L-DOPA enhances neural direction signals in younger and older adults
Previous studies indicate a role of dopamine in spatial navigation. Although neural representations of direction are an important aspect of spatial cognition, it is not well understood whether dopamine directly affects these representations, or only impacts other aspects of spatial brain function. M...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2022-12-01
|
| Series: | NeuroImage |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811922007911 |
| _version_ | 1811201383470202880 |
|---|---|
| author | Christoph Koch Christian Baeuchl Franka Glöckner Philipp Riedel Johannes Petzold Michael N. Smolka Shu-Chen Li Nicolas W. Schuck |
| author_facet | Christoph Koch Christian Baeuchl Franka Glöckner Philipp Riedel Johannes Petzold Michael N. Smolka Shu-Chen Li Nicolas W. Schuck |
| author_sort | Christoph Koch |
| collection | DOAJ |
| description | Previous studies indicate a role of dopamine in spatial navigation. Although neural representations of direction are an important aspect of spatial cognition, it is not well understood whether dopamine directly affects these representations, or only impacts other aspects of spatial brain function. Moreover, both dopamine and spatial cognition decline sharply during age, raising the question which effect dopamine has on directional signals in the brain of older adults. To investigate these questions, we used a double-blind cross-over L-DOPA/Placebo intervention design in which 43 younger and 37 older adults navigated in a virtual spatial environment while undergoing functional magnetic resonance imaging (fMRI). We studied the effect of L-DOPA, a dopamine precursor, on fMRI activation patterns that encode spatial walking directions that have previously been shown to lose specificity with age. This was done in predefined regions of interest, including the early visual cortex, retrosplenial cortex, and hippocampus. Classification of brain activation patterns associated with different walking directions was improved across all regions following L-DOPA administration, suggesting that dopamine broadly enhances neural representations of direction. No evidence for differences between regions was found. In the hippocampus these results were found in both age groups, while in the retrosplenial cortex they were only observed in younger adults. Taken together, our study provides evidence for a link between dopamine and the specificity of neural responses during spatial navigation. Significance Statement: The sense of direction is an important aspect of spatial navigation, and neural representations of direction can be found throughout a large network of space-related brain regions. But what influences how well these representations track someone’s true direction? Using a double-blind cross-over L-DOPA/Placebo intervention design, we find causal evidence that the neurotransmitter dopamine impacts the fidelity of direction selective neural representations in the human hippocampus and retrosplenial cortex. Interestingly, the effect of L-DOPA was either equally present or even smaller in older adults, despite the well-known age related decline of dopamine. These results provide novel insights into how dopamine shapes the neural representations that underlie spatial navigation. |
| first_indexed | 2024-04-12T02:19:55Z |
| format | Article |
| id | doaj.art-5a32e97feb314796abbcc70e042f6a21 |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-04-12T02:19:55Z |
| publishDate | 2022-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-5a32e97feb314796abbcc70e042f6a212022-12-22T03:52:08ZengElsevierNeuroImage1095-95722022-12-01264119670L-DOPA enhances neural direction signals in younger and older adultsChristoph Koch0Christian Baeuchl1Franka Glöckner2Philipp Riedel3Johannes Petzold4Michael N. Smolka5Shu-Chen Li6Nicolas W. Schuck7Max Planck Research Group NeuroCode, Max Planck Institute for Human Development, Berlin, Germany; International Max Planck Research School on the Life Course, Max Planck Institute for Human Development, Berlin, Germany; Corresponding author.Faculty of Psychology, Chair of Lifespan Developmental Neuroscience, Technische Universität Dresden, Dresden, GermanyFaculty of Psychology, Chair of Lifespan Developmental Neuroscience, Technische Universität Dresden, Dresden, GermanyDepartment of Psychiatry, Technische Universität Dresden, Dresden, GermanyDepartment of Psychiatry, Technische Universität Dresden, Dresden, GermanyDepartment of Psychiatry, Technische Universität Dresden, Dresden, GermanyFaculty of Psychology, Chair