scholarly journals Spatial organization of functional clusters representing reward and movement information in the striatal direct and indirect pathways

2020 ◽  
Vol 117 (43) ◽  
pp. 27004-27015
Author(s):  
Jung Hwan Shin ◽  
Min Song ◽  
Se-Bum Paik ◽  
Min Whan Jung

To obtain insights into striatal neural processes underlying reward-based learning and movement control, we examined spatial organizations of striatal neurons related to movement and reward-based learning. For this, we recorded the activity of direct- and indirect-pathway neurons (D1 and A2a receptor-expressing neurons, respectively) in mice engaged in probabilistic classical conditioning and open-field free exploration. We found broadly organized functional clusters of striatal neurons in the direct as well as indirect pathways for both movement- and reward-related variables. Functional clusters for different variables were partially overlapping in both pathways, but the overlap between outcome- and value-related functional clusters was greater in the indirect than direct pathway. Also, value-related spatial clusters were progressively refined during classical conditioning. Our study shows the broad and learning-dependent spatial organization of functional clusters of dorsal striatal neurons in the direct and indirect pathways. These findings further argue against the classic model of the basal ganglia and support the importance of spatiotemporal patterns of striatal neuronal ensemble activity in the control of behavior.

2021 ◽  
Author(s):  
Lele Cui ◽  
Shunhang Tang ◽  
Kai Zhao ◽  
Jingwei Pan ◽  
Zhaoran Zhang ◽  
...  

Action selection during decision-making depends on the basal ganglia circuits that comprise the direct and indirect pathways known to oppositely control movement. However, the mechanism for coordinating these opponent pathways during decision-making remains unclear. We address this by employing deep-brain two-photon imaging and optogenetic manipulations of the direct- and indirect-pathway spiny projection neurons (dSPNs and iSPNs) in the posterior striatum during an auditory decision-making behavior. We show that while dSPNs and iSPNs play opposite causal roles during decision-making, each subtype contains divergent ensembles preferring different choices. The ensembles in dSPNs show stronger contralateral dominance than those in iSPNs manifested by higher-level activation and synchronization. Consistent with this asymmetrical contralateral dominance, optogenetic disinhibition of both pathways promoted contralateral choices. A computational model incorporating the striatal ensemble asymmetry recapitulated the causal behavioral effects. Our results uncover the asymmetry between opponent SPN ensembles as a circuit mechanism for action selection during decision-making.


2021 ◽  
Author(s):  
Nicholas M Blauch ◽  
Marlene Behrmann ◽  
David Plaut

Inferotemporal cortex (IT) in humans and other primates is topographically organized, with multiple domain-selective areas and other general patterns of functional organization. What factors underlie this organization, and what can this neural arrangement tell us about the mechanisms of high level vision? Here, we present an account of topographic organization involving a computational model with two components: 1) a feature-extracting encoder model of early visual processes, followed by 2) a model of high-level hierarchical visual processing in IT subject to specific biological constraints. In particular, minimizing the wiring cost on spatially organized feedforward and lateral connections within IT, combined with constraining the feedforward processing to be strictly excitatory, results in a hierarchical, topographic organization. This organization replicates a number of key properties of primate IT cortex, including the presence of domain-selective spatial clusters preferentially involved in the representation of faces, objects, and scenes, within-domain topographic organization such as animacy and indoor/outdoor distinctions, and generic spatial organization whereby the response correlation of pairs of units falls off with their distance. The model supports a view in which both domain-specific and domain-general topographic organization arise in the visual system from an optimization process that maximizes behavioral performance while minimizing wiring costs.


