Subspace mapping of the three-dimensional spectral receptive field of macaque MT neurons

Neurons in the middle temporal (MT) visual area are thought to represent the velocity (direction and speed) of motion. Previous studies suggest the importance of both excitation and suppression for creating velocity representation in MT; however, details of the organization of excitation and suppression at the MT stage are not understood fully. Here, we examine how excitatory and suppressive inputs are pooled in individual MT neurons by measuring their receptive fields in a three-dimensional (3-D) spatiotemporal frequency domain. We recorded the activity of single MT neurons from anesthetized macaque monkeys. To achieve both quality and resolution of the receptive field estimations, we applied a subspace reverse correlation technique in which a stimulus sequence of superimposed multiple drifting gratings was cross-correlated with the spiking activity of neurons. Excitatory responses tended to be organized in a manner representing a specific velocity independent of the spatial pattern of the stimuli. Conversely, suppressive responses tended to be distributed broadly over the 3-D frequency domain, supporting a hypothesis of response normalization. In spite of the nonspecific distributed profile, the total summed strength of suppression was comparable to that of excitation in many MT neurons. Furthermore, suppressive responses reduced the bandwidth of velocity tuning, indicating that suppression improves the reliability of velocity representation. Our results suggest that both well-organized excitatory inputs and broad suppressive inputs contribute significantly to the invariant and reliable representation of velocity in MT.

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