The Striosome and Matrix Compartments of the Striatum: A Path through the Labyrinth from Neurochemistry toward Function

Abstract

The striatum is a heterogeneous structure with a diverse range of neuron types and neuromodulators. Three decades of anatomical and biochemical studies have established that the neurochemical organization of striatum is not uniformly heterogeneous, but rather, can be differentiated into neurochemically discrete compartments known as striosomes (also known as patches) and matrix. These compartments are well understood to differ in their expression of neurochemical markers, with some differences in afferent and efferent connectivity and have also been suggested to have different involvement in a range of neurological diseases. However, the functional outcomes of striosome-matrix organization are poorly understood. Now, recent findings and new experimental tools are beginning to reveal that the distinctions between striosomes and matrix have distinct consequences for striatal synapse function. Here, we review recent findings that suggest there can be distinct regulation of neural function in striosome versus matrix compartments, particularly compartment-specific neurochemical interactions. We highlight that new transgenic and viral tools are becoming available that should now accelerate the pace of advances in understanding of these long-mysterious striatal compartments.

Monitoring Dopamine Responses to Potassium Ion and Nomifensine by in Vivo Microdialysis with Online Liquid Chromatography at One-Minute Resolution

“…Another intriguing possibility for future investigations is whether any of the variability that we see under the same stimulation conditions is related to the striatum’s physiological heterogeneity. 52 …”

Compartmental function and modulation of the striatum

“…The homogenous mix of dSPNs and iSPNs observed in adults is this result of a parallel, active intermixing of iSPNs (Tinterri et al, 2018). It should also be noted that the mature morphological appearance of compartmentalization varies by region, with striosomes in dorsal and central striatal regions having canonical "patchy" appearances, and those ventrally often appearing more like "swirls" (Brimblecombe & Cragg, 2017). It should also be noted that the mature morphological appearance of compartmentalization varies by region, with striosomes in dorsal and central striatal regions having canonical "patchy" appearances, and those ventrally often appearing more like "swirls" (Brimblecombe & Cragg, 2017).…”

“…It soon became apparent that this histological pattern represented a coordinated organizational principle of the mature striatum, with neighboring neurons having more in common than just the local acetylcholinesterase activity level. Numerous other striatal proteins and genes are preferentially expressed in striosomes versus matrix-exhaustive lists are available elsewhere (Brimblecombe & Cragg, 2017;Crittenden & Graybiel, 2011). Numerous other striatal proteins and genes are preferentially expressed in striosomes versus matrix-exhaustive lists are available elsewhere (Brimblecombe & Cragg, 2017;Crittenden & Graybiel, 2011).…”

“…This likely involves an interplay between (a) selective activation of afferents; (b) modulation of neuronal activity and synaptic transmission by neuromodulators such as dopamine (DA), acetylcholine (ACh), and opioid peptides; and (c) interneuron-mediated intra-and inter-compartmental signaling (Abudukeyoumu, Hernandez-Flores, Garcia-Munoz, & Arbuthnott, 2018;Brimblecombe & Cragg, 2017;Brimblecombe et al, 2018;Crittenden & Graybiel, 2011;Friedman et al, 2015). This likely involves an interplay between (a) selective activation of afferents; (b) modulation of neuronal activity and synaptic transmission by neuromodulators such as dopamine (DA), acetylcholine (ACh), and opioid peptides; and (c) interneuron-mediated intra-and inter-compartmental signaling (Abudukeyoumu, Hernandez-Flores, Garcia-Munoz, & Arbuthnott, 2018;Brimblecombe & Cragg, 2017;Brimblecombe et al, 2018;Crittenden & Graybiel, 2011;Friedman et al, 2015).…”

Striatal Local Circuitry: A New Framework for Lateral Inhibition

“…First identified by the expression patterns of proteins such as mu-opioid receptors and acetylcholinesterase, there are now over 60 genes known to be differentially expressed in patch vs. matrix compartments (Crittenden and Graybiel, 2011). Though patches only represent a small proportion of the striatum by volume, many of the differentially expressed genes are neuromodulators and their receptors suggesting that the patch and matrix have distinct pharmacological properties (Banghart et al, 2015; Brimblecombe and Cragg, 2016). Afferents to patch and matrix are also thought to arise from different sources with patches receiving limbic inputs and matrix neurons receiving sensorimotor inputs (Gerfen, 1984).…”