Skip to main content

Formation of the Looming-evoked Innate Defensive Response during Postnatal Development in Mice

  • Original Article
  • Published:
Neuroscience Bulletin Aims and scope Submit manuscript

Abstract

Environmental threats often trigger innate defensive responses in mammals. However, the gradual development of functional properties of these responses during the postnatal development stage remains unclear. Here, we report that looming stimulation in mice evoked flight behavior commencing at P14–16 and had fully developed by P20–24. The visual-evoked innate defensive response was not significantly altered by sensory deprivation at an early postnatal stage. Furthermore, the percentages of wide-field and horizontal cells in the superior colliculus were notably elevated at P20–24. Our findings define a developmental time window for the formation of the visual innate defense response during the early postnatal period and provide important insight into the underlying mechanism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Tovote P, Esposito MS, Botta P, Chaudun F, Fadok JP, Markovic M. Midbrain circuits for defensive behaviour. Nature 2016, 534: 206–212.

    Article  CAS  PubMed  Google Scholar 

  2. Ydenberg RC, Dill LM. The economics of fleeing from predators. Adv Study Behav 1986, 16: 229–249.

    Article  Google Scholar 

  3. Fischer S, Oberhummer E, Cunha-Saraiva F, Gerber N, Taborsky B. Smell or vision? The use of different sensory modalities in predator discrimination. Behav Ecol Sociobiol 2017, 71: 1–10.

    Article  Google Scholar 

  4. Pereira AG, Moita MA. Is there anybody out there? Neural circuits of threat detection in vertebrates. Curr Opin Neurobiol 2016, 41: 179–187.

    Article  CAS  PubMed  Google Scholar 

  5. Albano JE, Humphrey AL, Norton TT. Laminar organization of receptive-field properties in tree shrew superior colliculus. J Neurophysiol 1978, 41: 1140–1164.

    Article  CAS  PubMed  Google Scholar 

  6. McIlwain JT, Buser P. Receptive fields of single cells in the cat’s superior colliculus. Exp Brain Res 1968, 5: 314–325.

    Article  CAS  PubMed  Google Scholar 

  7. Stewart DL, Birt D, Towns LC. Visual receptive-field characteristics of superior colliculus neurons after cortical lesions in the rabbit. Vision Res 1973, 13: 1965–1977.

    Article  CAS  PubMed  Google Scholar 

  8. Fortin S, Chabli A, Dumont I, Shumikhina S, Itaya SK, Molotchnikoff S. Maturation of visual receptive field properties in the rat superior colliculus. Brain Res Dev Brain Res 1999, 112: 55–64.

    Article  CAS  PubMed  Google Scholar 

  9. Dräger UC, Hubel DH. Responses to visual stimulation and relationship between visual, auditory, and somatosensory inputs in mouse superior colliculus. J Neurophysiol 1975, 38: 690–713.

    Article  PubMed  Google Scholar 

  10. Sen R, Wu M, Branson K, Robie A, Rubin GM, Dickson BJ. Moonwalker descending neurons mediate visually evoked retreat in Drosophila. Curr Biol 2017, 27: 766–771.

    Article  CAS  PubMed  Google Scholar 

  11. LeDoux J. Rethinking the emotional brain. Neuron 2012, 73: 653–676.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. LeDoux JE. Coming to terms with fear. Proc Natl Acad Sci U S A 2014, 111: 2871–2878.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Mobbs D, Hagan CC, Dalgleish T, Silston B, Prévost C. The ecology of human fear: Survival optimization and the nervous system. Front Neurosci 2015, 9: 55.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Moriceau S, Roth TL, Okotoghaide T, Sullivan RM. Corticosterone controls the developmental emergence of fear and amygdala function to predator odors in infant rat pups. Int J Dev Neurosci 2004, 22: 415–422.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Arakawa H. Age and sex differences in the innate defensive behaviors of C57BL/6 mice exhibited in a fear conditioning paradigm and upon exposure to a predatory odor. Physiol Behav 2019, 204: 264–274.

    Article  CAS  PubMed  Google Scholar 

  16. Sharma A, LeVaillant CJ, Plant GW, Harvey AR. Changes in expression of Class 3 Semaphorins and their receptors during development of the rat Retina and superior colliculus. BMC Dev Biol 2014, 14: 34.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Williams E, Scott JP. The development of social behavior patterns in the mouse, in relation to natural periods 1). Behaviour 1954, 6: 35–64.

