Author response: A unified internal model theory to resolve the paradox of active versus passive self-motion sensation

Jean Laurens, Dora E. Angelaki · 2017

When seated in a car, we can detect when the vehicle begins to move even with our eyes closed. Structures in the inner ear called the vestibular, or balance, organs enable us to sense our own movement. They do this by detecting head rotations, accelerations and gravity. They then pass this information on to specialized vestibular regions of the brain. Experiments using rotating chairs and moving platforms have shown that passive movements – such as car journeys and rollercoaster rides – activate the brain’s vestibular regions. But recent work has revealed that voluntary movements – in which individuals start the movement themselves – activate these regions far less than passive movements. Does this mean that the brain ignores signals from the inner ear during voluntary movements? Another possibility is that the brain predicts in advance how each movement will affect the vestibular organs in the inner ear. It then compares these predictions with the signals it receives during the movement. Only mismatches between the two activate the brain’s vestibular regions. To test this theory, Laurens and Angelaki created a mathematical model that compares predicted signals with actual signals in the way the theory proposes. The model accurately predicts the patterns of brain activity seen during both active and passive movement. This reconciles the results of previous experiments on active and passive motion. It also suggests that the brain uses similar processes to analyze vestibular signals during both types of movement. These findings can help drive further research into how the brain uses sensory signals to refine our everyday movements. They can also help us understand how people recover from damage to the vestibular system. Most patients with vestibular injuries learn to walk again, but have difficulty walking on uneven ground. They also become disoriented by passive movement. Using the model to study how the brain adapts to loss of vestibular input could lead to new strategies to aid recovery.

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