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.

As you move through the environment, you see a radial pattern of visual motion with a focus of expansion (FOE) that indicates your heading direction. When self-movement is combined with smooth pursuit eye movements, the turning of the eye distorts the retinal image of the FOE but somehow you still can perceive heading. We studied neurons in the medial superior temporal area (MST) of monkey visual cortex, recording responses to FOE stimuli presented during fixation and smooth pursuit eye movements. Almost all neurons showed significant changes in their FOE selective responses during pursuit eye movements. However, the vector average of all the neuronal responses indicated the direction of the FOE during both fixation and pursuit. Furthermore, the amplitude of the net vector increased with increasing FOE eccentricity. We conclude that neuronal population encoding in MST might contribute to pursuit-tolerant heading perception.

Basis functions have been extensively used in models of neural computation because they can be combined linearly to approximate any nonlinear functions of the encoded variables. We investigated whether dorsal medial superior temporal (MSTd) area neurons use basis functions to simultaneously encode heading direction, eye position, and the velocity of ocular pursuit. Using optimal linear estimators, we first show that the head-centered and eye-centered position of a focus of expansion (FOE) in optic flow, pursuit direction, and eye position can all be estimated from the single-trial responses of 144 MSTd neurons with an average accuracy of 2-3 degrees, a value consistent with the discrimination thresholds measured in humans and monkeys. We then examined the format of the neural code for the head-centered position of the FOE, eye position, and pursuit direction. The basis function hypothesis predicts that a large majority of cells in MSTd should encode two or more signals simultaneously and combine these signals nonlinearly. Our analysis shows that 95% of the neurons encode two or more signals, whereas 76% code all three signals. Of the 95% of cells encoding two or more signals, 90% show nonlinear interactions between the encoded variables. These findings support the notion that MSTd may use basis functions to represent the FOE in optic flow, eye position, and pursuit.

Yu CP, Page WK, Gaborski R, Duffy CJ. Receptive field dynamics underlying MST neuronal optic flow selectivity. J Neurophysiol 103: 2794 -2807, 2010. First published March 24, 2010 doi:10.1152/jn.01085.2009. Optic flow informs moving observers about their heading direction. Neurons in monkey medial superior temporal (MST) cortex show heading selective responses to optic flow and planar direction selective responses to patches of local motion. We recorded MST neuronal responses to a 90 ϫ 90°optic flow display and to a 3 ϫ 3 array of local motion patches covering the same area. Our goal was to test the hypothesis that the optic flow responses reflect the sum of the local motion responses. The local motion responses of each neuron were modeled as mixtures of Gaussians, combining the effects of two Gaussian response functions derived using a genetic algorithm, and then used to predict that neuron's optic flow responses. Some neurons showed good correspondence between local motion models and optic flow responses, others showed substantial differences. We used the genetic algorithm to modulate the relative strength of each local motion segment's responses to accommodate interactions between segments that might modulate their relative efficacy during co-activation by global patterns of optic flow. These gain modulated models showed uniformly better fits to the optic flow responses, suggesting that coactivation of receptive field segments alters neuronal response properties. We tested this hypothesis by simultaneously presenting local motion stimuli at two different sites. These two-segment stimuli revealed that interactions between response segments have direction and location specific effects that can account for aspects of optic flow selectivity. We conclude that MST's optic flow selectivity reflects dynamic interactions between spatially distributed local planar motion response mechanisms.

We hypothesized that neuronal responses to virtual self-movement would be enhanced during steering tasks. We recorded the activity of medial superior temporal (MSTd) neurons in monkeys trained to steer a straight-ahead course, using optic flow. We found smaller optic flow responses during active steering than during the passive viewing of the same stimuli. Behavioral analysis showed that the monkeys had learned to steer using local motion cues. Retraining the monkeys to use the global pattern of optic flow reversed the effects of the active-steering task: active steering then evoked larger responses than passive viewing. We then compared the responses of neurons during active steering by local motion and by global patterns: Local motion trials promoted the use of local dot movement near the center of the stimulus by occluding the peripheral visual field midway through the trial. Global pattern trials promoted the use of radial pattern movement by occluding the central visual field midway through the trial. In this study, identical full-field optic-flow stimuli evoked larger responses in global-pattern trials than in local motion trials. We conclude that the selection of specific visual cues reflects strategies for active steering and alters MSTd neuronal responses to optic flow.