scholarly journals A computational model explains and predicts substantia nigra pars reticulata responses to pallidal and striatal inputs

2020 ◽  
Author(s):  
Ryan S. Phillips ◽  
Ian Rosner ◽  
Aryn H. Gittis ◽  
Jonathan E. Rubin
Keyword(s):  
Substantia Nigra ◽  
Low Frequency ◽  
Operating Mode ◽  
Impact Behavior ◽  
Substantia Nigra Pars Reticulata ◽  
Indirect Pathway ◽  
Optogenetic Stimulation ◽  
Low Frequency Oscillations ◽  
Computational Work ◽  
Stimulation Of

AbstractAs a rodent basal ganglia (BG) output nucleus, the substantia nigra pars reticulata (SNr) is well positioned to impact behavior. SNr neurons receive GABAergic inputs from the striatum (direct pathway) and globus pallidus (GPe, indirect pathway). Dominant theories of action selection rely on these pathways’ inhibitory actions. Yet, experimental results on SNr responses to these inputs are limited and include excitatory effects. Our study combines experimental and computational work to characterize, explain, and make predictions about these pathways. We observe diverse SNr responses to stimulation of SNr-projecting striatal and GPe neurons, including biphasic and excitatory effects, which our modeling shows can be explained by intracellular chloride processing. Our work predicts that ongoing GPe activity could tune the SNr operating mode, including its responses in decision-making scenarios, and GPe output may modulate synchrony and low-frequency oscillations of SNr neurons, which we confirm using optogenetic stimulation of GPe terminals within the SNr.

scholarly journals The effects of chloride dynamics on substantia nigra pars reticulata responses to pallidal and striatal inputs

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Ryan S Phillips ◽  
Ian Rosner ◽  
Aryn H Gittis ◽  
Jonathan E Rubin
Keyword(s):  
Substantia Nigra ◽  
Low Frequency ◽  
Operating Mode ◽  
Impact Behavior ◽  
Substantia Nigra Pars Reticulata ◽  
Indirect Pathway ◽  
Optogenetic Stimulation ◽  
Low Frequency Oscillations ◽  
Computational Work ◽  
Stimulation Of

As a rodent basal ganglia (BG) output nucleus, the substantia nigra pars reticulata (SNr) is well positioned to impact behavior. SNr neurons receive GABAergic inputs from the striatum (direct pathway) and globus pallidus (GPe, indirect pathway). Dominant theories of action selection rely on these pathways’ inhibitory actions. Yet, experimental results on SNr responses to these inputs are limited and include excitatory effects. Our study combines experimental and computational work to characterize, explain, and make predictions about these pathways. We observe diverse SNr responses to stimulation of SNr-projecting striatal and GPe neurons, including biphasic and excitatory effects, which our modeling shows can be explained by intracellular chloride processing. Our work predicts that ongoing GPe activity could tune the SNr operating mode, including its responses in decision-making scenarios, and GPe output may modulate synchrony and low-frequency oscillations of SNr neurons, which we confirm using optogenetic stimulation of GPe terminals within the SNr.

scholarly journals Functional territories in primate substantia nigra pars reticulata separately signaling stable and flexible values

2015 ◽  
Vol 113 (6) ◽  
pp. 1681-1696 ◽  
Author(s):  
Masaharu Yasuda ◽  
Okihide Hikosaka
Keyword(s):  
Electrical Stimulation ◽  
Basal Ganglia ◽  
Substantia Nigra ◽  
Signal Transmission ◽  
Inhibitory Response ◽  
Substantia Nigra Pars Reticulata ◽  
Visual Objects ◽  
Direct Input ◽  
Antidromic Response ◽  
Stimulation Of

Gaze is strongly attracted to visual objects that have been associated with rewards. Key to this function is a basal ganglia circuit originating from the caudate nucleus (CD), mediated by the substantia nigra pars reticulata (SNr), and aiming at the superior colliculus (SC). Notably, subregions of CD encode values of visual objects differently: stably by CD tail [CD(T)] vs. flexibly by CD head [CD(H)]. Are the stable and flexible value signals processed separately throughout the CD-SNr-SC circuit? To answer this question, we identified SNr neurons by their inputs from CD and outputs to SC and examined their sensitivity to object values. The direct input from CD was identified by SNr neuron's inhibitory response to electrical stimulation of CD. We found that SNr neurons were separated into two groups: 1) neurons inhibited by CD(T) stimulation, located in the caudal-dorsal-lateral SNr (cdlSNr), and 2) neurons inhibited by CD(H) stimulation, located in the rostral-ventral-medial SNr (rvmSNr). Most of CD(T)-recipient SNr neurons encoded stable values, whereas CD(H)-recipient SNr neurons tended to encode flexible values. The output to SC was identified by SNr neuron's antidromic response to SC stimulation. Among the antidromically activated neurons, many encoded only stable values, while some encoded only flexible values. These results suggest that CD(T)-cdlSNr-SC circuit and CD(H)-rvmSNr-SC circuit transmit stable and flexible value signals, largely separately, to SC. The speed of signal transmission was faster through CD(T)-cdlSNr-SC circuit than through CD(H)-rvmSNr-SC circuit, which may reflect automatic and controlled gaze orienting guided by these circuits.

scholarly journals Opponent regulation of action performance and timing by striatonigral and striatopallidal pathways

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Konstantin I Bakhurin ◽  
Xiaoran Li ◽  
Alexander D Friedman ◽  
Nicholas A Lusk ◽  
Glenn DR Watson ◽  
...  
Keyword(s):  
Basal Ganglia ◽  
Reinforcement Schedule ◽  
Action Selection ◽  
Fixed Time ◽  
Indirect Pathway ◽  
Optogenetic Stimulation ◽  
Direct Pathway ◽  
Stimulation Of

The basal ganglia have been implicated in action selection and timing, but the relative contributions of the striatonigral (direct) and striatopallidal (indirect) pathways to these functions remain unclear. We investigated the effects of optogenetic stimulation of D1+ (direct) and A2A+ (indirect) neurons in the ventrolateral striatum in head-fixed mice on a fixed time reinforcement schedule. Direct pathway stimulation initiates licking, whereas indirect pathway stimulation suppresses licking and results in rebound licking after stimulation. Moreover, direct and indirect pathways also play distinct roles in timing. Direct pathway stimulation produced a resetting of the internal timing process, whereas indirect pathway stimulation transiently paused timing, and proportionally delayed the next bout of licking. Our results provide evidence for the continuous and opposing contributions of the direct and indirect pathways in the production and timing of reward-guided behavior.

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