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

Neuroimage. 2021 Oct 15:240:118283. doi: 10.1016/j.neuroimage.2021.118283. Epub 2021 Jun 17.

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 (mainly medial pulvinar) 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 fronto-parietal cortex and along the superior temporal sulcus (STS) including putative face patch locations, as well as in extrastriate cortex. LIP microstimulation elicited strong activity in the opposite homotopic LIP while no homotopic activation was found with dPul stimulation. Both dPul and LIP stimulation also elicited activity in several heterotopic cortical areas in the opposite hemisphere, implying polysynaptic propagation of excitation. 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 dissimilar ventral pulvinar also showed distinct connectivity. On the level of single trial timecourses within each region of interest (ROI), most ROIs did not show task-dependence of stimulation-elicited response modulation. Across ROIs, however, there was an interaction between task and 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 pulvinar and LIP, 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.

Keywords: Eye movements; Fixation; Macaque monkeys; Memory saccades; Spatial selectivity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Electric Stimulation / methods
  • Macaca mulatta
  • Magnetic Resonance Imaging / methods*
  • Male
  • Microelectrodes
  • Nerve Net / diagnostic imaging
  • Nerve Net / physiology*
  • Parietal Lobe / diagnostic imaging
  • Parietal Lobe / physiology*
  • Pulvinar / diagnostic imaging
  • Pulvinar / physiology*
  • Saccades / physiology*
  • Spatial Behavior / physiology*