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Effective connectivity and spatial selectivity-dependent fMRI changes elicited by microstimulation of pulvinar and LIP

View ORCID ProfileIgor Kagan, Lydia Gibson, Elena Spanou, Melanie Wilke
doi: https://doi.org/10.1101/2020.09.16.298539
Igor Kagan
1Decision and Awareness Group, Cognitive Neuroscience Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, Goettingen, 37077, Germany
2Department of Cognitive Neurology, University of Goettingen, Robert-Koch-Str. 40, Goettingen, 37075, Germany
3Leibniz ScienceCampus Primate Cognition, Kellnerweg 4, Goettingen, 37077, Germany
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  • For correspondence: ikagan@dpz.eu
Lydia Gibson
1Decision and Awareness Group, Cognitive Neuroscience Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, Goettingen, 37077, Germany
2Department of Cognitive Neurology, University of Goettingen, Robert-Koch-Str. 40, Goettingen, 37075, Germany
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  • For correspondence: ikagan@dpz.eu
Elena Spanou
1Decision and Awareness Group, Cognitive Neuroscience Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, Goettingen, 37077, Germany
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Melanie Wilke
1Decision and Awareness Group, Cognitive Neuroscience Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, Goettingen, 37077, Germany
2Department of Cognitive Neurology, University of Goettingen, Robert-Koch-Str. 40, Goettingen, 37075, Germany
3Leibniz ScienceCampus Primate Cognition, Kellnerweg 4, Goettingen, 37077, Germany
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Abstract

The thalamic pulvinar and the lateral intraparietal area (LIP) share reciprocal anatomical connections and are part of an extensive cortical and subcortical network involved in spatial attention and oculomotor processing. The goal of this study was to compare the effective connectivity of dorsal pulvinar (dPul) and LIP and to probe the dependency of microstimulation effects on task demands and spatial tuning properties of a given brain region. To this end, we applied unilateral electrical microstimulation in the dPul and LIP in combination with event-related BOLD fMRI in monkeys performing fixation and memory-guided saccade tasks. Microstimulation in both dPul and LIP enhanced task-related activity in monosynaptically-connected prefrontal cortex and along the superior temporal sulcus (STS) as well as in extrastriate cortex. Both dPul and LIP stimulation also elicited activity in several cortical areas in the opposite hemisphere, implying polysynaptic propagation of excitation. LIP microstimulation elicited strong activity in the opposite homotopic LIP while no homotopic activation was found during dPul stimulation. Despite extensive activation along the intraparietal sulcus evoked by LIP stimulation, there was a difference in frontal and occipital connectivity elicited by posterior and anterior LIP stimulation sites. Comparison of dPul stimulation with the adjacent but functionally distinct ventral pulvinar also showed distinct connectivity. On the level of single trial timecourses within a region, most microstimulation regions did not show task-dependence of stimulation-elicited response modulation. Across regions, however, there was an interaction between the task and the stimulation, and task-specific correlations between the initial spatial selectivity and the magnitude of stimulation effect were observed. Consequently, stimulation-elicited modulation of task-related activity was best fitted by an additive model scaled down by the initial response amplitude. In summary, we identified overlapping and distinct patterns of thalamocortical and corticocortical connectivity of the two key visuospatial areas, highlighting the dorsal bank and fundus of STS as a prominent node of shared circuitry. Spatial task-specific and partly polysynaptic modulations of cue and saccade planning delay period activity in both hemispheres exerted by unilateral pulvinar and parietal stimulation provide insight into the distributed interhemispheric processing underlying spatial behavior.

  • Electrical stimulation of pulvinar and LIP was used to study fMRI effective connectivity

  • Both regions activated prefrontal cortex and the dorsal bank of superior temporal sulcus

  • Activations within and across hemispheres suggest polysynaptic propagation

  • Stimulation effects show interactions between task- and spatial selectivity

  • Stimulation effects are best fitted by an additive model scaled by the initial response

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 17, 2020.
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Effective connectivity and spatial selectivity-dependent fMRI changes elicited by microstimulation of pulvinar and LIP
Igor Kagan, Lydia Gibson, Elena Spanou, Melanie Wilke
bioRxiv 2020.09.16.298539; doi: https://doi.org/10.1101/2020.09.16.298539
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Effective connectivity and spatial selectivity-dependent fMRI changes elicited by microstimulation of pulvinar and LIP
Igor Kagan, Lydia Gibson, Elena Spanou, Melanie Wilke
bioRxiv 2020.09.16.298539; doi: https://doi.org/10.1101/2020.09.16.298539

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