Previous studies in rodents have identified four major cell types that are involved in navigation functions, including head direction (HD), place, grid, and border cells. In rodents, HD cells are reported to encode the direction the head is pointing independent of the animal's behavior or spatial location and have been identified in the anterior thalamus, hippocampus, subiculum, and other parahippocampal regions. Although much has been learned regarding HD cell responses from the rodent model, it has limitations. For example, it has been difficult to determine if HD cells encode head direction or gaze direction. In addition, although lesion studies have shown that HD cell tuning is dependent upon vestibular cues, the type and properties of these signals remain obscure. We propose to examine HD cell responses in rhesus macaques, where answers to these questions can readily be determined. Our first goal will be to localize, characterize, and compare the tuning properties of macaque HD cells in the anterior thalamus and subiculum complex. Our second goal is to determine if HD cells in these two regions encode head direction or gaze direction. We will train macaques to dissociate eye and head position and use Fisher information analysis to determine whether HD cells are more closely related to head direction or gaze direction tuning. We hypothesize that most macaque HD cells encode head direction, although some might be tuned to gaze direction and the relative proportion of each cell type might differ between the anterior thalamus and subiculum. Our third goal is to characterize the three- dimensional, gravity-dependent properties of HD cells during passive rotations in both the light and darkness. The project represents a new area of research through a collaborative effort, with the long-term goal to understand the mechanisms underlying primate spatial navigation.

Public Health Relevance

When our sense of spatial orientation is compromised by central nervous system or vestibular disease, devastating effects upon our ability to orient in familiar environments, navigate from place to place, or even find our way home can occur. The current project seeks to initiate a new field of research regarding how spatial navigation information is generated from vestibular motion signals in the primate brain; a direction that promises to provide a large impact for exploration of spatial navigation deficits suffered by many with dementia or vestibular system loss. How spatial information, navigation, and place memory is generated in primates is a fascinating and important line of inquiry, which remains in its infancy, and the current project was conceived to initiate an opening into a rich area of insight yet to be explored.

National Institute of Health (NIH)
National Institute on Deafness and Other Communication Disorders (NIDCD)
Research Project (R01)
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Sensorimotor Integration Study Section (SMI)
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Poremba, Amy
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Baylor College of Medicine
Schools of Medicine
United States
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Laurens, Jean; Liu, Sheng; Yu, Xiong-Jie et al. (2017) Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex. Elife 6:
Laurens, Jean; Kim, Byounghoon; Dickman, J David et al. (2016) Gravity orientation tuning in macaque anterior thalamus. Nat Neurosci 19:1566-1568