Encoding of cerebellar dentate neuron activity during visual attention in rhesus macaques
The role of cerebellum in controlling eye movements is well established, but its contribution to more complex forms of visual behavior has remained elusive. To study cerebellar activity during visual attention we recorded extracellular activity of dentate nucleus (DN) neurons in two non-human primat...
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eLife Sciences Publications Ltd
2025-01-01
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| Online Access: | https://elifesciences.org/articles/99696 |
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| author | Nico A Flierman Sue Ann Koay Willem S van Hoogstraten Tom JH Ruigrok Pieter Roelfsema Aleksandra Badura Chris I De Zeeuw |
| author_facet | Nico A Flierman Sue Ann Koay Willem S van Hoogstraten Tom JH Ruigrok Pieter Roelfsema Aleksandra Badura Chris I De Zeeuw |
| author_sort | Nico A Flierman |
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| description | The role of cerebellum in controlling eye movements is well established, but its contribution to more complex forms of visual behavior has remained elusive. To study cerebellar activity during visual attention we recorded extracellular activity of dentate nucleus (DN) neurons in two non-human primates (NHPs). NHPs were trained to read the direction indicated by a peripheral visual stimulus while maintaining fixation at the center, and report the direction of the cue by performing a saccadic eye movement into the same direction following a delay. We found that single-unit DN neurons modulated spiking activity over the entire time course of the task, and that their activity often bridged temporally separated intra-trial events, yet in a heterogeneous manner. To better understand the heterogeneous relationship between task structure, behavioral performance, and neural dynamics, we constructed a behavioral, an encoding, and a decoding model. Both NHPs showed different behavioral strategies, which influenced the performance. Activity of the DN neurons reflected the unique strategies, with the direction of the visual stimulus frequently being encoded long before an upcoming saccade. Moreover, the latency of the ramping activity of DN neurons following presentation of the visual stimulus was shorter in the better performing NHP. Labeling with the retrograde tracer Cholera Toxin B in the recording location in the DN indicated that these neurons predominantly receive inputs from Purkinje cells in the D1 and D2 zones of the lateral cerebellum as well as neurons of the principal olive and medial pons, all regions known to connect with neurons in the prefrontal cortex contributing to planning of saccades. Together, our results highlight that DN neurons can dynamically modulate their activity during a visual attention task, comprising not only sensorimotor but also cognitive attentional components. |
| format | Article |
| id | doaj-art-ee866ac6a53f4d30b1fea6dd04cd36c7 |
| institution | Kabale University |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj-art-ee866ac6a53f4d30b1fea6dd04cd36c72025-01-16T15:11:35ZengeLife Sciences Publications LtdeLife2050-084X2025-01-011310.7554/eLife.99696Encoding of cerebellar dentate neuron activity during visual attention in rhesus macaquesNico A Flierman0https://orcid.org/0000-0003-3911-8228Sue Ann Koay1https://orcid.org/0000-0002-9648-2475Willem S van Hoogstraten2https://orcid.org/0000-0002-3635-4893Tom JH Ruigrok3https://orcid.org/0000-0001-5537-1165Pieter Roelfsema4https://orcid.org/0000-0002-1625-0034Aleksandra Badura5https://orcid.org/0000-0002-0119-5108Chris I De Zeeuw6https://orcid.org/0000-0001-5628-8187Netherlands Institute for Neuroscience, Amsterdam, Netherlands; Department of Neuroscience, Erasmus MC, Rotterdam, NetherlandsJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesDepartment of Neuroscience, Erasmus MC, Rotterdam, NetherlandsDepartment of Neuroscience, Erasmus MC, Rotterdam, NetherlandsNetherlands Institute for Neuroscience, Amsterdam, Netherlands; Department of Integrative Neurophysiology, VU University, Amsterdam, Netherlands; Department of Psychiatry, Academic Medical Centre, Amsterdam, NetherlandsDepartment of Neuroscience, Erasmus MC, Rotterdam, NetherlandsNetherlands Institute for Neuroscience, Amsterdam, Netherlands; Department of Neuroscience, Erasmus MC, Rotterdam, NetherlandsThe role of cerebellum in controlling eye movements is well established, but its contribution to more complex forms of visual behavior has remained elusive. To study cerebellar activity during visual attention we recorded extracellular activity of dentate nucleus (DN) neurons in two non-human primates (NHPs). NHPs were trained to read the direction indicated by a peripheral visual stimulus while maintaining fixation at the center, and report the direction of the cue by performing a saccadic eye movement into the same direction following a delay. We found that single-unit DN neurons modulated spiking activity over the entire time course of the task, and that their activity often bridged temporally separated intra-trial events, yet in a heterogeneous manner. To better understand the heterogeneous relationship between task structure, behavioral performance, and neural dynamics, we constructed a behavioral, an encoding, and a decoding model. Both NHPs showed different behavioral strategies, which influenced the performance. Activity of the DN neurons reflected the unique strategies, with the direction of the visual stimulus frequently being encoded long before an upcoming saccade. Moreover, the latency of the ramping activity of DN neurons following presentation of the visual stimulus was shorter in the better performing NHP. Labeling with the retrograde tracer Cholera Toxin B in the recording location in the DN indicated that these neurons predominantly receive inputs from Purkinje cells in the D1 and D2 zones of the lateral cerebellum as well as neurons of the principal olive and medial pons, all regions known to connect with neurons in the prefrontal cortex contributing to planning of saccades. Together, our results highlight that DN neurons can dynamically modulate their activity during a visual attention task, comprising not only sensorimotor but also cognitive attentional components.https://elifesciences.org/articles/99696dentate nucleusvisual attentionheterogeneous activitycognitionprefrontal cortexcerebellum |
| spellingShingle | Nico A Flierman Sue Ann Koay Willem S van Hoogstraten Tom JH Ruigrok Pieter Roelfsema Aleksandra Badura Chris I De Zeeuw Encoding of cerebellar dentate neuron activity during visual attention in rhesus macaques eLife dentate nucleus visual attention heterogeneous activity cognition prefrontal cortex cerebellum |
| title | Encoding of cerebellar dentate neuron activity during visual attention in rhesus macaques |
| title_full | Encoding of cerebellar dentate neuron activity during visual attention in rhesus macaques |
| title_fullStr | Encoding of cerebellar dentate neuron activity during visual attention in rhesus macaques |
| title_full_unstemmed | Encoding of cerebellar dentate neuron activity during visual attention in rhesus macaques |
| title_short | Encoding of cerebellar dentate neuron activity during visual attention in rhesus macaques |
| title_sort | encoding of cerebellar dentate neuron activity during visual attention in rhesus macaques |
| topic | dentate nucleus visual attention heterogeneous activity cognition prefrontal cortex cerebellum |
| url | https://elifesciences.org/articles/99696 |
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