Specific populations of basal ganglia output neurons target distinct brain stem areas while collateralizing throughout the diencephalon

McElvain, Lauren E.; Chen, Yuncong; Moore, Jeffrey D.; Brigidi, G. Stefano; Bloodgood, Brenda L.; Lim, Byung Kook; Costa, Rui M.; Kleinfeld, David

doi:10.1016/j.neuron.2021.03.017

Cited by 100 publications

(113 citation statements)

References 105 publications

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“…It most likely depends on the precise connectivity patterns between different populations of MLR neurons and basal ganglia recipient neurons, as well as their recruitment profiles during natural behavior regulated through their inputs. In line with this idea, different behaviors are encoded by specific neuronal ensembles in the striatum ( Klaus et al., 2017 ), and SNr neurons divide into at least seven populations based on their projection targets ( McElvain et al., 2021 ). Movement therefore entails the orchestrated activation and inhibition of these ensembles in adequate sequence and vigor.…”

Section: Discussionmentioning

confidence: 97%

Functional diversity for body actions in the mesencephalic locomotor region

Ferreira‐Pinto

Kanodia

Falasconi

et al. 2021

Cell

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Summary The mesencephalic locomotor region (MLR) is a key midbrain center with roles in locomotion. Despite extensive studies and clinical trials aimed at therapy-resistant Parkinson’s disease (PD), debate on its function remains. Here, we reveal the existence of functionally diverse neuronal populations with distinct roles in control of body movements. We identify two spatially intermingled glutamatergic populations separable by axonal projections, mouse genetics, neuronal activity profiles, and motor functions. Most spinally projecting MLR neurons encoded the full-body behavior rearing. Loss- and gain-of-function optogenetic perturbation experiments establish a function for these neurons in controlling body extension. In contrast, Rbp4-transgene-positive MLR neurons project in an ascending direction to basal ganglia, preferentially encode the forelimb behaviors handling and grooming, and exhibit a role in modulating movement. Thus, the MLR contains glutamatergic neuronal subpopulations stratified by projection target exhibiting roles in action control not restricted to locomotion.

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Section: Discussionmentioning

confidence: 97%

Functional diversity for body actions in the mesencephalic locomotor region

Ferreira‐Pinto

Kanodia

Falasconi

et al. 2021

Cell

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“…While there is growing evidence that neural signals across cortex and striatum grow more coordinated during skill learning ( Santos et al, 2015 ; Lemke et al, 2019 ; Koralek et al, 2013 ; Costa et al, 2004 ), the relative importance of the ‘direction’ of communication between cortex and the striatum remains unclear. On one hand, it is well-established that cortical activity influences striatal activity ( Peters et al, 2021 ), and that, in turn, the basal ganglia is connected to brain stem regions that control movement ( McElvain et al, 2021 ). On the other hand, there is evidence that DLS activity may be important for stabilizing cortical activity patterns ( Koralek et al, 2012 ; Lemke et al, 2019 ), suggesting a role for basal ganglia ‘feedback’ to cortex through the thalamus ( Aoki et al, 2019 ; Athalye et al, 2020 ).…”

Section: Discussionmentioning

confidence: 99%

Coupling between motor cortex and striatum increases during sleep over long-term skill learning

Lemke

Ramanathan

Darevksy

et al. 2021

eLife

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The strength of cortical connectivity to the striatum influences the balance between behavioral variability and stability. Learning to consistently produce a skilled action requires plasticity in corticostriatal connectivity associated with repeated training of the action. However, it remains unknown whether such corticostriatal plasticity occurs during training itself or 'offline' during time away from training, such as sleep. Here, we monitor the corticostriatal network throughout long-term skill learning in rats and find that non-REM (NREM) sleep is a relevant period for corticostriatal plasticity. We first show that the offline activation of striatal NMDA receptors is required for skill learning. We then show that corticostriatal functional connectivity increases offline, coupled to emerging consistent skilled movements and coupled cross-area neural dynamics. We then identify NREM sleep spindles as uniquely poised to mediate corticostriatal plasticity, through interactions with slow oscillations. Our results provide evidence that sleep shapes cross-area coupling required for skill learning.

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“…On the other hand, a high release probability would lead to oIPSC depression during the light train, resulting in brief suppression of tonic firing that is not sustained over the course of seconds. SNr neurons are electrophysiologically heterogeneous (McElvain et al, 2021b) and it is likely that fundamental differences between SNr GABAergic synapses engaged in closed versus open loops stem from the recruitment of non-overlapping subpopulations of GABAergic SNr cells.…”

Section: Discussionmentioning

confidence: 99%

“…It is also possible that some DA neurons received Cre through unintended retrograde movement of the transsynaptic Cre virus (Ii et al, 2008;Zingg et al, 2017Zingg et al, , 2020. However, any retrograde movement of the virus does not affect the labeling of SNr neurons, since these cells do not project to striatum (McElvain et al, 2021a).…”

Section: Dissection Of Polysynaptic Striato-nigro-striatal Circuits Using a Transsynaptic Cre Virus And Intersectional Geneticsmentioning

confidence: 99%

Striatonigrostriatal Circuit Architecture for Disinhibition of Dopamine Signaling

Lerner

2021

Preprint

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The basal ganglia operate largely in closed parallel loops, including an associative circuit for goal-directed behavior originating from the dorsomedial striatum (DMS) and a somatosensory circuit important for habit formation originating from the dorsolateral striatum (DLS). An exception to this parallel circuit organization has been proposed to explain how information might be transferred between striatal subregions, for example from DMS to DLS during habit formation. The "ascending spiral hypothesis" proposes that DMS disinhibits dopamine signaling in DLS through a tri-synaptic, open-loop striato-nigro-striatal circuit. Here, we used transsynaptic and intersectional genetic tools to investigate both closed- and open-loop striato-nigro-striatal circuits. We found strong evidence for closed loops, which would allow striatal subregions to regulate their own dopamine release. We also found evidence for functional synapses in open loops. However, these synapses were unable to modulate tonic dopamine neuron firing, questioning the prominence of their role in mediating crosstalk between striatal subregions.

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Specific populations of basal ganglia output neurons target distinct brain stem areas while collateralizing throughout the diencephalon

Cited by 100 publications

References 105 publications

Functional diversity for body actions in the mesencephalic locomotor region

Functional diversity for body actions in the mesencephalic locomotor region

Coupling between motor cortex and striatum increases during sleep over long-term skill learning

Striatonigrostriatal Circuit Architecture for Disinhibition of Dopamine Signaling

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