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Functional Roles of Neurotransmitters and Neuromodulators in the Dorsal Striatum

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Functional Roles of Neurotransmitters and Neuromodulators in the Dorsal Striatum Downloaded from learnmem.cshlp.org on October 1, 2021 - Published by Cold Spring Harbor Laboratory Press Review Functional roles of neurotransmitters and neuromodulators in the dorsal striatum Jeehaeh Do,1 Jae-Ick Kim,2 Joseph Bakes,1 Kyungmin Lee,3 and Bong-Kiun Kaang1,2,4 1Department of Brain and Cognitive Sciences, College of Natural Sciences, Seoul National University, Seoul 151-747, Korea; 2National Creative Research Initiative Center for Memory, Department of Biological Sciences, College of Natural Sciences, Seoul, National University, Seoul 151-747, Korea; 3Department of Anatomy, School of Medicine, Kyungpook National University, 2-101 Dongin-Dong, Daegu 700-842, Korea The dorsal striatum, with its functional microcircuits galore, serves as the primary gateway of the basal ganglia and is known to play a key role in implicit learning. Initially, excitatory inputs from the cortex and thalamus arrive on the direct and indirect pathways, where the precise flow of information is then regulated by local GABAergic interneurons. The balance of excitatory and inhibitory transmission in the dorsal striatum is modulated by neuromodulators such as dopa- mine and acetylcholine. Under pathophysiological states in the dorsal striatum, an alteration in excitatory and inhibitory transmission may underlie dysfunctional motor control. Here, we review the cellular connections and modulation of striatal microcircuits and propose that modulating the excitatory and inhibitory balance in synaptic transmission of the dorsal stri- atum is important for regulating locomotion. The dorsal striatum is best known for its role in decision-making, such as attention deficit/hyperactivity disorder (ADHD) and especially in action selection and initiation through the conver- autism. gence of sensorimotor, cognitive, and motivational information (DeLong 1990; Smith et al. 1998; Balleine et al. 2007). As the pri- mary input of the basal ganglia, the striatum receives glutamater- Circuits: Glutamatergic and GABAergic transmission gic inputs from the cortex and thalamus and in turn projects GABAergic outputs to the globus pallidus and substantia nigra Corticostriatal circuit: Direct/indirect pathway pars reticulata (SNr). Inputs from the cortex and thalamus both MSNs constitute .90% of the dense GABAergic striatal neuron form excitatory synaptic connections on medium spiny neurons population and can be subdivided into two main classes: the (MSN) in which cortical afferents are from the sensory, motor, direct-pathway (striatonigral) and indirect-pathway (striatopalli- and associational cortex (Bolam et al. 2000), and thalamic affer- dal) MSNs. The striatonigral MSNs (D -MSN) express high levels ents are from the intralaminar thalamic nuclei (Doig et al. 1 of both D dopamine (DA) receptors and M4 muscarinic receptors 2010). These glutamatergic inputs are then processed in the dorsal 1 and project directly to the internal globus pallidus (GPi in pri- striatum where numerous connections between various types of mates, GPm in rodents) and SNr. Striatopallidal MSNs (D -MSN) neurons exist. Thus, the complexity of neuronal circuits has 2 highly express D dopamine receptors and adenosine A recep- made it difficult to elucidate the functional roles of the striatum. 2 2A tors and project to the external globus pallidus (GPe in primates, Recently, studies focused on interneurons that reside in the dorsal GP in rodents). Direct and indirect pathways act in opposition striatum have characterized the physiological features and func- to one another to control movement, which indicates segregat- tional connections. For example, parvalbumin-expressing fast- ed information processing (Albin et al. 1989; DeLong 1990). spiking interneurons (PV-FSI) and neuropeptide-Y positive low- Compelling evidence of this segregation has been obtained from threshold spiking interneurons (NPY-LTS) form synaptic connec- studies in bacterial artificial chromosome (BAC) transgenic mice tions with MSNs and regulate the firing activity of the principal (Gong et al. 2003). The existence of synaptic connections between neuron MSNs (Koos and Tepper 1999; Gittis et al. 2010; direct- and indirect-pathway MSNs was reported only recently. Chuhma et al. 2011). These interneurons were shown to have dis- However, the functional significance of these connections is yet tinct firing patterns and connections, and thus they may exert to be characterized. different effects on MSNs. Other crucial connections are the cho- Cell-type specific whole-cell voltage clamp recordings have linergic, dopaminergic, and serotonergic axons that strongly in- revealed distinct physiological properties in D - and D -MSNs in nervate the dorsal striatum. These projections are essential for 1 2 BAC transgenic mice. D -MSNs have a higher NMDA/AMPA (2- modulating striatal circuits and disruption of such signaling can 2 amino-3-hydroxy-5-methyl-4-isoxazol propionic acid/N-Methyl- result in movement impairments and neurological disorders D-aspartate) ratio. Also, a greater paired-pulse ratio (PPR) value such as Huntington’s disease (Lovinger 2010). This review sum- than that of D -MSN indicates that corticostriatal inputs to marizes recent reports of the microcircuits present in the dorsal 1 D -MSNs have a higher probability in neurotransmitter release striatum, although serotonergic signaling is excluded, and sug- 2 (Ding et al. 2008). Further, membranes of D -MSNs are intrinsical- gests a putative role for striatal microcircuits in motor dysfunction 2 ly more excitable than those of D -MSNs (Kreitzer and Malenka and/or hyperactivity that often accompany psychiatric disorders 1 2007), which is supported by an anatomical comparison of soma- 4 todendritic trees, where the surface area of D1-MSNs is larger than Corresponding author that of D -MSNs (Gertler et al. 2008). E-mail [email protected] 2 Article is online at http://www.learnmem.org/cgi/doi/10.1101/lm.025015.111. Once the striatonigral direct-pathway circuit receives glu- Freely available online through the Learning & Memory Open Access option. tamatergic inputs from the sensorimotor cortex, GABAergic 20:21–28 # 2013 Cold Spring Harbor Laboratory Press 21 Learning & Memory ISSN 1549-5485/13; www.learnmem.org Downloaded from learnmem.cshlp.org on October 1, 2021 - Published by Cold Spring Harbor Laboratory Press Microcircuits in dorsal striatum and hyperactivity D1-MSNs, which project directly to GABAergic neurons in the GPi Local GABAergic circuits: Parvalbumin-expressing and SNr, are activated. Thus, GABAergic GPi and SNr neurons, fast-spiking interneurons and neuropeptide-Y positive which in turn send axons to motor nuclei of the thalamus, low-threshold spiking interneurons become inhibited. The net effect of this information flow is a disinhibition of excitatory thalamocortical projections. Since The GABAergic interneurons in the striatum form feed-forward the GPi is involved in axial and limb movements and the SNr in inhibitory synaptic connections on both MSNs and neighboring head and eye movements, activation of the striatonigral path- interneurons (Ding et al. 2010). The neighboring interneurons way is predicted to promote action selection and movement. have been largely classified into two groups: parvalbumin positive The striatopallidal indirect-pathway circuit also receives gluta- fast-spiking interneurons (PV-FSI) and neuropeptide-Y expressing matergic inputs from the cortex. Glutamatergic input onto low-threshold spiking interneurons (NPY-LTS). Although inter- GABAergic D2-MSNs inhibits GABAergic pallidal neurons of the neurons constitute a very small population of the dorsal striatum GPe, whereupon the target of the GPe neurons, the glutamatergic compared to that of MSNs, the minority exerts powerful inhibito- neurons of the subthalamic nucleus (STN), are disinhibited. ry effects on MSNs through GABAergic transmission. Studies have Disinhibition of excitatory STN neurons could activate inhib- shown that FSIs form multiple synapses, roughly ranging from itory output neurons of the GPi and SNr, resulting in a net effect 135 to 541 in number, on MSNs. One FSI could delay the genera- of an inhibition of excitatory thalamocortical projection neurons. tion of action potentials in MSNs by a single inhibitory postsynap- This would then lead to a reduction of cortical premotor drive tic current (IPSC) (Koos and Tepper 1999). FSIs both receive and inhibition of movement. and respond to cortical input faster than MSNs (Kawaguchi A compelling number of studies of synaptic plasticity in 1993), and in turn can exert fast inhibitory actions on both types corticostriatal synapses have been reported, but an in-depth of MSNs (Planert et al. 2010). BAC transgenic mice in which examination of these studies is beyond the scope of this review. GABAergic interneurons can be identified showed that FSIs prefer- Long-term depression (LTD), long-term potentiation (LTP), and entially target direct-pathway MSNs over indirect-pathway MSNs spike-timing dependent plasticity (STDP) occur in these types (Gittis et al. 2010). In addition, it is important to note that there is of synapses (Calabresi et al. 1992a,b; Centonze et al. 2001; Fino a prominent distinction between the actions of GABAA receptors et al. 2005; Wang et al. 2006; Pawlak and Kerr 2008). Endocanna- in direct- and indirect-pathway MSNs; currents through GABAA binoid-dependent LTD (Gerdeman et al. 2002) is much better receptors always depressed the response to corticostriatal stimula- characterized than NMDAR-dependent or NMDAR-independent tion
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