Abstract
The mammalian striatum has a topographical organization of input-output connectivity, but a complex internal, nonlaminar neuronal architecture comprising projection neurons of two types interspersed among multiple interneuron types and potential local neuromodulators. From this cellular melange arises a biochemical compartmentalization of areas termed striosomes and extrastriosomal matrix. The functions of these compartments are poorly understood but might confer distinct features to striatal signal processing and be discretely governed. Dopamine transmission occurs throughout striosomes and matrix, and is reported to be modulated by the striosomally enriched neuromodulator substance P. However, reported effects are conflicting, ranging from facilitation to inhibition. We addressed whether dopamine transmission is modulated differently in striosome-matrix compartments by substance P.We paired detection of evoked dopamine release at carbon-fiber microelectrodes in mouse striatal slices with subsequent identification of the location of recording sites with respect to μ-opioid receptor-rich striosomes. Substance P had bidirectional effects on dopamine release that varied between recording sites and were prevented by inhibition of neurokinin-1 receptors. The direction of modulation was determined by location within the striosomal-matrix axis: dopamine release was boosted in striosome centers, diminished in striosomal-matrix border regions, and unaffected in the matrix. In turn, this different weighting of dopamine transmission by substance P modified the apparent center-surround contrast of striosomal dopamine signals. These data reveal that dopamine transmission can be differentially modulated within the striosomal-matrix axis, and furthermore, indicate a functionally distinct zone at the striosome-matrix interface, which may have key impacts on striatal integration.
Highlights
The mammalian striatum is critical to the control of our voluntary movements, reinforcement, and motor learning
We investigated whether the different effects of substance P (SP) were due to location within the striosome-matrix axis
SP acting through NK1Rs can boost DA release within the centers of striosomes, but diminish DA release in a border region where striosomes and matrix interface, suggesting that SP weights striosomal DA signals in a center-surround manner
Summary
The mammalian striatum is critical to the control of our voluntary movements, reinforcement, and motor learning. A network of interneurons and neuromodulators, including dopamine (DA) released from mesostriatal DA neurons, regulates the balance of outputs from two types of spiny projection neurons. The further differentiation of striatum into reticular patches called striosomes within the extrastriosomal matrix has long been known, and these compartments are developmentally, anatomically, and biochemically distinct (Graybiel and Ragsdale, 1978; Bolam et al, 1988; Gerfen, 1992; Crittenden and Graybiel, 2011). Little, has been clarified about their differential function. Striosomes and matrix can be partially distinguished by their inputs and outputs.
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