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The neural basis of predictive pursuit

Abstract

It remains unclear whether and, if so, how nonhuman animals make on-the-fly predictions during pursuit. Here we used a novel laboratory pursuit task that incentivizes the prediction of future prey positions. We trained three macaques to perform a joystick-controlled pursuit task in which prey follow intelligent escape algorithms. Subjects aimed toward the likely future positions of the prey, which indicated that they generate internal predictions and use these to guide behavior. We then developed a generative model that explains real-time pursuit trajectories and showed that our subjects use prey position, velocity and acceleration to make predictions. We identified neurons in the dorsal anterior cingulate cortex whose responses track these three variables. These neurons multiplexed prediction-related variables with a distinct and explicit representation of the future position of the prey. Our results provide a clear demonstration that the brain can explicitly represent future predictions and highlight the critical role of anterior cingulate cortex for future-oriented cognition.

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Fig. 1: Experimental paradigm and behavioral results.
Fig. 2: Model description and fitting results.
Fig. 3: Basic neural results.
Fig. 4: Properties of future position selectivity.
Fig. 5: Analyses that control for potential gaze confounds.
Fig. 6: Modulatory effect of reward size on tuning for prey variables.

Data availability

A portion of the data is available on Github (https://github.com/sbyoo/prospectpursuit/). Full data are available from the corresponding author upon reasonable request.

Code availability

Code is available at https://github.com/sbyoo/prospectpursuit/.

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Acknowledgements

The authors thank A. Thomé for his critical role in designing the task, for devising the training protocols and for developing our joysticks. They thank M. Mancarella for his critical help with joystick training, and appreciate invaluable help from M. Schieber, A. Rouse and S. Heilbronner. This work was supported by an award from the Templeton Foundation to B.Y.H. and by an R01 from NIDA (DA038615).

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S.B.M.Y. and B.Y.H. conceptualized and designed the experiment. S.B.M.Y. collected the data. S.B.M.Y. and S.T.P. developed the behavioral model, S.B.M.Y., J.C.T. and B.Y.H. developed the physiological model and analyzed the data. S.B.M.Y. and B.Y.H. wrote the manuscript.

Corresponding author

Correspondence to Seng Bum Michael Yoo.

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Supplementary Figs. 1–6.

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Supplementary Video 1

Video exhibiting subject while performing the experimental task.

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Yoo, S.B.M., Tu, J.C., Piantadosi, S.T. et al. The neural basis of predictive pursuit. Nat Neurosci 23, 252–259 (2020). https://doi.org/10.1038/s41593-019-0561-6

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