2012 ◽  
Vol 15 (6) ◽  
pp. 816-818 ◽  
Author(s):  
Alexxai V Kravitz ◽  
Lynne D Tye ◽  
Anatol C Kreitzer

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Mingqi Zhao ◽  
Marco Marino ◽  
Jessica Samogin ◽  
Stephan P. Swinnen ◽  
Dante Mantini

AbstractThe primary sensorimotor cortex plays a major role in the execution of movements of the contralateral side of the body. The topographic representation of different body parts within this brain region is commonly investigated through functional magnetic resonance imaging (fMRI). However, fMRI does not provide direct information about neuronal activity. In this study, we used high-density electroencephalography (hdEEG) to map the representations of hand, foot, and lip movements in the primary sensorimotor cortex, and to study their neural signatures. Specifically, we assessed the event-related desynchronization (ERD) in the cortical space. We found that the performance of hand, foot, and lip movements elicited an ERD in beta and gamma frequency bands. The primary regions showing significant beta- and gamma-band ERD for hand and foot movements, respectively, were consistent with previously reported using fMRI. We observed relatively weaker ERD for lip movements, which may be explained by the fact that less fine movement control was required. Overall, our study demonstrated that ERD based on hdEEG data can support the study of motor-related neural processes, with relatively high spatial resolution. An interesting avenue may be the use of hdEEG for deeper investigations into the pathophysiology of neuromotor disorders.


2009 ◽  
Vol 9 ◽  
pp. 1321-1344 ◽  
Author(s):  
César Quiroz ◽  
Rafael Luján ◽  
Motokazu Uchigashima ◽  
Ana Patrícia Simoes ◽  
Talia N. Lerner ◽  
...  

Basal ganglia processing results from a balanced activation of direct and indirect striatal efferent pathways, which are controlled by dopamine D1and D2receptors, respectively. Adenosine A2Areceptors are considered novel antiparkinsonian targets, based on their selective postsynaptic localization in the indirect pathway, where they modulate D2receptor function. The present study provides evidence for the existence of an additional, functionally significant, segregation of A2Areceptors at the presynaptic level. Using integrated anatomical, electrophysiological, and biochemical approaches, we demonstrate that presynaptic A2Areceptors are preferentially localized in cortical glutamatergic terminals that contact striatal neurons of the direct pathway, where they exert a selective modulation of corticostriatal neurotransmission. Presynaptic striatal A2Areceptors could provide a new target for the treatment of neuropsychiatric disorders.


2004 ◽  
Vol 46 (7) ◽  
pp. 994-1007 ◽  
Author(s):  
Kerstin Wirkner ◽  
Zoltan Gerevich ◽  
Thomas Krause ◽  
Albrecht Günther ◽  
Laszlo Köles ◽  
...  

2013 ◽  
Vol 33 (10) ◽  
pp. 1612-1620 ◽  
Author(s):  
Zeng-Jin Yang ◽  
Bing Wang ◽  
Herman Kwansa ◽  
Kerry D Heitmiller ◽  
Gina Hong ◽  
...  

Pharmacologic inactivation or genetic deletion of adenosine A2A receptors protects ischemic neurons in adult animals, but studies in neonatal hypoxia-ischemia (H-I) are inconclusive. The present study in neonatal piglets examined the hypothesis that A2A receptor signaling after reoxygenation from global H-I contributes to injury in highly vulnerable striatal neurons where A2A receptors are enriched. A2A receptor immunoreactivity was detected in striatopallidal neurons. In nonischemic piglets, direct infusion of the selective A2A receptor agonist CGS 21680 through microdialysis probes into putamen increased phosphorylation of N-methyl-D-aspartic acid (NMDA) receptor NR1 subunit and Na+, K+-ATPase selectively at protein kinase A (PKA)-sensitive sites. In ischemic piglets, posttreatment with SCH 58261, a selective A2A receptor antagonist, improved early neurologic recovery and preferentially protected striatopallidal neurons. SCH 58261 selectively inhibited the ischemia-induced phosphorylation of NR1, Na+, K+-ATPase, and cAMP-regulated phosphoprotein 32 KDa (DARPP32) at PKA-sensitive sites at 3 hours of recovery and improved Na+, K+-ATPase activity. SCH 58261 also suppressed ischemia-induced protein nitration and oxidation. Thus, A2A receptor activation during reoxygenation contributes to the loss of a subpopulation of neonatal putamen neurons after H-I. Its toxic signaling may be related to DARPP32-dependent phosphorylation of PKA-sensitive sites on NR1 and Na+, K+-ATPase, thereby augmenting excitotoxicity-induced oxidative stress after reoxygenation.


