Functional architecture of the mammalian striatum: Mouse vascular and striosome organization and their anatomic relationships

Breuer, O.; Lawhorn, Collene; Miller, Timothy M.; Smith, Diane; Brown, Lucy L.

doi:10.1016/j.neulet.2005.05.029

Cited by 17 publications

(18 citation statements)

References 42 publications

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“…Rows in the matrix have been identified in anterograde tracer studies from motor cortex [11] but these lamina also resemble striosomes innervation from deep layer prefrontal cortex developmentally and in the adult [48], indicating that the projections to the striosome and matrix may be arranged in parallel. Striosomes were also frequently observed in close proximity to and surrounding large blood vessels, as has previously been noted [49]. Layers were curved parallel to the corpus callosum in the dorsal and lateral regions of the rostral striatum but formed dorsomedial to ventrolateral layers in the ventral striatum (Fig.…”

Section: Resultssupporting

confidence: 73%

Nr4a1-eGFP Is a Marker of Striosome-Matrix Architecture, Development and Activity in the Extended Striatum

Davis

Puhl

2011

PLoS ONE

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Transgenic mice expressing eGFP under population specific promoters are widely used in neuroscience to identify specific subsets of neurons in situ and as sensors of neuronal activity in vivo. Mice expressing eGFP from a bacterial artificial chromosome under the Nr4a1 promoter have high expression within the basal ganglia, particularly within the striosome compartments and striatal-like regions of the extended amygdala (bed nucleus of the stria terminalis, striatal fundus, central amygdaloid nucleus and intercalated cells). Grossly, eGFP expression is inverse to the matrix marker calbindin 28K and overlaps with mu-opioid receptor immunoreactivity in the striatum. This pattern of expression is similar to Drd1, but not Drd2, dopamine receptor driven eGFP expression in structures targeted by medium spiny neuron afferents. Striosomal expression is strong developmentally where Nr4a1-eGFP expression overlaps with Drd1, TrkB, tyrosine hydroxylase and phospho-ERK, but not phospho-CREB, immunoreactivity in “dopamine islands”. Exposure of adolescent mice to methylphenidate resulted in an increase in eGFP in both compartments in the dorsolateral striatum but eGFP expression remained brighter in the striosomes. To address the role of activity in Nr4a1-eGFP expression, primary striatal cultures were prepared from neonatal mice and treated with forskolin, BDNF, SKF-83822 or high extracellular potassium and eGFP was measured fluorometrically in lysates. eGFP was induced in both neurons and contaminating glia in response to forskolin but SKF-83822, brain derived neurotrophic factor and depolarization increased eGFP in neuronal-like cells selectively. High levels of eGFP were primarily associated with Drd1+ neurons in vitro detected by immunofluorescence; however ∼15% of the brightly expressing cells contained punctate met-enkephalin immunoreactivity. The Nr4a1-GFP mouse strain will be a useful model for examining the connectivity, physiology, activity and development of the striosome system.

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Section: Resultssupporting

confidence: 73%

Nr4a1-eGFP Is a Marker of Striosome-Matrix Architecture, Development and Activity in the Extended Striatum

Davis

Puhl

2011

PLoS ONE

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“…There has been accumulating evidence that striosomes that appear as patchy profiles in individual sections actually form a continuous labyrinth in many species, including the cat (Groves et al 1988), rat (Desban et al 1993), mouse (Breuer et al 2005), monkey (Mikula et al 2009), and human (Manley et al 1994). The present analysis confirmed this, and further revealed that the five types of striosomes formed a single labyrinth.…”

Section: Resultsmentioning

confidence: 99%

Striosome-based map of the mouse striatum that is conformable to both cortical afferent topography and uneven distributions of dopamine D1 and D2 receptor-expressing cells