    Article  Google Scholar 

  18. Barbara K. Components of lifetime reproductive success in communally and solitarily nursing house mice—a laboratory study. Behav Ecol Sociobiol 1994, 34: 275–283.

    Article  Google Scholar 

  19. Latham N, Mason G. From house mouse to mouse house: The behavioural biology of free-living Mus musculus and its implications in the laboratory. Appl Animal Behav Sci 2004, 86: 261–289.

    Article  Google Scholar 

  20. Yilmaz M, Meister M. Rapid innate defensive responses of mice to looming visual stimuli. Curr Biol 2013, 23: 2011–2015.

    Article  CAS  PubMed  Google Scholar 

  21. Zhou Z, Liu XM, Chen SP, Zhang ZJ, Liu YM, Montardy Q, et al. A VTA GABAergic neural circuit mediates visually evoked innate defensive responses. Neuron 2019, 103: 473-488.e6.

    Article  CAS  PubMed  Google Scholar 

  22. Wei P, Liu N, Zhang Z, Liu X, Tang Y, He X, et al. Processing of visually evoked innate fear by a non-canonical thalamic pathway. Nat Commun 2015, 6: 6756.

    Article  CAS  PubMed  Google Scholar 

  23. Li L, Feng X, Zhou Z, Zhang H, Shi Q, Lei Z, et al. Stress accelerates defensive responses to looming in mice and involves a locus coeruleus-superior colliculus projection. Curr Biol 2018, 28: 859-871.e5.

    Article  CAS  PubMed  Google Scholar 

  24. Shang CP, Liu ZH, Chen ZJ, Shi YC, Wang Q, Liu S, et al. BRAIN CIRCUITS A parvalbumin-positive excitatory visual pathway to trigger fear responses in mice. Science 2015, 348: 1472–1477.

    Article  CAS  PubMed  Google Scholar 

  25. Gale SD, Murphy GJ. Distinct representation and distribution of visual information by specific cell types in mouse superficial superior colliculus. J Neurosci 2014, 34: 13458–13471.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Dana H, Chen TW, Hu A, Shields BC, Guo CY, Looger LL, et al. Thy1-GCaMP6 transgenic mice for neuronal population imaging in vivo. PLoS One 2014, 9: e108697. https://doi.org/10.1371/journal.pone.0108697.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Zheng JJ, Li SJ, Zhang XD, Miao WY, Zhang DH, Yao HS, et al. Oxytocin mediates early experience-dependent cross-modal plasticity in the sensory cortices. Nat Neurosci 2014, 17: 391–399.

    Article  CAS  PubMed  Google Scholar 

  28. Endo T, Tarusawa E, Notomi T, Kaneda K, Hirabayashi M, Shigemoto R, et al. Dendritic Ih ensures high-fidelity dendritic spike responses of motion-sensitive neurons in rat superior colliculus. J Neurophysiol 2008, 99: 2066–2076.

    Article  PubMed  Google Scholar 

  29. Chuang N, Mori S, Yamamoto A, Jiang HY, Ye X, Xu X, et al. An MRI-based atlas and database of the developing mouse brain. Neuroimage 2011, 54: 80–89.

    Article  PubMed  Google Scholar 

  30. Brust V, Schindler PM, Lewejohann L. Lifetime development of behavioural phenotype in the house mouse (Mus musculus). Front Zool 2015, 12: S17.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Fox K, Wong RO. A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron 2005, 48: 465–477.

    Article  CAS  PubMed  Google Scholar 

  32. Gianfranceschi L, Siciliano R, Walls J, Morales B, Kirkwood A, Huang ZJ, et al. Visual cortex is rescued from the effects of dark rearing by overexpression of BDNF. Proc Natl Acad Sci U S A 2003, 100: 12486–12491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Dean P, Redgrave P, Westby GW. Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci 1989, 12: 137–147.

    Article  CAS  PubMed  Google Scholar 

  34. Basso MA, May PJ. Circuits for action and cognition: A view from the superior colliculus. Ann Rev Vis Sci 2017, 3: 197–226.

