Indirect pathway from caudate tail mediates rejection of bad objects in periphery

The essential everyday task of making appropriate choices is a process controlled mainly by the basal ganglia. To this end, subjects need not only to find “good” objects in their environment but also to reject “bad” objects. To reveal this rejection mechanism, we created a sequential saccade choice task for monkeys and studied the role of the indirect pathway from the CDt (tail of the caudate nucleus) mediated by cvGPe (caudal-ventral globus pallidus externus). Neurons in cvGPe were typically inhibited by the appearance of bad objects; however, this inhibition was reduced on trials when the monkeys made undesired saccades to the bad objects. Moreover, disrupting the inhibitory influence of CDt on cvGPe by local injection of bicuculline (GABAA receptor antagonist) impaired the monkeys’ ability to suppress saccades to bad objects. Thus, the indirect pathway mediates the rejection of bad choices, a crucial component of goal-directed behavior.

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Indirect pathway of caudate tail for choosing good objects in periphery

10.1101/547232 ◽

2019 ◽

Author(s):

Hidetoshi Amita ◽

Okihide Hikosaka

Keyword(s):

Basal Ganglia ◽

Globus Pallidus ◽

Real Life ◽

Inhibitory Response ◽

Choice Task ◽

Local Injection ◽

Indirect Pathway ◽

Rejection Mechanism ◽

Goal Directed Behavior ◽

Globus Pallidus Externus

AbstractChoosing good objects is essential for real life, which is controlled mainly by the basal ganglia. For that, a subject need to not only find good objects, but ‘reject’ bad objects. To reveal this ‘rejection’ mechanism, we created a sequential saccade choice task for monkeys and studied the indirect pathway of caudate tail mediated by cvGPe (caudal-ventral globus pallidus externus). The inhibitory responses of cvGPe neurons to bad objects were smaller when the monkey made saccades to them by mistake. Moreover, experimental reduction of the inhibitory response by local injection of bicuculline (GABAA antagonist) disabled the monkey to reject bad objects. In conclusion, rejecting bad objects is crucial for goal-directed behavior, which is controlled by the indirect pathway in the basal ganglia.

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Modeling the role of basal ganglia in saccade generation: Is the indirect pathway the explorer?

Neural Networks ◽

10.1016/j.neunet.2011.06.002 ◽

2011 ◽

Vol 24 (8) ◽

pp. 801-813 ◽

Cited By ~ 18

Author(s):

R. Krishnan ◽

S. Ratnadurai ◽

D. Subramanian ◽

V.S. Chakravarthy ◽

M. Rengaswamy

Keyword(s):

Basal Ganglia ◽

Indirect Pathway ◽

Saccade Generation

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Key Modulatory Role of Presynaptic Adenosine A2AReceptors in Cortical Neurotransmission to the Striatal Direct Pathway

The Scientific World JOURNAL ◽

10.1100/tsw.2009.143 ◽

2009 ◽

Vol 9 ◽

pp. 1321-1344 ◽

Cited By ~ 65

Author(s):

César Quiroz ◽

Rafael Luján ◽

Motokazu Uchigashima ◽

Ana Patrícia Simoes ◽

Talia N. Lerner ◽

...

Keyword(s):

Basal Ganglia ◽

Neuropsychiatric Disorders ◽

Receptor Function ◽

Striatal Neurons ◽

Indirect Pathway ◽

Direct Pathway ◽

Selective Modulation ◽

Efferent Pathways

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.

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Modeling Basal Ganglia for Understanding Parkinsonian Reaching Movements

Neural Computation ◽

10.1162/neco_a_00073 ◽

2011 ◽

Vol 23 (2) ◽

pp. 477-516 ◽

Cited By ~ 30

Author(s):

K. N. Magdoom ◽

D. Subramanian ◽

V. S. Chakravarthy ◽

B. Ravindran ◽

Shun-ichi Amari ◽

...

