Spatiotemporal Profile of Voltage-Sensitive Dye Responses in the Visual Cortex of Tree Shrews Evoked by Electric Microstimulation of the Dorsal Lateral Geniculate and Pulvinar Nuclei

Abstract

The primary visual cortex (V1) receives its main thalamic drive from the dorsal lateral geniculate nucleus (dLGN) through synaptic contacts terminating primarily in cortical layer IV. In contrast, the projections from the pulvinar nucleus to the cortex are less clearly defined. The pulvinar projects predominantly to layer I in V1, and layer IV in extrastriate areas. These projection patterns suggest that the pulvinar nucleus most strongly influences (drives) activity in cortical areas beyond V1. Should this hypothesis be true, one would expect the spatiotemporal responses evoked by pulvinar activation to be different in V1 and extrastriate areas, reflecting the different connectivity patterns. We investigated this issue by analyzing the spatiotemporal dynamics of cortical visual areas' activity following thalamic electrical microstimulation in tree shrews, using optical imaging and voltage-sensitive dyes. As expected, electrical stimulation of the dLGN induced fast and local responses in V1, as well as in extrastriate and contralateral cortical areas. In contrast, electrical stimulation of the pulvinar induced fast and local responses in extrastriate areas, followed by weak and diffuse activation in V1 and contralateral cortical areas. This study highlights spatiotemporal cortical activation characteristics induced by stimulation of first (dLGN) and high-order (pulvinar) thalamic nuclei.

Significance statement: The pulvinar nucleus represents the main extrageniculate thalamic visual structure in higher-order mammals, but its exact role remains enigmatic. The pulvinar receive prominent inputs from virtually all visual cortical areas. Cortico-thalamo-cortical pathways through the pulvinar nuclei may then provide a complementary route for corticocortical information flow. One step toward the understanding of the role of transthalamic corticocortical pathways is to determine the nature of the signals transmitted between the cortex and the thalamus. By performing, for the first time, high spatiotemporal mesoscopic imaging on tree shrews (the primate's closest relative) through the combination of voltage-sensitive dye recordings and brain stimulation, we revealed clear evidence of distinct thalamocortical functional connectivity pattern originating from the geniculate nucleus and the pulvinar nuclei.

Keywords: driver; geniculate nucleus; modulator; pulvinar; thalamocortical connections.

Figure 1.

Retinotopic mapping. A, Left, Responses to a moving bar recorded in the three cortical locations indicated in B (blue, green, and red circles). The bottom inset shows the visual stimulus. B, Map of delay (time-to-peak) to reach the maximum response. Scale bar, 1 mm. C, Diagram showing the correspondence between visual field and the cortical retinotopy. Art, Artifact where the dye did not stain this location.

Figure 2.

Cortical activation evoked by dLGN and pulvinar stimulation. A, Example of averaged (between trials) cortical response maps (in color) overlaid on the basal fluorescence (in gray level) after stimulation of the left dLGN. B, Time-to-peak and latency maps of responses evoked after dLGN stimulation. C, D, Same as A and B but for stimulation of the Pv subdivision of pulvinar. E, Left, Fluorescence time course within area V1 (blue lines) and extrastriate cortex (thick orange lines) in response to dLGN stimulation. Right, Top, Averaged responses across recordings of the whole dataset. Right, Bottom, Normalized time close-up of the responses. Arrows indicate onset latency. F, Same as E but for pulvinar stimulation.

Figure 3.

Properties of the cortical responses evoked by thalamic stimulation. A, Left, Delimitations of the cortical surfaces activated in response to dLGN (red) and pulvinar nuclei (green) stimulation from all animals tested. Data originating from both hemispheres were pooled. Drawings delimit stimulated cortical areas based on the image immediately following response onset. Right, Crosses indicate centers of each ROI presented on the left. B, C, Amplitude and latencies measured in area V1 and extrastriate cortical areas after pulvinar and dLGN stimulations (±SEM across values and number of observation). *p < 0.05, EC, Extrastriate cortex.