Department of Neuroscience, Baylor College of Medicine, Houston, United States
Sheng Liu
State Key Laboratory of Ophthalmology, Zhongshan Opthalmic Center, Sun Yat-sen University, Guangzhou, China
Xiong-Jie Yu
Department of Neuroscience, Baylor College of Medicine, Houston, United States; Zhejiang University Interdisciplinary Institute of Neuroscience and Technology, Zhejiang University, Hangzhou, China; Qiushi Academy for Advanced Studies, Zhejiang University, Hangzhou, China
Raymond Chan
Department of Neuroscience, Baylor College of Medicine, Houston, United States
David Dickman
Department of Neuroscience, Baylor College of Medicine, Houston, United States
Sensory signals undergo substantial recoding when neural activity is relayed from sensors through pre-thalamic and thalamic nuclei to cortex. To explore how temporal dynamics and directional tuning are sculpted in hierarchical vestibular circuits, we compared responses of macaque otolith afferents with neurons in the vestibular and cerebellar nuclei, as well as five cortical areas, to identical three-dimensional translational motion. We demonstrate a remarkable spatio-temporal transformation: otolith afferents carry spatially aligned cosine-tuned translational acceleration and jerk signals. In contrast, brainstem and cerebellar neurons exhibit non-linear, mixed selectivity for translational velocity, acceleration, jerk and position. Furthermore, these components often show dissimilar spatial tuning. Moderate further transformation of translation signals occurs in the cortex, such that similar spatio-temporal properties are found in multiple cortical areas. These results suggest that the first synapse represents a key processing element in vestibular pathways, robustly shaping how self-motion is represented in central vestibular circuits and cortical areas.
