Instantaneous movement-unrelated midbrain activity modifies ongoing eye movements
- Tübingen University, Germany
Abstract
At any moment in time, new information is sampled from the environment and interacts with ongoing brain state. Often, such interaction takes place within individual circuits that are capable of both mediating the internally ongoing plan as well as representing exogenous sensory events. Here we investigated how sensory-driven neural activity can be integrated, very often in the same neuron types, into ongoing saccade motor commands. Despite the ballistic nature of saccades, visually-induced action potentials in the rhesus macaque superior colliculus (SC), a structure known to drive eye movements, not only occurred intra-saccadically, but they were also associated with highly predictable modifications of ongoing eye movements. Such predictable modifications reflected a simultaneity of movement-related discharge at one SC site and visually-induced activity at another. Our results suggest instantaneous readout of the SC during movement generation, irrespective of activity source, and they explain a significant component of kinematic variability of motor outputs.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all figures.
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft (FOR1847 (project A6: HA6749/2-1))
- Antimo Buonocore
- Ziad M Hafed
Deutsche Forschungsgemeinschaft (DFG EXC307)
- Antimo Buonocore
- Ziad M Hafed
Deutsche Forschungsgemeinschaft (SFB1233; TP 11; project number 276693517)
- Fatemeh Khademi
- Ziad M Hafed
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: The experiments were approved (licenses: CIN3/13; CIN4/19G) by ethics committees at the regional governmental offices of the city of Tuebingen and were in accordance with European Union guidelines on animal research and the associated implementations of these guidelines in German law.
Copyright
© 2021, Buonocore et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,001
- views
-
- 142
- downloads
-
- 19
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Instantaneous movement-unrelated midbrain activity modifies ongoing eye movements
eLife 10:e64150.
https://doi.org/10.7554/eLife.64150
Further reading
-
- Neuroscience
When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
-
- Neuroscience
When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.
