Active intermixing of indirect and direct neurons builds the striatal mosaic

Tinterri, Andrea; Menardy, Fabien; Diana, Marco A.; Lokmane, Ludmilla; Keita, Maryama; Coulpier, Fanny; Lemoine, Sophie; Mailhes, Caroline; Mathieu, Benjamin; Merchan-Sala, Paloma; Campbell, Kenneth; Győry, Ildikó; Grosschedl, Rudolf; Popa, Daniela; Garel, Sonia

doi:10.1038/s41467-018-07171-4

Cited by 33 publications

(28 citation statements)

References 70 publications

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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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“…These dopamine islands overlap with immature striosome compartments (Davis & Puhl, 2011;Graybiel, Pickel, Joh, Reis, & Ragsdale, 1981;Hagimoto et al, 2017;Miura, Saino-Saito, Masuda, Kobayashi, & Aosaki, 2007). The homogenous mix of dSPNs and iSPNs observed in adults is this result of a parallel, active intermixing of iSPNs (Tinterri et al, 2018). The homogenous mix of dSPNs and iSPNs observed in adults is this result of a parallel, active intermixing of iSPNs (Tinterri et al, 2018).…”

Section: Significancementioning

confidence: 96%

“…Striatal cells migrate from the lateral ganglionic eminence in two distinct waves, beginning around embryonic days 9.5-13.5 in rodents (Kelly et al, 2018;Tinterri et al, 2018). In fact, striosomes represent some of the oldest and earliest assembled circuit components in the striatum.…”

Section: E Ti Ology Of S Triatal Compartmental Org Aniz Ationmentioning

confidence: 99%

“…In fact, striosomes represent some of the oldest and earliest assembled circuit components in the striatum. Striatal cells migrate from the lateral ganglionic eminence in two distinct waves, beginning around embryonic days 9.5-13.5 in rodents (Kelly et al, 2018;Tinterri et al, 2018). The cells in the first wave ultimately correspond to striosomal SPNs and migrate to their destinations around the same time as the earliest cortical (Layer 6) neurons do, putting them in position to receive early corticostriatal as well as early thalamostriatal inputs (Fishell & van der Kooy, 1987;…”

Section: E Ti Ology Of S Triatal Compartmental Org Aniz Ationmentioning

confidence: 99%

“…Once positioned, striosome cells become mostly stationary and cluster together, whereas matrix cells continue to actively migrate in a multidirectional manner during late embryonic development (Hagimoto et al, 2017). The homogenous mix of dSPNs and iSPNs observed in adults is this result of a parallel, active intermixing of iSPNs (Tinterri et al, 2018). While striosomes form a continuous labyrinthine network that extends through the striatum (Graybiel & Ragsdale, 1978), it should be noted that recent work has discovered the presence of scattered SPNs within the matrix (termed "exo-patches") that are more similar to striosome than matrix SPNs in terms of genetic profiles, birth date, synaptic connectivity, and modulation by neuropeptides (Crittenden & Graybiel, 2011;Newman, Liu, & Graybiel, 2015;Smith et al, 2016).…”

Section: Dopaminergic Nigrostriatal Fibers Initially Form "Dopamine Imentioning

confidence: 99%

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Compartmental function and modulation of the striatum

Prager

Plotkin

2019

J of Neuroscience Research

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The striatum plays a central role in guiding numerous complex behaviors, ranging from motor control to action selection and reward learning. The diverse responsibilities of the striatum are reflected by the complexity of its organization. In this review, we will summarize what is currently known about the compartmental layout of the striatum, an organizational principle that is crucial for allowing the striatum to guide such a diverse array of behaviors. We will focus on the anatomical and functional properties of striosome (patch) and matrix compartments of the striatum, and how the engagement of these compartments is uniquely controlled by their afferents, intrinsic properties, and neuromodulation. We will give examples of how advances in technology have opened the door to functionally dissecting the striatum's compartmental design, and close by offering thoughts on the future and relevance for human disease.

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Neurogenesis in the basal ganglia

Rubenstein

Campbell

2020

Patterning and Cell Type Specification in the Developing CNS and PNS

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Active intermixing of indirect and direct neurons builds the striatal mosaic

Cited by 33 publications

References 70 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

Compartmental function and modulation of the striatum

Neurogenesis in the basal ganglia

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