scholarly journals Tonically active neurons in the monkey dorsal striatum signal outcome feedback during trial-and-error search behavior

2020 ◽  
Author(s):  
Hitoshi Inokawa ◽  
Naoyuki Matsumoto ◽  
Minoru Kimura ◽  
Hiroshi Yamada

AbstractAn animal’s choice behavior is shaped by the outcome feedback from selected actions in a trial-and-error approach. Tonically active neurons (TANs), presumed cholinergic interneurons in the striatum, are thought to be involved in the learning and performance of reward-directed behaviors, but it remains unclear how TANs are involved in shaping reward-directed choice behaviors based on the outcome feedback. To this end, we recorded activity of TANs from the dorsal striatum of two macaque monkeys (Macaca fuscata; 1 male, 1 female) while they performed a multi-step choice task to obtain multiple rewards. In this task, the monkeys first searched for a rewarding target from among three alternatives in a trial-and-error manner and then earned additional rewards by repeatedly choosing the rewarded target. We found that a considerable proportion of TANs selectively responded to either the reward or the no-reward outcome feedback during the trial-and-error search, but these feedback responses were not observed during repeat trials. Moreover, the feedback responses of TANs were similarly observed in any search trials, without distinctions regarding the predicted probability of rewards and the location of chosen targets. Unambiguously, TANs detected reward and no-reward feedback specifically when the monkeys performed trial-and-error searches, in which the monkeys were learning the value of the targets and adjusting their subsequent choice behavior based on the reward and no-reward feedback. These results suggest that striatal cholinergic interneurons signal outcome feedback specifically during search behavior, in circumstances where the choice outcomes cannot be predicted with certainty by the animals.HighlightsTANs signal reward and no-reward outcome feedback when monkeys made search behaviorsTANs respond regardless of predicted reward probability or chosen target locationTANs may signal feedback outcomes when rewards cannot be predicted with certainty

Neuroscience ◽  
2020 ◽  
Vol 446 ◽  
pp. 271-284
Author(s):  
Hitoshi Inokawa ◽  
Naoyuki Matsumoto ◽  
Minoru Kimura ◽  
Hiroshi Yamada

2018 ◽  
pp. 1-12
Author(s):  
Simon Bridge

Abstract In business the future is not predetermined, and the unexpected often happens. So how should entrepreneurs (and businesses) try to address that future uncertainty? This paper suggests that there are two main options: 1. The often-preferred approach seeks to reduce uncertainty by forecasting and planning, using ‘left-brained’ logic and analysis. 2. The alternative way seeks to live with, and to benefit from, uncertainty by using ideas derived from exploration, effectuation, antifragility and ‘trial and error’. This paper compares the two approaches and considers their rationales and potential effectiveness. It suggests that forecasting and planning has many drawbacks and is often not the best way to operate in uncertain conditions. Nevertheless, it is often advocated and its thinking seems to have been adopted as the default philosophy for business. Therefore if, as has been suggested, uncertainty is the norm, do we need to advocate adopting a different way of thinking?


2017 ◽  
Vol 125 (3) ◽  
pp. 501-513 ◽  
Author(s):  
Ko Yamanaka ◽  
Yukiko Hori ◽  
Takafumi Minamimoto ◽  
Hiroshi Yamada ◽  
Naoyuki Matsumoto ◽  
...  

2011 ◽  
Vol 23 (6) ◽  
pp. 1549-1566 ◽  
Author(s):  
F. Gregory Ashby ◽  
Matthew J. Crossley

An essential component of skill acquisition is learning the environmental conditions in which that skill is relevant. This article proposes and tests a neurobiologically detailed theory of how such learning is mediated. The theory assumes that a key component of this learning is provided by the cholinergic interneurons in the striatum known as tonically active neurons (TANs). The TANs are assumed to exert a tonic inhibitory influence over cortical inputs to the striatum that prevents the execution of any striatal-dependent actions. The TANs learn to pause in rewarding environments, and this pause releases the striatal output neurons from this inhibitory effect, thereby facilitating the learning and expression of striatal-dependent behaviors. When rewards are no longer available, the TANs cease to pause, which protects striatal learning from decay. A computational version of this theory accounts for a variety of single-cell recording data and some classic behavioral phenomena, including fast reacquisition after extinction.


2018 ◽  
Author(s):  
Tiffany Bell ◽  
Angela Langdon ◽  
Michael Lindner ◽  
William Lloyd ◽  
Anastasia Christakou

ABSTRACTCognitive flexibility is crucial for adaptation and is disrupted in neuropsychiatric disorders and psychopathology. Human studies of flexibility using reversal learning tasks typically contrast error trials before and after reversal, which provides little information about the mechanisms that support learning and expressing a new response. However, animal studies suggest a specific role in this latter process for the connections between the dorsal striatum and the centromedian parafascicular (CM-Pf) thalamus, a system which may recruit the striatal cholinergic interneurons, but which is not well understood in humans. This study investigated the role of this system in human probabilistic reversal learning, specifically with respect to learning a new response strategy, contrasting its function to that of the better understood orbitoftontal-striatal systems. Using psychophysiological interaction (PPI) analysis of functional magnetic resonance imaging (fMRI) data we show that connectivity between the striatum and both the lateral orbitofrontal cortex (lOFC) and CM-Pf pathways increased during reversal, but not initial learning. However, while the strength of lOFC-striatal connectivity was associated with the speed of the reversal, the strength of CM-Pf-striatal connectivity was associated specifically with the quality of the reversal (reduced regressive errors). These findings expand our understanding of flexibility mechanisms in the human brain, bridging the gap with animal studies of this system.