    Article  Google Scholar 

  35. Ito S, Feldheim DA. The mouse superior colliculus: An emerging model for studying circuit formation and function. Front Neural Circuits 2018, 12: 10.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Chen YM, Ni YL, Zhou JH, Zhou H, Zhong Q, Li XY, et al. The amygdala responds rapidly to flashes linked to direct retinal innervation: A flash-evoked potential study across cortical and subcortical visual pathways. Neurosci Bull 2021, 37: 1107–1118.

    Article  PubMed  Google Scholar 

  37. Tamietto M, Pullens P, de Gelder B, Weiskrantz L, Goebel R. Subcortical connections to human amygdala and changes following destruction of the visual cortex. Curr Biol 2012, 22: 1449–1455.

    Article  CAS  PubMed  Google Scholar 

  38. Gribizis A, Ge X, Daigle TL, Ackman JB, Zeng H, Lee D, et al. Visual cortex gains independence from peripheral drive before eye opening. Neuron 2019, 104: 711-723.e3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Yang X, Liu Q, Zhong J, Song R, Zhang L, Wang L. A simple threat-detection strategy in mice. BMC Biol 2020, 18: 93.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Zhao X, Liu M, Cang J. Visual cortex modulates the magnitude but not the selectivity of looming-evoked responses in the superior colliculus of awake mice. Neuron 2014, 84: 202–213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Wiesel TN. Postnatal development of the visual cortex and the influence of environment. Nature 1982, 299: 583–591.

    Article  CAS  PubMed  Google Scholar 

  42. Feldman DE, Brecht M. Map plasticity in somatosensory cortex. Science 2005, 310: 810–815.

    Article  CAS  PubMed  Google Scholar 

  43. Espinosa JS, Stryker MP. Development and plasticity of the primary visual cortex. Neuron 2012, 75: 230–249.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Gianfranceschi L, Siciliano R, Walls J, Morales B, Kirkwood A, Huang ZJ, et al. Visual cortex is rescued from the effects of dark rearing by overexpression of BDNF. Proc Natl Acad Sci U S A 2003, 100: 12486–12491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Teichert M, Isstas M, Wenig S, Setz C, Lehmann K, Bolz J. Cross-modal refinement of visual performance after brief somatosensory deprivation in adult mice. Eur J Neurosci 2018, 47: 184–191.

    Article  PubMed  Google Scholar 

  46. Adolphs R, Sears L, Piven J. Abnormal processing of social information from faces in autism. J Cogn Neurosci 2001, 13: 232–240.

    Article  CAS  PubMed  Google Scholar 

  47. Hu Y, Chen ZM, Huang L, Xi Y, Li BX, Wang H, et al. A translational study on looming-evoked defensive response and the underlying subcortical pathway in autism. Sci Rep 2017, 7: 14755.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31930047, 91732304 and 31630031); The Strategic Priority Research Program of the Chinese Academy of Science (XDB32030100); Guangdong Provincial Key Laboratory of Brain Connectome and Behavior (2017B030301017); the Natural Science Foundation of Guangdong Province (2018A030313439); a Shenzhen Government grant (JCYJ20170413164535041); Shenzhen Key Science and Technology Infrastructure Planning Project (ZDKJ20190204002); Key Laboratory of CAS (2019DP173024); The Ten Thousand Talents Program; The Guangdong Special Support Program; Chang Jiang Scholars Program; International Partnership Program of the Chinese Academy of Sciences (172644KYS820170004); and the Key-Area Research and Development Program of Guangdong Province (2018B030331001).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Liping Wang.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 219 kb)

Supplementary file2 (MP4 2287 kb)

Supplementary file3 (MP4 2648 kb)

Supplementary file4 (MP4 3036 kb)

Supplementary file5 (MP4 2519 kb)

Supplementary file6 (MP4 2486 kb)

Supplementary file7 (MP4 2656 kb)

Supplementary file8 (MP4 2967 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, S., Tan, H., Wang, Z. et al. Formation of the Looming-evoked Innate Defensive Response during Postnatal Development in Mice. Neurosci. Bull. 38, 741–752 (2022). https://doi.org/10.1007/s12264-022-00821-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12264-022-00821-0

Keywords