Steering Transforms the Cortical Representation of Self-Movement from Direction to Destination

Abstract

Steering demands rapid responses to heading deviations and uses optic flow to redirect self-movement toward the intended destination. We trained monkeys in a naturalistic steering paradigm and recorded dorsal medial superior temporal area (MSTd) cortical neuronal responses to the visual motion and spatial location cues in optic flow. We found that neuronal responses to the initial heading direction are dominated by the optic flow's global radial pattern cue. Responses to subsequently imposed heading deviations are dominated by the local direction of motion cue. Finally, as the monkey steers its heading back to the goal location, responses are dominated by the spatial location cue, the screen location of the flow field's center of motion. We conclude that MSTd responses are not rigidly linked to specific stimuli, but rather are transformed by the task relevance of cues that guide performance in learned, naturalistic behaviors.

Significance statement: Unplanned heading changes trigger lifesaving steering back to a goal. Conventionally, such behaviors are thought of as cortical sensory-motor reflex arcs. We find that a more reciprocal process underlies such cycles of perception and action, rapidly transforming visual processing to suit each stage of the task. When monkeys monitor their simulated self-movement, dorsal medial superior temporal area (MSTd) neurons represent their current heading direction. When monkeys steer to recover from an unplanned change in heading direction, MSTd shifts toward representing the goal location. We hypothesize that this transformation reflects the reweighting of bottom-up visual motion signals and top-down spatial location signals, reshaping MSTd's response properties through task-dependent interactions with adjacent cortical areas.

Keywords: cortical neurons; navigational cognition; optic flow; spatial vision; steering control.

Figure 1.

Steering task, stimulus set, behavioral paradigm, and performance. A, Steering demands monitoring for unpredictable heading changes and steering to redirect heading back to the intended direction (illustrated from left to right). C, In the delayed steer to Sample task, the monkey maintained centered fixation while one of eight Sample optic flow stimuli was presented for 500 ms. After a 1000 ± 250 ms blank screen delay, the Start optic flow was presented with a radial COM 90° clockwise (CW) or counterclockwise (CC) from Sample COM. After 500 ms, free viewing was allowed while the monkey used the rotational joystick to steer the COM to match the sample position, where it was held for 500 ms. When the fixation control was released during active steering, both monkeys saccaded to the COM and then tracked it to the Match location, prompting them to recenter their gaze to earn liquid reward. B, The stimulus set consisted of eight optic flow patterns, four outward (left) and four inward (right). D, Both monkeys performed well, as seen in average joystick (magenta, mean deflection from upright) and eye (green, eccentricity from centered fixation) position traces. Example eye traces from a single recording session are shown (dashed, green lines).

Figure 2.

The diversity of single-neuron response changes across steering conditions. A, Neuron with robust motion pattern selectivity and modest heading location selectivity. Spike density functions (SDFs) are arranged at the four cardinal COM locations used during the Sample (left), Start (middle), and Match (right) conditions. Average responses to radial-in motion (blue) and radial-out motion (red) are shown for 16 correct trials for each optic flow stimulus (128 trials). The polar plots each group of SDFs represent average firing rate in the last 200 ms of each response period. The position of each apex corresponds to one of the four COM locations for inward and outward radial motion, with the co-plotted radial line representing the in and out net vectors. B, This neuron shows decreased response selectivity from the Sample to the Start and Match conditions. C, Polar plots of the responses of a neuron that maintains selectivity but shows declining total response amplitude. C, Polar plots of the responses of a neuron that changes its stimulus selectivity to prefer inward and outward left side COMs. D, Polar plots of the responses of a neuron that demonstrates initial pattern selectivity changing to location selectivity during the match period.

Figure 3.

Population average responses for all neurons with significant optic flow selectivity during the steering task. A, Averaged population neuronal responses aligned to the preferred optic flow stimulus in the Sample responses (thick solid red line) and normalized to the mean response rate evoked by that stimulus. Responses to the nondominant in/out radial motion pattern (blue), to the clockwise (CW; dashed), counterclockwise (CC; dotted), and anti-preferred (thin line) COM locations for the Sample (A), Start (B), and Match (C) conditions. Polar plots (right) show the average firing rate at the four COM locations of the dominant (red) and nondominant (blue) radial patterns in the last 200 ms of the three conditions. Across the population, there is a decrease in radial selectivity from Sample to Start and an increase in COM location selectivity from Start to Match. B, Averaged neuronal population responses aligned to the preferred motion pattern in each of the response periods (thick solid red line) and normalized to the mean response rate evoked by that stimulus (format as in A). Across the population, there are changes in which of the stimuli are preferred from Sample to Start and Match, with a subtle decline in selectivity (Sample to Start) and then a reversal of stimulus preferences to favor location effects (Start to Match).

Figure 4.

Population average selectivity indices across steering task conditions. A, The in/out radial pattern was randomized between Sample and Start to distinguish between the influence of local motion direction selectivity and COM location selectivity. The COM location selectivity index (yellow disk/icon) is the contrast ratio of response firing rates to the preferred stimulus and the stimulus with the opposite COM location and the same radial pattern (left icons). The local motion direction selectivity index (yellow lines) is the contrast ratio of response firing rates to the preferred stimulus and the stimulus with the nondominant in/out radial motion and the same COM location (right icons). B–D, Time course of neuronal population selectivity for COM location and motion direction across the Sample (B), Start (C), and Match (D) periods. During the Sample and Start periods, motion direction selectivity is more prominent than COM location selectivity. During the Match period, this relationship is reversed such that COM location selectivity is more prominent than local motion direction selectivity.