Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions.
Anterior cingulate cortex (ACC) and striatum (STR) contain neurons encoding not only the expected values of actions, but also the value of stimulus features irrespective of actions. Values about stimulus features in ACC or STR might contribute to adaptive behavior by guiding fixational information s...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2022-09-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3001785 |
| _version_ | 1811238956943015936 |
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| author | Kianoush Banaie Boroujeni Michelle K Sigona Robert Louie Treuting Thomas J Manuel Charles F Caskey Thilo Womelsdorf |
| author_facet | Kianoush Banaie Boroujeni Michelle K Sigona Robert Louie Treuting Thomas J Manuel Charles F Caskey Thilo Womelsdorf |
| author_sort | Kianoush Banaie Boroujeni |
| collection | DOAJ |
| description | Anterior cingulate cortex (ACC) and striatum (STR) contain neurons encoding not only the expected values of actions, but also the value of stimulus features irrespective of actions. Values about stimulus features in ACC or STR might contribute to adaptive behavior by guiding fixational information sampling and biasing choices toward relevant objects, but they might also have indirect motivational functions by enabling subjects to estimate the value of putting effort into choosing objects. Here, we tested these possibilities by modulating neuronal activity in ACC and STR of nonhuman primates using transcranial ultrasound stimulation while subjects learned the relevance of objects in situations with varying motivational and cognitive demands. Motivational demand was indexed by varying gains and losses during learning, while cognitive demand was varied by increasing the uncertainty about which object features could be relevant during learning. We found that ultrasound stimulation of the ACC, but not the STR, reduced learning efficiency and prolonged information sampling when the task required averting losses and motivational demands were high. Reduced learning efficiency was particularly evident at higher cognitive demands and when subjects experienced loss of already attained tokens. These results suggest that the ACC supports flexible learning of feature values when loss experiences impose a motivational challenge and when uncertainty about the relevance of objects is high. Taken together, these findings provide causal evidence that the ACC facilitates resource allocation and improves visual information sampling during adaptive behavior. |
| first_indexed | 2024-04-12T12:51:25Z |
| format | Article |
| id | doaj.art-3e001eb6b46441c7bb732853e313706e |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-04-12T12:51:25Z |
| publishDate | 2022-09-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-3e001eb6b46441c7bb732853e313706e2022-12-22T03:32:27ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852022-09-01209e300178510.1371/journal.pbio.3001785Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions.Kianoush Banaie BoroujeniMichelle K SigonaRobert Louie TreutingThomas J ManuelCharles F CaskeyThilo WomelsdorfAnterior cingulate cortex (ACC) and striatum (STR) contain neurons encoding not only the expected values of actions, but also the value of stimulus features irrespective of actions. Values about stimulus features in ACC or STR might contribute to adaptive behavior by guiding fixational information sampling and biasing choices toward relevant objects, but they might also have indirect motivational functions by enabling subjects to estimate the value of putting effort into choosing objects. Here, we tested these possibilities by modulating neuronal activity in ACC and STR of nonhuman primates using transcranial ultrasound stimulation while subjects learned the relevance of objects in situations with varying motivational and cognitive demands. Motivational demand was indexed by varying gains and losses during learning, while cognitive demand was varied by increasing the uncertainty about which object features could be relevant during learning. We found that ultrasound stimulation of the ACC, but not the STR, reduced learning efficiency and prolonged information sampling when the task required averting losses and motivational demands were high. Reduced learning efficiency was particularly evident at higher cognitive demands and when subjects experienced loss of already attained tokens. These results suggest that the ACC supports flexible learning of feature values when loss experiences impose a motivational challenge and when uncertainty about the relevance of objects is high. Taken together, these findings provide causal evidence that the ACC facilitates resource allocation and improves visual information sampling during adaptive behavior.https://doi.org/10.1371/journal.pbio.3001785 |
| spellingShingle | Kianoush Banaie Boroujeni Michelle K Sigona Robert Louie Treuting Thomas J Manuel Charles F Caskey Thilo Womelsdorf Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions. PLoS Biology |
| title | Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions. |
| title_full | Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions. |
| title_fullStr | Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions. |
| title_full_unstemmed | Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions. |
| title_short | Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions. |
| title_sort | anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions |
| url | https://doi.org/10.1371/journal.pbio.3001785 |
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