2019 ◽  
Author(s):  
Jonathan J. Cannon ◽  
Aniruddh D. Patel

AbstractBeat perception is central to music cognition. The motor system is involved in beat perception, even in the absence of movement, yet current frameworks for modeling beat perception do not strongly engage with the motor system’s neurocomputational properties. We believe fundamental progress on modeling beat perception requires a synthesis between cognitive science and motor neuroscience, yielding predictions to guide research. Success on this front would be a landmark in the study of how “embodied cognition” is implemented in brain activity. We illustrate this approach by proposing specific roles for two key motor brain structures (the supplementary motor area, and the dorsal striatum of the basal ganglia) in covert beat maintenance, building on current research on their role in actual movement.Highlights⍰Components of the brain’s motor system are activated by the perception of a musical beat, even in the absence of movement, and may play an important role in beat-based temporal prediction.⍰Two key brain regions involved in movement, the supplementary motor area and dorsal striatum, have neurocomputational properties that lend themselves to beat perception.⍰In supplementary motor area, neural firing rates represent the phase of cyclic sensorimotor processes.⍰Supplementary motor area’s involvement in perceptual suppression of self-generated sounds suggests that it could play a broader role in informing auditory expectations.⍰Dorsal striatum plays a central role in initiating and sequencing units of movement, and may serve similar functions in structuring beat-based temporal anticipation.


2016 ◽  
Vol 113 (3) ◽  
pp. 787-792 ◽  
Author(s):  
Tuğçe Tosun ◽  
Ezgi Gür ◽  
Fuat Balcı

Animals can shape their timed behaviors based on experienced probabilistic relations in a nearly optimal fashion. On the other hand, it is not clear if they adopt these timed decisions by making computations based on previously learnt task parameters (time intervals, locations, and probabilities) or if they gradually develop their decisions based on trial and error. To address this question, we tested mice in the timed-switching task, which required them to anticipate when (after a short or long delay) and at which of the two delay locations a reward would be presented. The probability of short trials differed between test groups in two experiments. Critically, we first trained mice on relevant task parameters by signaling the active trial with a discriminative stimulus and delivered the corresponding reward after the associated delay without any response requirement (without inducing switching behavior). During the test phase, both options were presented simultaneously to characterize the emergence and temporal characteristics of the switching behavior. Mice exhibited timed-switching behavior starting from the first few test trials, and their performance remained stable throughout testing in the majority of the conditions. Furthermore, as the probability of the short trial increased, mice waited longer before switching from the short to long location (experiment 1). These behavioral adjustments were in directions predicted by reward maximization. These results suggest that rather than gradually adjusting their time-dependent choice behavior, mice abruptly adopted temporal decision strategies by directly integrating their previous knowledge of task parameters into their timed behavior, supporting the model-based representational account of temporal risk assessment.


2003 ◽  
Vol 986 (1-2) ◽  
pp. 22-29 ◽  
Author(s):  
Adriana A Alcantara ◽  
Violeta Chen ◽  
Bruce E Herring ◽  
John M Mendenhall ◽  
Monica L Berlanga

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Shahzad S Khan ◽  
Yuriko Sobu ◽  
Herschel S Dhekne ◽  
Francesca Tonelli ◽  
Kerryn Berndsen ◽  
...  

Activating LRRK2 mutations cause Parkinson's disease, and pathogenic LRRK2 kinase interferes with ciliogenesis. Previously, we showed that cholinergic interneurons of the dorsal striatum lose their cilia in R1441C LRRK2 mutant mice (Dhekne et al., 2018). Here, we show that cilia loss is seen as early as 10 weeks of age in these mice and also in two other mouse strains carrying the most common human G2019S LRRK2 mutation. Loss of the PPM1H phosphatase that is specific for LRRK2-phosphorylated Rab GTPases yields the same cilia loss phenotype seen in mice expressing pathogenic LRRK2 kinase, strongly supporting a connection between Rab GTPase phosphorylation and cilia loss. Moreover, astrocytes throughout the striatum show a ciliation defect in all LRRK2 and PPM1H mutant models examined. Hedgehog signaling requires cilia, and loss of cilia in LRRK2 mutant rodents correlates with dysregulation of Hedgehog signaling as monitored by in situ hybridization of Gli1 and Gdnf transcripts. Dopaminergic neurons of the substantia nigra secrete a Hedgehog signal that is sensed in the striatum to trigger neuroprotection; our data support a model in which LRRK2 and PPM1H mutant mice show altered responses to critical Hedgehog signals in the nigrostriatal pathway.


2018 ◽  
Author(s):  
Mark D. Condon ◽  
Nicola J. Platt ◽  
Yan-Feng Zhang ◽  
Bradley M. Roberts ◽  
Michael A. Clements ◽  
...  

AbstractMesostriatal DA neurons possess extensively branched axonal arbours. Whether action potentials are converted to DA output in striatum will be influenced dynamically and critically by axonal properties and mechanisms that are poorly understood. We addressed the roles for mechanisms governing release probability and axonal activity in determining short-term plasticity of DA release, using fast-scan cyclic voltammetry in ex vivo mouse striatum. Brief short-term facilitation (STF) and longer short-term depression (STD) were only weakly dependent on the level of initial release, i.e. were release-insensitive. Rather, short-term plasticity was strongly determined by mechanisms which governed axonal activation, including K+-gated excitability and the dopamine transporter (DAT), particularly in dorsal striatum. We identify the DAT as a master regulator of DA short-term plasticity, governing the balance between release-dependent and independent mechanisms that also show region-specific gating.Key FindingsShort-term plasticity in dopamine release is only weakly governed by initial releaseShort-term depression is strongly dependent on axonal excitability and activationThe dopamine transporter controls short-term plasticity and drives short-term depressionDopamine transporters govern the balance between release-dependent and -independent mechanisms


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