of Lifespan Developmental Neuroscience, Technische Universität Dresden, Dresden, Germany; Centre for Tactile Internet with Human-in-the-Loop (CeTI), Technische Universität, Dresden, GermanyMax Planck Research Group NeuroCode, Max Planck Institute for Human Development, Berlin, Germany; Max Planck UCL Centre for Computational Psychiatry and Aging Research, Berlin, Germany; Institute of Psychology, Universität Hamburg, Hamburg, GermanyPrevious studies indicate a role of dopamine in spatial navigation. Although neural representations of direction are an important aspect of spatial cognition, it is not well understood whether dopamine directly affects these representations, or only impacts other aspects of spatial brain function. Moreover, both dopamine and spatial cognition decline sharply during age, raising the question which effect dopamine has on directional signals in the brain of older adults. To investigate these questions, we used a double-blind cross-over L-DOPA/Placebo intervention design in which 43 younger and 37 older adults navigated in a virtual spatial environment while undergoing functional magnetic resonance imaging (fMRI). We studied the effect of L-DOPA, a dopamine precursor, on fMRI activation patterns that encode spatial walking directions that have previously been shown to lose specificity with age. This was done in predefined regions of interest, including the early visual cortex, retrosplenial cortex, and hippocampus. Classification of brain activation patterns associated with different walking directions was improved across all regions following L-DOPA administration, suggesting that dopamine broadly enhances neural representations of direction. No evidence for differences between regions was found. In the hippocampus these results were found in both age groups, while in the retrosplenial cortex they were only observed in younger adults. Taken together, our study provides evidence for a link between dopamine and the specificity of neural responses during spatial navigation. Significance Statement: The sense of direction is an important aspect of spatial navigation, and neural representations of direction can be found throughout a large network of space-related brain regions. But what influences how well these representations track someone’s true direction? Using a double-blind cross-over L-DOPA/Placebo intervention design, we find causal evidence that the neurotransmitter dopamine impacts the fidelity of direction selective neural representations in the human hippocampus and retrosplenial cortex. Interestingly, the effect of L-DOPA was either equally present or even smaller in older adults, despite the well-known age related decline of dopamine. These results provide novel insights into how dopamine shapes the neural representations that underlie spatial navigation.http://www.sciencedirect.com/science/article/pii/S1053811922007911Spatial navigationAgingNeural dedifferentiationTuning functionsfMRIMVPA |
| spellingShingle | Christoph Koch Christian Baeuchl Franka Glöckner Philipp Riedel Johannes Petzold Michael N. Smolka Shu-Chen Li Nicolas W. Schuck L-DOPA enhances neural direction signals in younger and older adults NeuroImage Spatial navigation Aging Neural dedifferentiation Tuning functions fMRI MVPA |
| title | L-DOPA enhances neural direction signals in younger and older adults |
| title_full | L-DOPA enhances neural direction signals in younger and older adults |
| title_fullStr | L-DOPA enhances neural direction signals in younger and older adults |
| title_full_unstemmed | L-DOPA enhances neural direction signals in younger and older adults |
| title_short | L-DOPA enhances neural direction signals in younger and older adults |
| title_sort | l dopa enhances neural direction signals in younger and older adults |
| topic | Spatial navigation Aging Neural dedifferentiation Tuning functions fMRI MVPA |
| url | http://www.sciencedirect.com/science/article/pii/S1053811922007911 |
| work_keys_str_mv | AT christophkoch ldopaenhancesneuraldirectionsignalsinyoungerandolderadults AT christianbaeuchl ldopaenhancesneuraldirectionsignalsinyoungerandolderadults AT frankaglockner ldopaenhancesneuraldirectionsignalsinyoungerandolderadults AT philippriedel ldopaenhancesneuraldirectionsignalsinyoungerandolderadults AT johannespetzold ldopaenhancesneuraldirectionsignalsinyoungerandolderadults AT michaelnsmolka ldopaenhancesneuraldirectionsignalsinyoungerandolderadults AT shuchenli ldopaenhancesneuraldirectionsignalsinyoungerandolderadults AT nicolaswschuck ldopaenhancesneuraldirectionsignalsinyoungerandolderadults |