Basal ganglia role in learning rewarded actions and executing previously learned choices: Healthy and diseased states
| Autor: | Alexey Kuznetsov, Brady K. Atwood, Garrett Mulcahy |
|---|---|
| Jazyk: | angličtina |
| Rok vydání: | 2020 |
| Předmět: |
0301 basic medicine
medicine.medical_treatment Social Sciences Basal Ganglia Cognition Learning and Memory 0302 clinical medicine Animal Cells Basal ganglia Medicine and Health Sciences Psychology Prefrontal cortex Neurons Cerebral Cortex Movement Disorders Neuronal Plasticity Multidisciplinary Random switching Brain Neurodegenerative Diseases Parkinson Disease Long-term potentiation Huntington Disease Hebbian theory medicine.anatomical_structure Neurology Genetic Diseases Cerebral cortex Medicine Cellular Types Anatomy Research Article Deep brain stimulation Science Decision Making Models Neurological Prefrontal Cortex Action selection 03 medical and health sciences Developmental Neuroscience Reward medicine Learning Humans Clinical Genetics Autosomal Dominant Diseases Cognitive Psychology Biology and Life Sciences Cell Biology Neostriatum 030104 developmental biology Action (philosophy) Cellular Neuroscience Case-Control Studies Synaptic plasticity Cognitive Science Neuroscience 030217 neurology & neurosurgery Synaptic Plasticity |
| Zdroj: | PLoS ONE, Vol 15, Iss 2, p e0228081 (2020) PLoS ONE |
| ISSN: | 1932-6203 |
| Popis: | The basal ganglia (BG) is a collection of nuclei located deep beneath the cerebral cortex that is involved in learning and selection of rewarded actions. Here, we analyzed BG mechanisms that enable these functions. We implemented a rate model of a BG-thalamo-cortical loop and simulated its performance in a standard action selection task. We have shown that potentiation of corticostriatal synapses enables learning of a rewarded option. However, these synapses became redundant later as direct connections between prefrontal and premotor cortices (PFC-PMC) were potentiated by Hebbian learning. After we switched the reward to the previously unrewarded option (reversal), the BG was again responsible for switching to the new option. Due to the potentiated direct cortical connections, the system was biased to the previously rewarded choice, and establishing the new choice required a greater number of trials. Guided by physiological research, we then modified our model to reproduce pathological states of mild Parkinson’s and Huntington’s diseases. We found that in the Parkinsonian state PMC activity levels become extremely variable, which is caused by oscillations arising in the BG-thalamo-cortical loop. The model reproduced severe impairment of learning and predicted that this is caused by these oscillations as well as a reduced reward prediction signal. In the Huntington state, the potentiation of the PFC-PMC connections produced better learning, but altered BG output disrupted expression of the rewarded choices. This resulted in random switching between rewarded and unrewarded choices resembling an exploratory phase that never ended. Our results reconcile the apparent contradiction between the critical involvement of the BG in execution of previously learned actions and yet no impairment of these actions after BG output is ablated by lesions or deep brain stimulation. We predict that the cortico-BG-thalamo-cortical loop conforms to previously learned choice in healthy conditions, but impedes those choices in disease states.Author summaryLearning and selection of a rewarded action, as well as avoiding punishments, are known to involve interaction of cortical and subcortical structures in the brain. The subcortical structure that is included in this interaction is called Basal Ganglia (BG). Accordingly, diseases that damage BG, such as Parkinson and Huntington, disrupt action selection functions. A long-standing puzzle is that abolition of the BG output that disconnects the BG-cortical interaction does not disrupt execution of previously learned actions. This is the principle that is suggested to underlie standard Parkinsonian treatments, such as deep brain stimulation. We model the BG-cortical interaction and reconcile this apparent contradiction. Our simulations show that, while BG is necessary for learning of new rewarded choices, it is not necessary for the expression of previously learned actions. Our model predicts that the BG conforms to previously learned choice in healthy conditions, but impedes those choices in disease states. |
| Databáze: | OpenAIRE |
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