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Dorsal hippocampus contributes to model-based planning

Nature Neuroscience volume 20, pages 1269–1276 (2017)Cite this article

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An Author Correction to this article was published on 17 November 2017

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Abstract

Planning can be defined as action selection that leverages an internal model of the outcomes likely to follow each possible action. Its neural mechanisms remain poorly understood. Here we adapt recent advances from human research for rats, presenting for the first time an animal task that produces many trials of planned behavior per session, making multitrial rodent experimental tools available to study planning. We use part of this toolkit to address a perennially controversial issue in planning: the role of the dorsal hippocampus. Although prospective hippocampal representations have been proposed to support planning, intact planning in animals with damaged hippocampi has been repeatedly observed. Combining formal algorithmic behavioral analysis with muscimol inactivation, we provide causal evidence directly linking dorsal hippocampus with planning behavior. Our results and methods open the door to new and more detailed investigations of the neural mechanisms of planning in the hippocampus and throughout the brain.

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Figure 1: Two-step decision task for rats.
Figure 2: Multitrial history regression analysis.
Figure 3: Model-fitting analysis.
Figure 4: Effects of muscimol inactivation.
Figure 5: Effects of muscimol inactivation on mixture model fits.

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  • 17 November 2017

    In the version of this article initially published, the green label in Fig. 1c read "rightward choices" instead of "leftward choices." The error has been corrected in the HTML and PDF versions of the article.

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Acknowledgements

We thank J. Erlich, C. Kopec, C.A. Duan, T. Hanks and A. Begelfer for training K.J.M. in the techniques necessary to carry out these experiments, as well as for comments and advice on the project. We thank N. Daw, I. Witten, Y. Niv, B. Wilson, T. Akam, A. Akrami and A. Solway for comments and advice on the project, and we thank J. Teran, K. Osorio, A. Sirko, R. LaTourette, L. Teachen and S. Stein for assistance in carrying out behavioral experiments. We especially thank T. Akam for suggestions on the physical layout of the behavior box and other experimental details. We thank A. Bornstein, B. Scott, A. Piet and L. Hunter for comments on the manuscript. K.J.M. was supported by training grant NIH T-32 MH065214 and by a Harold W. Dodds fellowship from Princeton University.

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Authors and Affiliations

  1. Princeton Neuroscience Institute, Princeton University, Princeton, New Jersey, USA

    Kevin J Miller, Matthew M Botvinick & Carlos D Brody

  2. Gatsby Computational Neuroscience Unit, University College London, London, UK

    Matthew M Botvinick

  3. Google DeepMind, London, UK

    Matthew M Botvinick

  4. Howard Hughes Medical Institute and Department of Molecular Biology, Princeton University, Princeton, New Jersey, USA

    Carlos D Brody

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  1. Kevin J Miller
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Contributions

K.J.M., M.M.B. and C.D.B. conceived the project. K.J.M. designed and carried out the experiments and the data analysis, with supervision from M.M.B. and C.D.B. K.J.M., M.M.B. and C.D.B. wrote the paper, starting from an initial draft by K.J.M.

Corresponding authors

Correspondence to Matthew M Botvinick or Carlos D Brody.

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Integrated supplementary information

Supplementary Figure 1 Reward rates of model-based and model-free agents.

Reward rates achieved by synthetic datasets generated by a hybrid model-based/model-free agent. Data were generated under the constraints αplan=αMF, βplan+βMF=5, with λ, αT, and all other betas set to zero. The highest reward rates are achieved by purely model-based agents, but the best purely model-free agents still outperformed the average rat, earning around 58% rewards (rat’s reward rate mean: 56.8%, sem: 0.4%, std: 2%).

Supplementary Figure 2 Results of one-trial-back analysis applied to the behavioral dataset.

Above: Average and standard error of the stay probability across rats. Below: Stay probability for each rat, with binomial 95% confidence intervals

Supplementary Figure 3 Results of logistic regression analysis applied to each rat, as well as simulated data generated from a fit of the mixture model to that rat’s dataset.

Rats are ordered by the relative quality of fit of the mixture model with respect to the regression model - earlier rats datasets are better explained by the mixture model than the regression, while later rats are better explained by the regression model.

Supplementary Figure 4 Movement times are faster following common transition trials.

Median movement time, in seconds, from the bottom center port to the reward port for common and uncommon transition trials, broken down by whether the movement was towards (right panel) or away from (left panel) the port with the higher reward probability.

Supplementary Figure 5 Placement of cannula in individual rats.

Purple points indicate OFC cannula tips, green points indicate PL cannula tips, and orange points indicate dH cannula tips.

Supplementary Figure 6 Results of logistic regression analysis applied to the inactivation dataset.

Above: Regression coefficients for the Saline, Control, dH, and OFC conditions. Points are averages across rats, and error bars are standard errors. Below: Differences between regression coefficients for different conditions

Supplementary Figure 7 Results of logistic regression analysis applied to each rat in the inactivation dataset.

Note that rat #6 did not complete any saline sessions

Supplementary Figure 8 Results of logistic regression analysis applied to simulated data generated by the reduced model fit to each rat in the inactivation dataset

Supplementary Figure 9 Rat performances compared between inactivation and control sessions.

Top: Fraction of times each rat selected the choice port with the greatest probability of leading to the reward port with the greatest probability of reward, for control vs. OFC sessions (Left) and for control vs. dH sessions (Right). Bottom: Fraction of times the better port was selected, as a function of the number of trials since the last reward probability flip.

Supplementary Figure 10 Results of one-trial-back analysis applied to the inactivation dataset.

Above: Average stay probability by trial-type for the Control, dH, and OFC conditions. Bar height is the average across rats, and error bars are standard errors. Below: Differences between stay probabilities coefficients for the different conditions

Supplementary Figure 11 Results of one-trial-back stay/switch analysis applied to each rat in the inactivation dataset

Supplementary Figure 12 Results of fitting the multiagent model jointly to the OFC inactivation and saline datasets.

Top Row: Posterior belief distributions over parameters governing the effect of inactivation on performance across the population. Only βplan is significantly affected by the inactivation. Below: Posterior belief distributions over parameters governing behavior on OFC (purple) and Saline (blue) sessions. Only βplan is affected by inactivation in a way that is consistent across animals.

Supplementary Figure 13 Results of fitting the multiagent model jointly to the dH inactivation and saline datasets.

Top Row: Posterior belief distributions over parameters governing the effect of inactivation on performance across the population. Only βplan is significantly affected by the inactivation. Below: Posterior belief distributions over parameters governing behavior on dH (orange) and Saline (blue) sessions. Only βplan is affected by inactivation in a way that is consistent across animals.

Supplementary Figure 14 Plots of posterior density projected onto planes defined by the parameter governing change in model-based weight and other population parameters for hippocampus (top, orange) and OFC (bottom, purple) inactivation datasets.

Supplementary Figure 15 Normalized cross-validated likelihood for logistic regression models (Online Methods), as a function of the number of previous trials used to predict the upcoming choice.

Including more than five previous trials in the model results in negligible improvements in quality of model fit.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–15 and Supplementary Discussion (PDF 4128 kb)

Life Sciences Reporting Summary (PDF 73 kb)

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Miller, K., Botvinick, M. & Brody, C. Dorsal hippocampus contributes to model-based planning. Nat Neurosci 20, 1269–1276 (2017). https://doi.org/10.1038/nn.4613

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