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Flexible coding of object motion in multiple reference frames by parietal cortex neurons

Nature Neuroscience volume 23, pages 1004–1015 (2020)Cite this article

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Abstract

Neurons represent spatial information in diverse reference frames, but it remains unclear whether neural reference frames change with task demands and whether these changes can account for behavior. In this study, we examined how neurons represent the direction of a moving object during self-motion, while monkeys switched, from trial to trial, between reporting object direction in head- and world-centered reference frames. Self-motion information is needed to compute object motion in world coordinates but should be ignored when judging object motion in head coordinates. Neural responses in the ventral intraparietal area are modulated by the task reference frame, such that population activity represents object direction in either reference frame. In contrast, responses in the lateral portion of the medial superior temporal area primarily represent object motion in head coordinates. Our findings demonstrate a neural representation of object motion that changes with task requirements.

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Fig. 1: Schematic illustration of interactions between object motion and self-motion.
Fig. 2: Behavioral task design and predicted psychometric functions.
Fig. 3: Summary of behavioral performance for each task reference frame.
Fig. 4: Data from example neurons recorded from areas VIP and MSTl.
Fig. 5: Summary of single-unit results for VIP and MSTl.
Fig. 6: Summary of population decoding results.
Fig. 7: Time course of decoder performance.
Fig. 8: Time courses of classification accuracy using within-task versus cross-task decoding.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Code availability

Custom analysis code was written using MATLAB (v. 2018a). MATLAB scripts employed are available from the corresponding author upon reasonable request.

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Acknowledgements

This work was supported by National Institutes of Health grants EY016178 (to G.C.D.) and DC014678 (to D.E.A.), the Uehara Memorial Foundation (to R.S.), the Japan Society for the Promotion of Science (to R.S.) and an NEI CORE grant (EY001319). We thank D. Graf, S. Shimpi and E. Murphy for excellent technical support and J. Wen and A. Yung for programming support.

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Author notes

  1. Ryo Sasaki

    Present address: Department of Neuroscience, Graduate School of Medicine, Kyoto University, Kyoto, Japan

Authors and Affiliations

  1. Department of Brain and Cognitive Sciences, Center for Visual Science, University of Rochester, Rochester, NY, USA

    Ryo Sasaki, Akiyuki Anzai & Gregory C. DeAngelis

  2. Center for Neural Science, New York University, New York, NY, USA

    Dora E. Angelaki

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Contributions

R.S. and G.C.D. conceived and designed the research. R.S. performed experiments. R.S. analyzed data. A.A. built the recording system. R.S., A.A., D.E.A. and G.C.D. interpreted results of experiments. R.S. prepared the figures. R.S. and G.C.D. drafted the manuscript. R.S., A.A., D.E.A. and G.C.D. edited and revised the manuscript. R.S., A.A., D.E.A. and G.C.D. approved the final version of the manuscript.

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Correspondence to Ryo Sasaki.

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Peer review information Nature Neuroscience thanks Alexander Huk, Shawn M. Willett and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Summary of psychophysical thresholds (inverse of sensitivity) across task conditions.

a, Average threshold for the Object Only condition (no self-motion) is plotted against average thresholds for the Object+Visual and Object+Combined conditions for the world (brown/magenta) and head (blue/cyan) coordinate tasks. Error bars represent 95% confident intervals. Averages taken over n = 185 sessions across the two animals. b, For each session, threshold in the Object+Combined condition is plotted against the corresponding threshold in the Object+Visual condition. Black symbols show mean thresholds and error bars represent 95% confidence intervals. Data from 128 sessions for Monkey N and 57 sessions for monkey K.

Extended Data Fig. 2 Summary of receptive field locations for populations of VIP (orange, N = 66) and MSTl (green, N = 44) neurons.

Cells are included here if they had significant structure in receptive field maps obtained by reverse correlation (17% of VIP and 13% of MSTl neurons) or if they had clear hand-mapped receptive fields for which good estimates of RF center and size were obtained (13% of VIP neurons and 12% of MSTl neurons). Significant structure in reverse correlation maps was assessed by a two-sided permutation test (p < 0.05), in which we scrambled the relationship between response amplitude and stimulus location within the RF, as described previously56. Ellipses approximate the RF dimensions and were derived either from a two-dimensional Gaussian fit (contour at half-maximal response) to receptive field maps obtained by reverse correlation (VIP: N = 38; MSTl: N = 23), or from hand mapping (VIP: N = 28; MSTl: N = 21). Coordinate (0, 0) represents the center of the visual display, where the fixation target was located. Yellow dashed lines represent the starting location of the moving object and the range of directions in head coordinates.

Extended Data Fig. 3 Data from four additional VIP neurons, illustrating diversity of effects of self-motion on tuning curves.

Top: Object+Combined condition. Bottom: Object+Visual condition. Format as in Fig. 4. Error bars denote SEM (n = 10 stimulus repetitions per datum).

Extended Data Fig. 4 Summary of time courses of average firing rates and directional selectivity.

a, Average response across all 223 VIP and 177 MSTl neurons is shown for each stimulus condition for both the head and world coordinate task conditions. For each neuron, responses were taken from the object motion direction that elicited the maximum firing rate. Error bars represent SEM. Color coding as in Fig. 7. Results were nearly identical if the responses of neurons were normalized before averaging. b, Average direction discrimination index (DDI) for populations of VIP (n = 223) and MSTl (n = 177) neurons (see Methods, Eq. 2). DDI values were computed separately for leftward and rightward self-motion and then averaged for each neuron. Error bars represent 95% confidence intervals. For this figure, both average responses and DDI values were computed within a 300 ms sliding time window that was advanced across the stimulus epoch in steps of 50 ms.

