A sensory-motor decoder that transforms neural responses in extrastriate area MT into smooth pursuit eye movements

Visual motion drives smooth pursuit eye movements through a sensory-motor decoder that uses multiple parallel neural pathways to transform the population response in extrastriate area MT into movement. We evaluated the decoder by challenging pursuit in monkeys with reduced motion reliability created by reducing coherence of motion in patches of dots. Our strategy was to determine how reduced dot coherence changes the population response in MT. We then predicted the properties of a decoder that transforms the MT population response into dot coherence-induced deficits in the initiation of pursuit and steady-state tracking. During pursuit initiation, decreased dot coherence reduces MT population response amplitude without changing the preferred speed at its peak. The successful decoder reproduces the measured eye movements by multiplication of 1) the estimate of target speed from the peak of the population response with 2) visual-motor gain based on the amplitude of the population response. During steady-state tracking, the decoder that worked for pursuit initiation failed to reproduce the paradox that steady-state eye speeds do not accelerate to the target speed despite persistent image motion. It predicted eye acceleration to target speed even when monkeys' eye speeds were steady at well below the target speed. To account for the effect of dot coherence on steady-state eye speed, we postulate that the decoder uses sensory-motor gain to modulate the eye velocity positive feedback that normally sustains perfect steady-state tracking. Then, poor steady-state tracking persists because of balance between eye deceleration caused by low positive feedback gain and acceleration driven by MT.NEW & NOTEWORTHY By challenging a sensory-motor system with degraded sensory stimuli, we reveal how the sensory-motor decoder transforms the population response in extrastriate area MT into commands for the initiation and steady-state behavior of smooth pursuit eye movements. Conclusions are based on measuring population responses in MT for multiple target speeds and different levels of motion reliability and evaluating a decoder with a biologically motivated architecture to determine the decoder properties that create the measured eye movements.