et al. 2018

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The striatum is critically involved in execution of appropriate behaviors, but its internal structures remain unmapped due to its unique structural organization, leading to ambiguity when interpreting heterogeneous properties of striatal neurons that differ by location. We focused on site-specific diversity of striosomes/matrix compartmentalization to draw the striatum map. Five types of striosomes were discriminated according to diverse immunoreactivities for the µ-opioid receptor, substance P (SP) and enkephalin, and each type occupied a particular domain inside the striatum. Furthermore, there was an additional domain lacking striosomes. This striosome-free space was located at the dorsolateral region and received afferents preferentially from the primary motor and sensory cortices, whereas the striosome-rich part received afferents from associational/limbic cortices, with topography inside both innervations. The proportion of dopamine D1 receptor-expressing, presumptive striatonigral neurons was approximately 70% in SP-positive striosomes, 40% in SP-deficient striosomes, 30% in the striosome-free space, and 50% in the matrix. In contrast, the proportion of D2 receptor-expressing, presumptive striatopallidal neurons was complementary to that of D1 receptor-expressing cells, indicating a close relationship between the map and the direct and indirect parallel circuitry. Finally, the most caudal part of the striatum lacked compartmentalization and consisted of three lamina characterized by intense and mutually exclusive immunoreactivities for SP and enkephalin. This tri-laminar part also received specific afferents from the cortex. The newly obtained map will facilitate broad fields of research in the basal ganglia with higher resolution of the three-dimensional anatomy of the striatum.Electronic supplementary materialThe online version of this article (10.1007/s00429-018-1749-3) contains supplementary material, which is available to authorized users.

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“…Within the striatum, striosomes reportedly have a leakier BBB than matrix. 13 Both the nigral neurons of the nigrosomes and the limbic cortical neurons of layers V and VI (which develop strong, earlier lewy bodies) project exclusively to striosomes. 14,15 The BBB of the striatum is especially fragile, whether to ischemic, osmotic, or other stressors.…”

Section: Discussionmentioning

confidence: 99%

Striatal Blood–Brain Barrier Permeability in Parkinson'S Disease

Gray

Woulfe

2015

J Cereb Blood Flow Metab

299

222

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In vivo studies have shown that blood-brain barrier (BBB) dysfunction is involved in the course of Parkinson's disease (PD). However, these have lacked either anatomic definition or the ability to recognize minute changes in BBB integrity. Here, using histologic markers of serum protein, iron, and erythrocyte extravasation, we have shown significantly increased permeability of the BBB in the postcommissural putamen of PD patients. The dense innervation of the striatum by PD-affected regions allows for exploitation of this permeability for therapeutic goals. These results are also discussed in the context of the retrograde transsynaptic hypothesis of PD spread. Keywords: α-synuclein; blood-brain barrier; Parkinson's disease; striatum INTRODUCTION Parkinson's disease (PD) is characterized by aggregation of filamentous or oligomerized α-synuclein and degeneration of specific neuronal regions. According to the dual-hit hypothesis of PD pathogenesis, a microbial or toxic pathogen within the gut lumen and the olfactory mucosa represents the pathogenic agent, with subsequent prion-like spread of pathology, first to the dorsal motor nucleus of the vagus and central olfactory areas, respectively, then to higher centers. The connectional anatomy linking the dorsal motor nucleus and olfactory bulb with higher centers such as the substantia nigra is unproven.We have previously proposed that disease could be spread hematogenously. 1 This is conceivable within the paradigm of retrograde (axon terminal to soma) Lewy pathology spread. 2,3 Almost all regions affected in Braak stage 1 have axon terminals outside the blood-brain barrier (BBB). That same BBB, however, protects the higher-order regions, whose axon terminals reside within the central nervous system, from blood-borne substances. Cell-to-cell spread is a potential mechanism to circumvent this protection but the connectional neuroanatomy is not consistent with the temporal order of Lewy pathology development as it is currently understood.Nigrostriatal dopaminergic neuronal cell bodies develop significant Lewy pathology, but recent studies strongly suggest that α-synuclein aggregation in these cells begins at presynaptic axon terminal in the striatum and spreads retrogradely to nigral

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Functional architecture of the mammalian striatum: Mouse vascular and striosome organization and their anatomic relationships

Cited by 17 publications

References 42 publications

Nr4a1-eGFP Is a Marker of Striosome-Matrix Architecture, Development and Activity in the Extended Striatum

Nr4a1-eGFP Is a Marker of Striosome-Matrix Architecture, Development and Activity in the Extended Striatum

Striosome-based map of the mouse striatum that is conformable to both cortical afferent topography and uneven distributions of dopamine D1 and D2 receptor-expressing cells

Striatal Blood–Brain Barrier Permeability in Parkinson'S Disease

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