Compartmental function and modulation of the striatum

Prager, Eric M.; Plotkin, Joshua L.

doi:10.1002/jnr.24522

Cited by 40 publications

(26 citation statements)

References 138 publications

(282 reference statements)

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“…Consequently, these striosomal SPNs are more susceptible to receiving early inputs from cortex, thalamus and SNc. Indeed, early-forming dopaminergic innervation of the striatum occurs first in the patch compartment before its expansion into the matrix (Edley and Herkenham, 1984;Fishell and van der Kooy, 1989;Graybiel, 1984;Prager and Plotkin, 2019). Similarly, early cortical and thalamic innervation labeling by Vglut1 and Vglut2, respectively, appear to match with the striosomes' location (Nakamura et al, 2005).…”

Section: ) Postnatal Maturation Of the Striatal Circuitmentioning

confidence: 97%

Striatal Circuit Development and Its Alterations in Huntington’s Disease

Lebouc¹,

Richard²,

Garret³

et al. 2020

Preprint

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Huntington's disease (HD) is an inherited neurodegenerative disorder that usually starts during midlife with progressive alterations of motor and cognitive functions. The disease is caused by a CAG repeat expansion within the huntingtin gene leading to severe striatal neurodegeneration. Recent studies conducted on pre-HD children highlight early striatal developmental alterations starting as soon as 6 years old, the earliest age assessed. These findings, in line with data from mouse models of HD, raise the question of when during development do the first disease-related striatal alterations emerge or whether they contribute to the later appearance of the neurodegenerative features of the disease. In this review we will describe the different stages of striatal network development and then discuss recent evidence for its alterations in rodent models of the disease. We argue that a better understanding of the striatum’s development should help in assessing aberrant neurodevelopmental processes linked to the HD mutation.

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Section: ) Postnatal Maturation Of the Striatal Circuitmentioning

confidence: 97%

Striatal Circuit Development and Its Alterations in Huntington’s Disease

Lebouc¹,

Richard²,

Garret³

et al. 2020

Preprint

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“…In rodents, for example, patches are involved in cost-benefit trade-off decisions (Friedman et al, 2015 ), and in humans, striatal patches play a certain role in cognitive control (Beste et al, 2018 ). Also, the neurons inside the two compartments differ, for example in their synaptic connectivity and neuromodulation (for a recent review, see Prager and Plotkin, 2019 ). Importantly, the patch and matrix compartmentalization can be found in all anatomical domains of the striatum.…”

Section: Striatal Compartmentsmentioning

confidence: 99%

“…It is also known that dSPN axons do not exclusively terminate in the SNr, but also make very plastic connections in the GPe (Cazorla et al, 2012 ; Cui et al, 2021 ). Another open question is whether patches are equally composed dSPNs and iSPNs, or preferentially enriched with one type (see Prager and Plotkin, 2019 ). Along this line, it has been noted that the most caudal part of the striatum (corresponding to the fourth anatomical division mentioned above) is largely devoid of iSPNs (Gangarossa et al, 2013 ).…”

Section: Spiny Projection Neuron Populationsmentioning

confidence: 99%

Striatal Control of Movement: A Role for New Neuronal (Sub-) Populations?

Fieblinger

2021

Front. Hum. Neurosci.

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The striatum is a very heterogenous brain area, composed of different domains and compartments, albeit lacking visible anatomical demarcations. Two populations of striatal spiny projection neurons (SPNs) build the so-called direct and indirect pathway of the basal ganglia, whose coordinated activity is essential to control locomotion. Dysfunction of striatal SPNs is part of many movement disorders, such as Parkinson’s disease (PD) and L-DOPA-induced dyskinesia. In this mini review article, I will highlight recent studies utilizing single-cell RNA sequencing to investigate the transcriptional profiles of striatal neurons. These studies discover that SPNs carry a transcriptional signature, indicating both their anatomical location and compartmental identity. Furthermore, the transcriptional profiles reveal the existence of additional distinct neuronal populations and previously unknown SPN sub-populations. In a parallel development, studies in rodent models of PD and L-DOPA-induced dyskinesia (LID) report that direct pathway SPNs do not react uniformly to L-DOPA therapy, and that only a subset of these neurons is underlying the development of abnormal movements. Together, these studies demonstrate a new level of cellular complexity for striatal (dys-) function and locomotor control.

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“…Amongst the most commonly used phenotypic markers in the adult are the striosomal mu opiate receptor (MOR) encoded by Oprm1, and the matrix calbindin, encoded by Calb1 2 . Striosome and matrix neurons also differ in their electrophysiologic properties 26 and further mediate functions based on their connectivity 27 . The striosome compartment has been specifically associated with stimulus-response learning 28 and perhaps stereotypy 29,30 .…”

Section: Introductionmentioning

confidence: 99%

“…Replication of striatal development and function in vitro requires communication between compartments 26 , and only a handful of TFs and signaling systems have been shown to define striosome/matrix compartmentation, e.g. Ikaros--1, retinoids, and Nr4a1 22,36,37,42--45 .…”

Section: Introductionmentioning

confidence: 99%

Transcriptional and epigenetic characterization of early striosomes identifies Foxf2 and Olig2 as factors required for development of striatal compartmentation and neuronal phenotypic differentiation

Cirnaru

Song

Tshilenge

et al. 2020

Preprint

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The basal ganglia, best known for processing information required for multiple aspects of movement, is also part of a network which regulates reward and cognition. The major output nucleus of the basal ganglia is the striatum, and its functions are dependent on neuronal compartmentation, including striosomes and matrix, which are selectively affected in disease.Striatal projection neurons are GABAergic medium spiny neurons (MSNs), all of which share basic molecular signatures but are subtyped by selective expression of receptors, neuropeptides, and other gene families. Neurogenesis of the striosome and matrix occurs in separate waves, but the factors regulating terminal neuronal differentiation following migration are largely unidentified.We performed RNA--and ATAC--seq on sorted murine striosome and matrix cells at postnatal day 3. Focusing on the striosomal compartment, we validated the localization and role of transcription factors and their regulator(s), previously not known to be associated with striatal development, including Irx1, Foxf2, Olig2 and Stat1/2. In addition, we validated the enhancer function of a striosome--specific open chromatin region located 15Kb downstream of the Olig2 gene. These data and data bases provide novel tools to dissect and manipulate the networks regulating MSN compartmentation and differentiation and thus provide new approaches to establishing MSN subtypes from human iPSCs for disease modeling and drug discovery.

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Compartmental function and modulation of the striatum

Cited by 40 publications

References 138 publications

Striatal Circuit Development and Its Alterations in Huntington’s Disease

Striatal Circuit Development and Its Alterations in Huntington’s Disease

Striatal Control of Movement: A Role for New Neuronal (Sub-) Populations?

Transcriptional and epigenetic characterization of early striosomes identifies Foxf2 and Olig2 as factors required for development of striatal compartmentation and neuronal phenotypic differentiation

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