourette's syndrome. This study provides the first detailed quantitative investigation of development of D1 and D2 SPNs, including their cellular properties and connectivity within neural circuits, during the first postnatal weeks. This period is highly dynamic with many properties changing, but it is possible to make three main observations: many aspects of D1 and D2 SPNs progressively mature in parallel; there are notable exceptions when they diverge; and many of the defining properties of mature striatal SPNs and circuits are already established by the first and second postnatal weeks, suggesting guidance through intrinsic developmental programmes. These findings provide an experimental framework for future studies of striatal development in both health and disease. Abstract Many basal ganglia neurodevelopmental disorders are thought to result from imbalances in the activity of the D1‐expressing direct pathway and D2‐expressing indirect pathway striatal projection neurons (SPNs). Insight into these disorders is reliant on our understanding of normal D1 and D2 SPN development. Here we provide the first detailed study and quantification of the striatal cellular and circuit changes occurring for both D1 and D2 SPNs in the first postnatal weeks using in vitro whole‐cell patch‐clamp electrophysiology. Characterization of their intrinsic electrophysiological and morphological properties, the excitatory long‐range inputs coming from cortex and thalamus, as well their local gap junction and inhibitory synaptic connections reveals this period to be highly dynamic with numerous properties changing. However it is possible to make three main observations. Firstly, many aspects of SPNs mature in parallel, including intrinsic membrane properties, increases in dendritic arbours and spine densities, general synaptic inputs and expression of specific glutamate receptors. Secondly, there are notable exceptions, including a transient stronger thalamic innervation of D2 SPNs and stronger cortical NMDA receptor‐mediated inputs to D1 SPNs, both in the second postnatal week. Thirdly, many of the defining properties of mature D1 and D2 SPNs and striatal circuits are already established by the first and second postnatal weeks, including different electrophysiological properties as well as biased local inhibitory connections between SPNs, suggesting this is guided through intrinsic developmental programmes. Together these findings provide an experimental framework for future studies of D1 and D2 SPN development in health and disease.

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Section: Local Inhibitory Synaptic Connections Between D1 and D2 Spnssupporting

confidence: 89%

Dynamic postnatal development of the cellular and circuit properties of striatal D1 and D2 spiny projection neurons

Krajeski

Macey-Dare

Heusden

et al. 2019

The Journal of Physiology

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“…Ascl1 + /Dlx1/2 - and Ascl1 + /Dlx1/2 + progenitors are inferred to emerge in a sequence (Martín-Ibáñez et al, 2012) and to interact through Notch-mediated lateral inhibition to coordinate proliferation and neurogenesis (Mason, 2005). The orderly production of early- and late-born SPNs is also regulated in part through downstream transcription factors (e.g., Ebf1, Isl1, Sp9) (Zhang et al, 2016; Merchan-Sala., 2017). Here, by combining cellular resolution genetic fate mapping and neuronal birth dating, we identify distinct progenitor types and trace their lineage progression to their neuronal progenies and SPN types.…”

Section: Discussionmentioning

confidence: 99%

Radial Glial Lineage Progression and Differential Intermediate Progenitor Amplification Underlie Striatal Compartments and Circuit Organization

Kelly

Raudales

et al. 2018

Neuron

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The circuitry of the striatum is characterized by two organizational plans: the division into striosome and matrix compartments, thought to mediate evaluation and action, and the direct and indirect pathways, thought to promote or suppress behavior. The developmental origins of these organizations and their developmental relationships are unknown, leaving a conceptual gap in understanding the cortico-basal ganglia system. Through genetic fate mapping, we demonstrate that striosome-matrix compartmentalization arises from a lineage program embedded in lateral ganglionic eminence radial glial progenitors mediating neurogenesis through two distinct types of intermediate progenitors (IPs). The early phase of this program produces striosomal spiny projection neurons (SPNs) through fate-restricted apical IPs (aIPs) with limited capacity; the late phase produces matrix SPNs through fate-restricted basal IPs (bIPs) with expanded capacity. Notably, direct and indirect pathway SPNs arise within both aIP and bIP pools, suggesting that striosome-matrix architecture is the fundamental organizational plan of basal ganglia circuitry.

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“…Although these GABAergic neurons share many properties, they have some distinct molecular properties and differentially contribute to distinct circuits (e.g. direct and indirect pathway) (Lobo et al, 2006;Heiman et al, 2008;Gerfen and Surmeier, 2011;Ena et al, 2013;Gokce et al, 2016;Merchan-Sala et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

SP8 and SP9 coordinately promote D2-type medium spiny neuron production by activating Six3 expression

Liang

Song

et al. 2018

Development

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Dopamine receptor DRD1-expressing medium spiny neurons (D1 MSNs) and dopamine receptor DRD2-expressing medium spiny neurons (D2 MSNs) are the principal projection neurons in the striatum, which is divided into dorsal striatum (caudate nucleus and putamen) and ventral striatum (nucleus accumbens and olfactory tubercle). Progenitors of these neurons arise in the lateral ganglionic eminence (LGE). Using conditional deletion, we show that mice lacking the transcription factor genes and lose virtually all D2 MSNs as a result of reduced neurogenesis in the LGE, whereas D1 MSNs are largely unaffected. SP8 and SP9 together drive expression of the transcription factor in a spatially restricted domain of the LGE subventricular zone. Conditional deletion of also prevents the formation of most D2 MSNs, phenocopying the mutants. Finally, ChIP-Seq reveals that SP9 directly binds to the promoter and a putative enhancer of Thus, this study defines components of a transcription pathway in a regionally restricted LGE progenitor domain that selectively drives the generation of D2 MSNs.

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Selective neuronal expression of the SoxE factor, Sox8, in direct pathway striatal projection neurons of the developing mouse brain

Cited by 19 publications

References 64 publications

Dynamic postnatal development of the cellular and circuit properties of striatal D1 and D2 spiny projection neurons

Dynamic postnatal development of the cellular and circuit properties of striatal D1 and D2 spiny projection neurons

Radial Glial Lineage Progression and Differential Intermediate Progenitor Amplification Underlie Striatal Compartments and Circuit Organization

SP8 and SP9 coordinately promote D2-type medium spiny neuron production by activating Six3 expression

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