Keyword(s):

Basal Ganglia ◽

Motor Cortex ◽

Reaching Movements ◽

Substantia Nigra Pars Compacta ◽

Temporal Difference ◽

Indirect Pathway ◽

Dynamical Disease ◽

Exploratory Movements ◽

Dopamine Signal

We present a computational model that highlights the role of basal ganglia (BG) in generating simple reaching movements. The model is cast within the reinforcement learning (RL) framework with correspondence between RL components and neuroanatomy as follows: dopamine signal of substantia nigra pars compacta as the temporal difference error, striatum as the substrate for the critic, and the motor cortex as the actor. A key feature of this neurobiological interpretation is our hypothesis that the indirect pathway is the explorer. Chaotic activity, originating from the indirect pathway part of the model, drives the wandering, exploratory movements of the arm. Thus, the direct pathway subserves exploitation, while the indirect pathway subserves exploration. The motor cortex becomes more and more independent of the corrective influence of BG as training progresses. Reaching trajectories show diminishing variability with training. Reaching movements associated with Parkinson's disease (PD) are simulated by reducing dopamine and degrading the complexity of indirect pathway dynamics by switching it from chaotic to periodic behavior. Under the simulated PD conditions, the arm exhibits PD motor symptoms like tremor, bradykinesia and undershooting. The model echoes the notion that PD is a dynamical disease.

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Striatonigrostriatal Spirals in Addiction

Frontiers in Neural Circuits ◽

10.3389/fncir.2021.803501 ◽

2021 ◽

Vol 15 ◽

Author(s):

Andy Sivils ◽

John Q. Wang ◽

Xiang-Ping Chu

Keyword(s):

Substance Use ◽

Basal Ganglia ◽

Positive Emotions ◽

Physiological Role ◽

Reward System ◽

Pathophysiological Role ◽

The Us ◽

Goal Directed Behavior ◽

Economic Choices

A biological reward system is integral to all animal life and humans are no exception. For millennia individuals have investigated this system and its influences on human behavior. In the modern day, with the US facing an ongoing epidemic of substance use without an effective treatment, these investigations are of paramount importance. It is well known that basal ganglia contribute to rewards and are involved in learning, approach behavior, economic choices, and positive emotions. This review aims to elucidate the physiological role of striatonigrostriatal (SNS) spirals, as part of basal ganglia circuits, in this reward system and their pathophysiological role in perpetuating addiction. Additionally, the main functions of neurotransmitters such as dopamine and glutamate and their receptors in SNS circuits will be summarized. With this information, the claim that SNS spirals are crucial intermediaries in the shift from goal-directed behavior to habitual behavior will be supported, making this circuit a viable target for potential therapeutic intervention in those with substance use disorders.

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ACE (Actor-Critic-Explorer) Paradigm for Reinforcement Learning in Basal Ganglia: Highlighting the Role of the Indirect Pathway

Advances in Cognitive Science ◽

10.4135/9788132107910.n6 ◽

2014 ◽

pp. 71-90

Author(s):

Denny Joseph ◽

Garipelli Gangadhar ◽

V. Srinivasa Chakravarthy

Keyword(s):

Reinforcement Learning ◽

Basal Ganglia ◽

Indirect Pathway

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The limbic basal-ganglia-thalamocortical circuit and goal-directed behavior

Behavioral and Brain Sciences ◽

10.1017/s0140525x99292047 ◽

1999 ◽

Vol 22 (3) ◽

pp. 525-526 ◽

Cited By ~ 4

Author(s):

Daphna Joel

Keyword(s):

Basal Ganglia ◽

Motivational State ◽

Prefrontal Cortical ◽

Interconnected Model ◽

Goal Directed Behavior

Depue & Collins's model of incentive-motivational modulation of goal-directed behavior subserved by a medial orbital prefrontal cortical (MOC) network is appealing, but it leaves several questions unanswered: How are the stimuli that elicit an incentive motivational state selected? How does the incentive motivational state created by the MOC network modulate behavior? What is the function of the dopaminergic input to the striatum? This commentary suggests possible answers, based on the open-interconnected model of basal-ganglia-thalamocortical circuits, in which the limbic circuit selects goals and, via its connections with the motor and the associative circuits, directs behavior according to those goals, elaborating on the role of dopamine.

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