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

Yuta Miyamoto,Naoki Shigematsu,Takaichi Fukuda,Sachiko Katayama,Akinori Nishi

doi:10.1007/s00429-018-1749-3

Yuta Miyamoto, Naoki Shigematsu + Show 3 more

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https://doi.org/10.1007/s00429-018-1749-3

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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.

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The striatum is the major input structure of the basal ganglia and plays pivotal roles in optimizing behaviors through learning
Several weakly stained, but clearly discernible striosomes remained. This was because the intensity of labeling in both striosomes and the matrix was diverse depending of their positions inside the striatum even in a single section (Graybiel et al 1981; Prensa et al 1999); we found it was necessary to rescue such weakly stained striosomes by the visual inspection, which had an advantage over extracting striosomes through automatic-only or inspection-only procedures
We compared the combination of these markers in all the striosomes contained in serial sections through the whole striatum and found that striosomes could be classified into five types: those detectable only by MOR (MOR-only striosomes) or substance P (SP) (SP-only striosomes), those detectable by both MOR and SP (MOR/SP striosomes) or by both MOR and Enk (MOR/Enk striosomes), and those detectable by MOR, SP, and Enk (MOR/SP/Enk striosomes)

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The striatum is the major input structure of the basal ganglia and plays pivotal roles in optimizing behaviors through learning. It occupies a large portion of the subcortical gray matter in the mammalian telencephalon and receives driving. Functional division of the striatum into sensorimotor, associational, and limbic parts has been adopted in primates (Parent 1990). Faull 1989; Voorn et al 2004; Graybiel 2008) In both cases, the anatomical positions of these divisions are only roughly described, e.g., the dorsolateral part in rodent striatum is sensorimotor, the dorsomedial part is associational, and the ventral part is the limbic division. Even researchers using the newest technologies still do not have a common reference map that can be shared with others to facilitate mutual understanding of experimental data such as site-specific expression of genes (Tai et al 2013), virusmediated detailed connectivity (Fujiyama et al 2011; Wall et al 2013; Smith et al 2016), and responses to channelgating light with an illuminating apparatus placed in the brains of behaving animals (Valjent et al 2009; Friedman et al 2015; Smith et al 2016; Stephenson-Jones et al 2016; Bloem et al 2017)

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