Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Correspondence
  • Published:

Reply to ‘Post-encounter freezing during approach–avoidance conflict: the role of the hippocampus’

Nature Reviews Neuroscience volume 24, pages 453–454 (2023)Cite this article

Subjects

Access through your institution
Buy or subscribe

We thank Fernández-Teruel and McNaughton for their correspondence on our Perspective article (Roelofs, K. & Dayan, P. Freezing revisited: coordinated autonomic and central optimization of threat coping. Nat. Rev. Neurosci. 23, 568–580; 2022)1, which raises interesting issues about the role of the hippocampus in defensive freezing (Fernández-Teruel, A. & McNaughton, N. Post-encounter freezing during approach–avoidance conflict: the role of the hippocampus. Nat. Rev. Neurosci. https://doi.org/10.1038/s41583-023-00703-y; 2023)2. They provide an insightful analysis of two-way active avoidance (TWAA), showing hippocampal involvement in a form of approach–avoidance conflict that evolves over hundreds of trials. TWAA is an important paradigm in which Pavlovian ‘misbehaviour’ readily corrupts necessary instrumental actions3. How, though, does it relate to the focus of our Perspective1: single-trial, circumstance-specific, information gathering and action preparation in post-encounter threat states? Here, it is less clear that freezing depends on hippocampal involvement4 or that the approach–avoidance conflict is always the central problem to be resolved.

This is not to deny the important roles of the hippocampus in threat processing. Take the phenomenon of hippocampal replay and preplay — the reactivation or preactivation of activity patterns associated with actual or imagined states of the world8. Replay during safe and pre-encounter states can create effective defensive policies9. This can benefit all three stages of post-encounter threat outlined in our Perspective1. In phase 1, detection of potential danger, animals need effective policies to scan the environment for threats (and to track potential forms of escape). Habitized methods for this would limit the burden on more taxing forms of processing. In phase 2, sensory processing and planning, preplay might allow online previsioning of the consequences of courses of action. Depending on the nature of the potential danger and the affordances of the environment for escape, approach–avoidance conflicts may arise that this preplay could help to resolve. Defensive policies compiled by replay during safer states could also be very helpful. In phase 3, switch to action, fight or flight is engendered by sensory cues associated with the more proximal approach of danger, and is mediated via the central amygdala, anterior cingulate cortex and periaqueductal grey4,10. Here again, precompiled policies would be of great value, although they may be more generic and less situation-specific.

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Examples of freezing-related bradycardia, independent of approach–avoid conflict.

References

  1. Roelofs, K. & Dayan, P. Freezing revisited: coordinated autonomic and central optimization of threat coping. Nat. Rev. Neurosci. 23, 568–580 (2022).

    Article  CAS  PubMed  Google Scholar 

  2. Fernández-Teruel, A. & McNaughton, N. Post-encounter freezing during approach-avoidance conflict: the role of the hippocampus. Nat. Rev. Neurosci. https://doi.org/10.1038/s41583-023-00703-y (2023).

    Article  PubMed  Google Scholar 

  3. Dayan, P., Niv, Y., Seymour, B. & Daw, N. D. The misbehavior of value and the discipline of the will. Neural Netw. 19, 1153–1160 (2006).

    Article  PubMed  Google Scholar 

  4. Tovote, P. et al. Midbrain circuits for defensive behaviour. Nature 534, 206–212 (2016).

    Article  CAS  PubMed  Google Scholar 

  5. Hagenaars, M. A., Oitzl, M. & Roelofs, K. Updating freeze: aligning animal and human research. Neurosci. Biobehav. Rev. 47, 165–176 (2014).

    Article  PubMed  Google Scholar 

  6. Klaassen, F. H. et al. Defensive freezing and its relation to approach-avoidance decision-making under threat. Sci. Rep. 11, 12030 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. de Voogd, L. D., Hagenberg, E., Zhou, Y. J., de Lange, F. P. & Roelofs, K. Acute threat enhances perceptual sensitivity without affecting the decision criterion. Sci. Rep. 12, 9071 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Mattar, M. G. & Daw, N. D. Prioritized memory access explains planning and hippocampal replay. Nat. Neurosci. 21, 1609–1617 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Mobbs, D., Headley, D. B., Ding, W. & Dayan, P. Space, time, and fear: survival computations along defensive circuits. Trends Cogn. Sci. 24, 228–241 (2020).

    Article  PubMed  Google Scholar 

  10. Hashemi, M. M. et al. Neural dynamics of shooting decisions and the switch from freeze to fight. Sci. Rep. 9, 4240 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

K.R. was supported by a consolidator grant from the European Research Council (ERC_CoG-2017_772337), which also supported F.H.K. P.D. was supported by the Max Planck Society and the Alexander von Humboldt Foundation.

Author information

Authors and Affiliations

  1. Center for Cognitive Neuroimaging, Donders Institute for Brain Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands

    Karin Roelofs & Felix H. Klaassen

  2. Behavioural Science Institute, Radboud University, Nijmegen, The Netherlands

    Karin Roelofs

  3. Max Planck Institute for Biological Cybernetics, Tübingen, Germany

    Peter Dayan

  4. University of Tübingen, Tübingen, Germany

    Peter Dayan

Authors
  1. Karin Roelofs
    View author publications

    Search author on:PubMed Google Scholar

  2. Felix H. Klaassen
    View author publications

    Search author on:PubMed Google Scholar

  3. Peter Dayan
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Karin Roelofs.

Ethics declarations

Competing interests

The authors declare no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Roelofs, K., Klaassen, F.H. & Dayan, P. Reply to ‘Post-encounter freezing during approach–avoidance conflict: the role of the hippocampus’. Nat Rev Neurosci 24, 453–454 (2023). https://doi.org/10.1038/s41583-023-00704-x

Download citation

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41583-023-00704-x

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing