Bounded rational decision-making models suggest capacity-limited concurrent motor planning in human posterior parietal and frontal cortex
While traditional theories of sensorimotor processing have often assumed a serial decision-making pipeline, more recent approaches have suggested that multiple actions may be planned concurrently and vie for execution. Evidence for the latter almost exclusively stems from electrophysiological studie...
| Main Authors: | , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2022-10-01
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| Series: | PLoS Computational Biology |
| Online Access: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9560147/?tool=EBI |
| _version_ | 1811238903704715264 |
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| author | Sonja Schach Axel Lindner Daniel Alexander Braun |
| author_facet | Sonja Schach Axel Lindner Daniel Alexander Braun |
| author_sort | Sonja Schach |
| collection | DOAJ |
| description | While traditional theories of sensorimotor processing have often assumed a serial decision-making pipeline, more recent approaches have suggested that multiple actions may be planned concurrently and vie for execution. Evidence for the latter almost exclusively stems from electrophysiological studies in posterior parietal and premotor cortex of monkeys. Here we study concurrent prospective motor planning in humans by recording functional magnetic resonance imaging (fMRI) during a delayed response task engaging movement sequences towards multiple potential targets. We find that also in human posterior parietal and premotor cortex delay activity modulates both with sequence complexity and the number of potential targets. We tested the hypothesis that this modulation is best explained by concurrent prospective planning as opposed to the mere maintenance of potential targets in memory. We devise a bounded rationality model with information constraints that optimally assigns information resources for planning and memory for this task and determine predicted information profiles according to the two hypotheses. When regressing delay activity on these model predictions, we find that the concurrent prospective planning strategy provides a significantly better explanation of the fMRI-signal modulations. Moreover, we find that concurrent prospective planning is more costly and thus limited for most subjects, as expressed by the best fitting information capacities. We conclude that bounded rational decision-making models allow relating both behavior and neural representations to utilitarian task descriptions based on bounded optimal information-processing assumptions. Author summary When the future is uncertain, it can be beneficial to concurrently plan several action possibilities in advance. Electrophysiological research found evidence in monkeys that brain regions in posterior parietal and promotor cortex are indeed capable of planning several actions in parallel. We now used fMRI to study brain activity in these brain regions in humans. For our analyses we applied bounded rationality models that optimally assign information resources to fMRI activity in a complex motor planning task. We find that theoretical information costs of concurrent prospective planning explained fMRI activity profiles significantly better than assuming alternative memory-based strategies. Moreover, exploiting the model allowed us to quantify the individual capacity limit for concurrent planning and to relate these individual limits to both subjects’ behavior and to their neural representations of planning. |
| first_indexed | 2024-04-12T12:50:27Z |
| format | Article |
| id | doaj.art-50d7212bacea4f8db66ba90ca302f9e1 |
| institution | Directory Open Access Journal |
| issn | 1553-734X 1553-7358 |
| language | English |
| last_indexed | 2024-04-12T12:50:27Z |
| publishDate | 2022-10-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Computational Biology |
| spelling | doaj.art-50d7212bacea4f8db66ba90ca302f9e12022-12-22T03:32:29ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582022-10-011810Bounded rational decision-making models suggest capacity-limited concurrent motor planning in human posterior parietal and frontal cortexSonja SchachAxel LindnerDaniel Alexander BraunWhile traditional theories of sensorimotor processing have often assumed a serial decision-making pipeline, more recent approaches have suggested that multiple actions may be planned concurrently and vie for execution. Evidence for the latter almost exclusively stems from electrophysiological studies in posterior parietal and premotor cortex of monkeys. Here we study concurrent prospective motor planning in humans by recording functional magnetic resonance imaging (fMRI) during a delayed response task engaging movement sequences towards multiple potential targets. We find that also in human posterior parietal and premotor cortex delay activity modulates both with sequence complexity and the number of potential targets. We tested the hypothesis that this modulation is best explained by concurrent prospective planning as opposed to the mere maintenance of potential targets in memory. We devise a bounded rationality model with information constraints that optimally assigns information resources for planning and memory for this task and determine predicted information profiles according to the two hypotheses. When regressing delay activity on these model predictions, we find that the concurrent prospective planning strategy provides a significantly better explanation of the fMRI-signal modulations. Moreover, we find that concurrent prospective planning is more costly and thus limited for most subjects, as expressed by the best fitting information capacities. We conclude that bounded rational decision-making models allow relating both behavior and neural representations to utilitarian task descriptions based on bounded optimal information-processing assumptions. Author summary When the future is uncertain, it can be beneficial to concurrently plan several action possibilities in advance. Electrophysiological research found evidence in monkeys that brain regions in posterior parietal and promotor cortex are indeed capable of planning several actions in parallel. We now used fMRI to study brain activity in these brain regions in humans. For our analyses we applied bounded rationality models that optimally assign information resources to fMRI activity in a complex motor planning task. We find that theoretical information costs of concurrent prospective planning explained fMRI activity profiles significantly better than assuming alternative memory-based strategies. Moreover, exploiting the model allowed us to quantify the individual capacity limit for concurrent planning and to relate these individual limits to both subjects’ behavior and to their neural representations of planning.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9560147/?tool=EBI |
| spellingShingle | Sonja Schach Axel Lindner Daniel Alexander Braun Bounded rational decision-making models suggest capacity-limited concurrent motor planning in human posterior parietal and frontal cortex PLoS Computational Biology |
| title | Bounded rational decision-making models suggest capacity-limited concurrent motor planning in human posterior parietal and frontal cortex |
| title_full | Bounded rational decision-making models suggest capacity-limited concurrent motor planning in human posterior parietal and frontal cortex |
| title_fullStr | Bounded rational decision-making models suggest capacity-limited concurrent motor planning in human posterior parietal and frontal cortex |
| title_full_unstemmed | Bounded rational decision-making models suggest capacity-limited concurrent motor planning in human posterior parietal and frontal cortex |
| title_short | Bounded rational decision-making models suggest capacity-limited concurrent motor planning in human posterior parietal and frontal cortex |
| title_sort | bounded rational decision making models suggest capacity limited concurrent motor planning in human posterior parietal and frontal cortex |
| url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9560147/?tool=EBI |
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