The role of pulvinar during perceptual decision-making and thalamic interactions with cardiac and respiratory activity in macaques
Doctoral thesis
Date of Examination:2022-08-23
Date of issue:2023-08-22
Advisor:Dr. Igor Kagan
Referee:Dr. Igor Kagan
Referee:Prof. Dr. Melanie Wilke
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Abstract
English
The dorsal pulvinar (dPul), a higher-order thalamic hub, is instrumental in spatial orienting and selecting stimuli in our environment by gating cortico-thalamic-cortical communication. However, its precise role in perceptual decision-making, particularly under conditions of spatial competition and varying perceptual difficulty, is less understood. Moreover, dPul’s reciprocal connections with the central autonomic network (CAN) hint at its potentially profound influence on how the brain and physiological systems, such as the heart, interact. This thesis explores how the dPul modulates visuospatial cognition, influences perceptual decision processes, and potentially interacts with cardiac and respiratory activity to better understand heart-brain interactions. Chapter 2 examines the dorsal pulvinar’s role in visuospatial cognition by injecting GABA-A agonist THIP into dPul during a color discrimination task with varying difficulty. Utilizing Signal Detection Theory, we predict either a decrease in dprime if dPul inactivation affects perceptual discrimination or a shift in response criterion if dPul inactivation affects spatial orienting. We observed criterion shifts away from contralesional stimuli after inactivation for both difficulty levels, especially when competing peripheral stimuli in opposite hemifields were present. Additionally, saccade latency for the contralesional selection increased, while dprime and overall accuracy remained largely unaffected after inactivation. Using a more epoch-specific perturbation, Chapter 3 builds on this and Dominguez-Vargas et al.'s 2017 findings about increased contraversive target selection in free-choice trials after dPul microstimulation starting after the target onset (“late”). Late dPul microstimulation had little impact on contraversive criterion and dprime. We primarily observed criterion shifts away from ipsiversive stimuli, manifesting as reluctance to select ipsiversive stimuli. After early microstimulation, similar effects were observed as in the inactivation study. Together, our results underline the critical contribution of the dorsal pulvinar to spatial orienting while being less important for perceptual discrimination. In Chapter 4, we tested whether the dPul generally interacts with the CAN and cardiovascular system beyond a specific emotional content remains unknown. We found that suppressing the neural activity of the dPul pharmacologically decreased the heart and respiration rates of two out of three monkeys. Moreover, the RMSSD, as a measure of the heart rate variability, decreased after dPul inactivation in one monkey (M1). We conclude that suppressing the dorsal pulvinar’s neural activity impacts the heart and respiration rate, emphasizing the crucial role of the dPul in arousal-related processing. In the electrophysiology study, a significant proportion of thalamic neurons displayed robust coupling between their spiking activity and the cardiac cycle during the task (ventral posterior lateral nucleus (VPL): 88%, dPul and mediodorsal thalamus (MD): 68%). After analyzing the signal-to-noise ratio and firing rate changes, we found no sign of instability from potential cardiac mechanical influences. The identified link between dPul and the heart’s rhythm indicates dPul’s role in integrating multisensory and arousal-related signals. This insight enhances our understanding of heart-brain dynamics. Considering the medial pulvinar’s high density of alpha receptors, it raises questions regarding an intertwined neural mechanism for spatial attention and arousal in the dPul. Together, these results prompt a re-evaluation of the thalamus’s function in neuro-cardiological processes.
Keywords: perceptual decision; eye movements; distractors; pulvinar; macaque; ECG; respiration; spatial choice