2013 ◽  
Vol 110 (9) ◽  
pp. 2203-2216 ◽  
Author(s):  
Wei Wei ◽  
Li Li ◽  
Guoliang Yu ◽  
Shengyuan Ding ◽  
Chengyao Li ◽  
...  

The dopamine (DA) D2 receptor (D2R)-expressing medium spiny neurons (D2-MSNs) in the striatum project to and inhibit the GABAergic neurons in the globus pallidus (GP), forming an important link in the indirect pathway of the basal ganglia movement control circuit. These striatopallidal axon terminals express presynaptic D2Rs that inhibit GABA release and thus regulate basal ganglion function. Here we show that in transcription factor Pitx3 gene mutant mice with a severe DA loss in the dorsal striatum mimicking the DA denervation in Parkinson's disease (PD), the striatopallidal GABAergic synaptic transmission displayed a heightened sensitivity to presynaptic D2R-mediated inhibition with the dose-response curve shifted to the left, although the maximal inhibition was not changed. Functionally, low concentrations of DA were able to more efficaciously reduce the striatopallidal inhibition-induced pauses of GP neuron activity in DA-deficient Pitx3 mutant mice than in wild-type mice. These results demonstrate that presynaptic D2R inhibition of the striatopallidal synapse becomes supersensitized after DA loss. These supersensitive D2Rs may compensate for the lost DA in PD and also induce a strong disinhibition of GP neuron activity that may contribute to the motor-stimulating effects of dopaminergic treatments in PD.


2021 ◽  
Author(s):  
Vernie Aguda ◽  
Helen Chasiotis ◽  
Indira Riadi ◽  
Tod Rogers Thiele

Striatal neurons within the basal ganglia play a central role in vertebrate action selection; however, their location in larval zebrafish is not well defined. We assayed for conserved striatal markers in the zebrafish subpallium using fluorescent in situ hybridization (FISH) and immunohistochemistry. Whole mount FISH revealed an inhibitory neuronal cluster rostral to the anterior commissure that expresses tac1, the gene that encodes the precursor peptide for substance P. This molecular profile is shared by mammalian striatal direct pathway neurons. A second partially overlapping population of inhibitory neurons was identified that expresses penka, the gene that encodes the precursor peptide for enkephalin. This molecular profile is shared by striatal indirect pathway neurons. Immunostaining for substance P and enkephalin confirmed the presence of these peptides in the subpallium as well as the presence of dopaminergic innervation. The tac1 and penka populations were both found to increase linearly across larval stages. Together, these findings support the existence of a striatal homologue in larval zebrafish that grows to match the development and increasing behavioural complexity of the organism.


Function ◽  
2021 ◽  
Author(s):  
Tanya Sippy ◽  
Corryn Chaimowitz ◽  
Sylvain Crochet ◽  
Carl C H Petersen

Abstract The striatum integrates sensorimotor and motivational signals, likely playing a key role in reward-based learning of goal-directed behavior. However, cell type-specific mechanisms underlying reinforcement learning remain to be precisely determined. Here, we investigated changes in membrane potential dynamics of dorsolateral striatal neurons comparing naïve mice and expert mice trained to lick a reward spout in response to whisker deflection. We recorded from three distinct cell types: i) direct pathway striatonigral neurons, which express type 1 dopamine receptors; ii) indirect pathway striatopallidal neurons, which express type 2 dopamine receptors; and iii) tonically active, putative cholinergic, striatal neurons. Task learning was accompanied by cell type-specific changes in the membrane potential dynamics evoked by the whisker deflection and licking in successfully-performed trials. Both striatonigral and striatopallidal types of striatal projection neurons showed enhanced task-related depolarization across learning. Striatonigral neurons showed a prominent increase in a short latency sensory-evoked depolarization in expert compared to naïve mice. In contrast, the putative cholinergic striatal neurons developed a hyperpolarizing response across learning, driving a pause in their firing. Our results reveal cell type-specific changes in striatal membrane potential dynamics across the learning of a simple goal-directed sensorimotor transformation, helpful for furthering the understanding of the various potential roles of different basal ganglia circuits.


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