Extended Data Fig. 5 Decoder results are robust to the type of classifier used.

Black data points represent results from the FLD classifier used in all main figures. Red data points show results from a logistic regression decoder. For this comparison, the same population responses were used for training and testing each decoder. The results are very robust to the type of decoder used. Error bars represent 95% confidence intervals (across n = 1000 bootstraps).

Extended Data Fig. 6 Comparison of decoder results across animals.

a–d, Results for separate decoders trained to perform the world and head coordinate tasks. Format as in Fig. 6. Each row shows results separately for each animal. Pink and cyan dashed lines in panels b and d: expected ΔPSE for perfect performance in the world and head coordinate tasks, respectively. Error bars in panels b and d represent 95% confidence intervals (across n = 1000 bootstraps). e–h, Results for the single decoder, shown separately for each animal. Decoders were trained separately using responses from each animal, yet main results are conserved across subjects. Error bars represent 95% confidence intervals (across n = 1000 bootstraps). Format as in panels a-d.

Extended Data Fig. 7 Effect of partial cube frame on single-unit responses and population decoding.

a, d, Distributions of the cube effect index (CEI, see Methods) for areas VIP and MSTl, respectively, in the world coordinate task. Black and gray shading denotes neurons with CEI values that are significantly different from zero and non-significant, respectively (two-sided permutation test, p < 0.05). b, e, Distributions of CEI for VIP and MSTl, respectively, in the head coordinate task condition. c, f, Distributions of the difference in CEI (ΔCEI) between world and head task conditions for VIP and MSTl, respectively. Green and purple shading indicates a median split of the data based on the absolute value, |ΔCEI|. g, h, Comparison of decoder accuracy (proportion correct) for populations of neurons with above-median |ΔCEI| (abscissa) and below-median |ΔCEI| (ordinate) values, for areas VIP and MSTl, respectively. Error bars represent 95% confidence intervals (across n = 1000 bootstraps). Data in these panels come from decoders that were trained separately for the world and head coordinate task conditions. i, j, Same as panels g and h, except for a single decoder trained to perform the task across both reference frame conditions. Format as in g, h.

Extended Data Fig. 8 Summary of choice-related and task-related response modulations.

a, Scatter plot of task probability (TP) and choice probability (CP) values for VIP neurons (N = 223). Color of the symbol centers corresponds to significance of TP and CP values as follows: blue center, both TP and CP are significantly different from 0.5 (two-sided permutation test, p < 0.05); red center, only CP is significantly different from 0.5; gold center, only TP is significantly different from 0.5; white center, neither TP nor CP is significant. The observation that TP and CP values are largely uncorrelated here is an empirical observation that is not enforced by the analysis. b, Scatter plot of TP and CP values for MSTl neurons (N = 177). Symbol center color conventions as in panel a. c, Scatter plot of TP values for VIP neurons computed separately for right and left choices (N = 223). d, Same as panel c but for MSTl neurons (N = 177). e, Scatter plot comparing CP values from VIP for the world and head coordinate task conditions (N = 223). f, Same as panel e but for MSTl neurons (N = 177).

Extended Data Fig. 9 Effects of selectively removing choice- or task-related response modulations.

a, Scatter plot of TP and CP values for VIP (N = 223) after selective removal of choice-related response modulations (see Methods for details). Format as in Extended Data Fig. 8a. b, Same as panel a except for MSTl (N = 177). Format as in Extended Data Fig. 8b. c, Scatter plot of TP and CP values for VIP after selective removal of task-related response modulations. d, Same as panel c, except for MSTl. e, Time course of decoder performance based on activity of 223 VIP neurons on response conflict trials, after removal of task-related response modulations. Data are shown for the case of separate decoders for world and head coordinate task conditions. Format as in Fig. 7b. Error bars represent 95% confidence intervals (across n = 100 bootstraps). f, Time course of VIP decoder performance, as in panel e, but after removal of choice-related response modulations.

Extended Data Fig. 10 Results from behavioral control sessions in which the depth of the partial cube was varied across trials.

a, Predicted ΔPSE values are shown as a function of the depth of the partial cube. Red and blue data points show predicted ΔPSE values and depths for the near and far edges of the cube. b, Dashed curves replot the predictions from panel a, where the horizontal axis is now depth relative to the origins for the near (red) and far (blue) cube edges (where the origins are the farthest depths for each edge). Data points represent behavioral ΔPSE values for the two monkeys (n = 7 sessions for each animal); magenta and brown data points show results for the Object+Combined and Object+Visual conditions. Error bars show 95% confidence intervals, and lines show regression fits. The slopes of the linear fits were not significantly different from zero for either animal or either self-motion condition (two-tailed t-test, p > 0.15 for all four cases).

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Sasaki, R., Anzai, A., Angelaki, D.E. et al. Flexible coding of object motion in multiple reference frames by parietal cortex neurons. Nat Neurosci 23, 1004–1015 (2020). https://doi.org/10.1038/s41593-020-0656-0

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