A theory of geometric constraints on neural activity for natural three-dimensional movement.
Although the orientation of an arm in space or the static view of an object may be represented by a population of neurons in complex ways, how these variables change with movement often follows simple linear rules, reflecting the underlying geometric constraints in the physical world. A theoretical analysis is presented for how such constraints affect the average firing rates of sensory and motor neurons during natural movements with low degrees of freedom, such as a limb movement and rigid object motion. When applied to nonrigid reaching arm movements, the linear theory accounts for cosine directional tuning with linear speed modulation, predicts a curl-free spatial distribution of preferred directions, and also explains why the instantaneous motion of the hand can be recovered from the neural population activity. For three-dimensional motion of a rigid object, the theory predicts that, to a first approximation, the response of a sensory neuron should have a preferred translational direction and a preferred rotation axis in space, both with cosine tuning functions modulated multiplicatively by speed and angular speed, respectively. Some known tuning properties of motion-sensitive neurons follow as special cases. Acceleration tuning and nonlinear speed modulation are considered in an extension of the linear theory. This general approach provides a principled method to derive mechanism-insensitive neuronal properties by exploiting the inherently low dimensionality of natural movements.
Zhang
K
K
Howard Hughes Medical Institute, Computational Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla, California 92037, USA.
Sejnowski
T J
TJ
D000818:Animals; D019054:Evoked Potentials, Motor / Q000502:physiology; D006801:Humans; D016014:Linear Models; D008433:Mathematics; D009039:Motion Perception / Q000502:physiology; D009068:Movement / Q000502:physiology*; D009474:Neurons / Q000502:physiology*; D009949:Orientation / Q000502:physiology*; D013037:Spatial Behavior / Q000502:physiology*