Dorsal medial superior temporal cortex (MSTd)'s population response encodes heading direction from optic flow seen during fixation or pursuit. Vestibular responses in these neurons might enhance heading representation during self-movement in light or provide an alternative basis for heading representation during self-movement in darkness. We have compared these hypotheses by recording MSTd neuronal responses to translational self-movement in light and darkness, during fixation and pursuit. Translational movement in darkness, with gaze fixed, evokes transient vestibular responses during acceleration that reverse directionality during deceleration and persist without a fixation target. Movement in light increases the amplitude and duration of these responses so they mimic responses to simulated optic flow presented without translational movement. Pursuit of a stationary landmark during translational movement combines vestibular and visual effects with pursuit responses. Vestibular, visual, and pursuit effects interact so that single neuron heading responses vary across the stimulus period and between stimulus conditions. Combining single neuron responses by population vector summation yields stronger heading estimates in light than in darkness, with gaze fixed or during landmark pursuit. Adding translational movement to robust optic flow stimuli does not augment the population response. Vestibular signals enhance single neuron responses in light and maintain population heading estimation in darkness, potentially extending MSTd's heading representation across the continuum of naturalistic self-movement conditions.
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