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Goal-directed actions transiently depend on dorsal hippocampus

Nature Neuroscience volume 23, pages 1194–1197 (2020)Cite this article

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Abstract

The role of the hippocampus in goal-directed action is currently unclear; studies investigating this issue have produced contradictory results. Here we reconcile these contradictions by demonstrating that, in rats, goal-directed action relies on the dorsal hippocampus, but only transiently, immediately after initial acquisition. Furthermore, we found that goal-directed action also depends transiently on physical context, suggesting a psychological basis for the hippocampal regulation of goal-directed action control.

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Fig. 1: Inactivation of the dorsal hippocampus transiently impaired outcome devaluation performance when testing was immediate, but not after additional training or a delay.
Fig. 2: Outcome devaluation performance is impaired by a context switch immediately after limited training, but not after additional training or a delay.

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Data availability

Research data for this article (Figs. 1 and 2 and Extended Data Figs. 2–4) are available for download at https://osf.io/vd4an/?view_only=b161002919a24ca196ce23f7b2df84ad/.

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Acknowledgements

We thank G. Hart for helpful discussions and F. Westbrook for feedback on the manuscript. This work was supported by grants GNT1087689 and GNT1148244 from the National Health and Medical Research Council in Australia to L.A.B. and B.W.B.

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Author notes

  1. These authors contributed equally: Laura A. Bradfield, Beatrice K. Leung.

Authors and Affiliations

  1. Centre for Neuroscience and Regenerative Medicine, University of Technology Sydney, Sydney, New South Wales, Australia

    Laura A. Bradfield

  2. St Vincent’s Centre for Applied Medical Research, St Vincent’s Health Network, Sydney, New South Wales, Australia

    Laura A. Bradfield

  3. Decision Neuroscience Laboratory, School of Psychology, University of New South Wales, Sydney, New South Wales, Australia

    Beatrice K. Leung, Sophia Liang & Bernard W. Balleine

  4. School of Psychology, University of Sydney, Sydney, New South Wales, Australia

    Susan Boldt

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  5. Bernard W. Balleine
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Contributions

L.A.B., B.K.L. and B.W.B. designed the experiments. L.A.B., B.K.L., S.L. and S.B. performed the experiments. L.A.B., B.K.L. and B.W.B. wrote the manuscript.

Corresponding authors

Correspondence to Laura A. Bradfield or Bernard W. Balleine.

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The authors declare no competing interests.

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Peer review information Nature Neuroscience thanks Stan Floresco, Geoffrey Schoenbaum and Nicolas Schuck for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Cannula and DREADDs placements.

a, Diagrammatic representation of cannula placements from Experiment 1a (indicated by black dots). b, Photomicrograph of representative cannula placement (n = 24 rats with similar placements in Experiment 1a). c, Diagrammatic representation of cannula placements from Experiment 1b (indicated by black dots). d, Diagrammatic representation of CA1/Dorsal hippocampal viral DREADDs placements (indicated in red), showing each overlapping placement for Experiment 2. e, Diagrammatic representation of CA2 viral DREADDs placements (indicated in red), showing each overlapping placement for Experiment 2. f, Diagrammatic representation of dorsal hippocampal viral placements (indicated in red), showing each overlapping placement for Experiment 3a. g, Diagrammatic representation of dorsal hippocampal viral placements (indicated in red), showing each overlapping placement for Experiment 3b. All placements are shown on coronal sections adapted from the rat brain atlas of Paxinos & Watson21.

Extended Data Fig. 2 Supplementary experimental data for Experiments 1-3.

a, Mean presses per day during polycose pretraining for Experiment 1a. b, Mean presses on Day 6 of lever press training (pellets and sucrose delivered) for Experiment 1a (n = 19 rats). c, Mean pellet and sucrose deliveries on Day 6 in Experiment 1a (n = 19 rats). d, Mean presses per day during polycose pretraining for Experiment 1b (n = 16 rats). e, Mean presses on Day 6 of lever press training (pellets and sucrose delivered) for Experiment 1b (n = 16 rats). f, Mean pellet and sucrose deliveries on Day 6 in Experiment 1b (n = 16 rats). g, Mean presses during initial acquisition for Experiment 2 (n = 35 rats). h, Mean pellet and sucrose deliveries during initial acquisition for Experiment 2 (n = 35 rats). i, Mean presses per day during extended training for Experiment 2 (n = 35 rats). Although training performance in the hM4Di groups did not differ across days (largest F(1,31) = 1.06, p = .311), linear acquisition was significantly reduced for group mCherry+CNO relative to group hM4Di+Veh, F(1,31) 6.297, p = .018. These data were analyzed using orthogonal complex contrasts, controlling the per-contrast error rate at α = 0.05. j, Mean presses during initial acquisition for Experiment 3a (Immediate devaluation; n = 38 rats) and 3b (Delayed Devaluation; n = 37 rats). k, Mean pellet and sucrose deliveries during initial acquisition for Experiment 3a (n = 38 rats). l, Mean pellet and sucrose deliveries during initial acquisition for Experiment 3b (n = 37 rats). Data are shown as individual dot plots and mean ± SEM.

Extended Data Fig. 3 Supplementary experimental data for Experiments 4-5.

a, Mean presses per day during polycose pretraining for Experiment 4a (n = 25 rats). b, Mean presses on Day 6 of lever press training (pellets and sucrose delivered) for Experiment 4a (n = 25 rats). c, Mean pellet and sucrose deliveries on Day 6 in Experiment 4a (n = 25 rats). d, Mean presses per day during instrumental training (pellets and sucrose delivered) for Experiment 4b (n = 21 rats). e, Mean presses during initial acquisition for Experiment 5 (n = 26 rats). f, Mean pellet and sucrose deliveries during initial acquisition for Experiment 5 (n = 26 rats). Data are shown as individual dot plots and mean ± SEM.

Extended Data Fig. 4 Suppression ratios on devalued vs. valued lever on test for each experiment.

a, Suppression ratios for Experiment 1a (n = 19 rats). There was no main effect of group, F(1,17) = 1.583, p = .225, but there was a group x lever interaction, F(1,17) = 4.672, p = .045. However, neither lever simple effect was significant, largest p = .12 (on devalued lever, this result suggests group rather than lever simple effects comprise this interaction). b, Suppression ratios for Experiment 1b (n = 16 rats). There was a main effect of group, F(1,14) = 6.316, p = .025, but this did not interact with lever, F(1,14) = 3.808, p = .071, suggesting that overall responding was suppressed in group MUSCIMOL relative to group SALINE, but this was not specific to either lever. c, Suppression ratios for the initial test in Experiment 2 (n = 35 rats). There was no main effect of group, F < 1, but there was a group x lever interaction, F(1,31) = 5.603, p = .024. Once again this interacted was composed of group simple effects because neither lever simple effect was significant (largest p = .225 on devalued lever). d, Suppression ratios for the extended test in Experiment 2. There were no statistical differences between groups or levers, all Fs < 1. e, Suppression ratios for Experiment 3a (n = 38 rats). There were no main effects or interactions when controls were compared to M4+CNO (that is the analysis used in Fig. 1i). If animals that received training and test injections were analyzed separately, there was a main effect of group for test-injected animals, F(1,34) = 7.919, p = .008, that did not interact with lever, F < 1, indicating that group M4+CNO suppressed responding less than controls but this was not specific to either lever. For animals that received training injections, all Fs < 1. f, Suppression ratios for Experiment 3b (n = 37 rats). There were no statistical differences between groups or levers, all Fs < 1.21. g, Suppression ratios for Experiment 4a (n = 25 rats). There were no statistical differences between groups or levers, all Fs < 1. h, Suppression ratios for Experiment 4b (n = 21 rats). There were no statistical differences between groups or levers, all Fs < 1. i, Suppression ratios for Experiment 5 (n = 26 rats). There was no main effect of IMM-DIFF vs. Rest, F(1,22) = 1.68, p = .208. There was a group x lever interaction, F(1,22) = 10.306, p = .004. Follow-up simple effects reveal that this interaction was comprised of a significant group difference on the valued lever, F(1,22) = 6.417, p = .019, and not the devalued lever, F < 1. These data were analyzed using orthogonal complex contrasts, controlling the per-contrast error rate at α = 0.05. Data are shown as individual dot plots and mean ± SEM.

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Bradfield, L.A., Leung, B.K., Boldt, S. et al. Goal-directed actions transiently depend on dorsal hippocampus. Nat Neurosci 23, 1194–1197 (2020). https://doi.org/10.1038/s41593-020-0693-8

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