A Cross-modality Enhancement of Defensive Flight Via Parvalbumin Neurons in Zona Incerta

Overview

Journal Elife

Specialty Biology

Date 2019 Apr 16

PMID 30985276

Citations 21

Authors

Xiyue Wang

Xiaolin Chou

Bo Peng

Li Shen

Junxiang J Huang

Li I Zhang

Huizhong W Tao

Affiliations

Soon will be listed here.

Abstract

The ability to adjust defensive behavior is critical for animal survival in dynamic environments. However, neural circuits underlying the modulation of innate defensive behavior remain not well-understood. In particular, environmental threats are commonly associated with cues of multiple sensory modalities. It remains to be investigated how these modalities interact to shape defensive behavior. In this study, we report that auditory-induced defensive flight behavior can be facilitated by somatosensory input in mice. This cross-modality modulation of defensive behavior is mediated by the projection from the primary somatosensory cortex (SSp) to the ventral sector of zona incerta (ZIv). Parvalbumin (PV)-positive neurons in ZIv, receiving direct input from SSp, mediate the enhancement of the flight behavior via their projections to the medial posterior complex of thalamus (POm). Thus, defensive flight can be enhanced in a somatosensory context-dependent manner via recruiting PV neurons in ZIv, which may be important for increasing survival of prey animals.

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References

Petreanu L, Mao T, Sternson S, Svoboda K . The subcellular organization of neocortical excitatory connections. Nature. 2009; 457(7233):1142-5. PMC: 2745650. DOI: 10.1038/nature07709. View

Zingg B, Chou X, Zhang Z, Mesik L, Liang F, Tao H . AAV-Mediated Anterograde Transsynaptic Tagging: Mapping Corticocollicular Input-Defined Neural Pathways for Defense Behaviors. Neuron. 2016; 93(1):33-47. PMC: 5538794. DOI: 10.1016/j.neuron.2016.11.045. View

Ibrahim L, Mesik L, Ji X, Fang Q, Li H, Li Y . Cross-Modality Sharpening of Visual Cortical Processing through Layer-1-Mediated Inhibition and Disinhibition. Neuron. 2016; 89(5):1031-45. PMC: 4874809. DOI: 10.1016/j.neuron.2016.01.027. View

Mitrofanis J . Some certainty for the "zone of uncertainty"? Exploring the function of the zona incerta. Neuroscience. 2004; 130(1):1-15. DOI: 10.1016/j.neuroscience.2004.08.017. View

Shaw V, Mitrofanis J . Anatomical evidence for somatotopic maps in the zona incerta of rats. Anat Embryol (Berl). 2002; 206(1-2):119-30. DOI: 10.1007/s00429-002-0280-7. View

Zhu H, Roth B . Silencing synapses with DREADDs. Neuron. 2014; 82(4):723-5. PMC: 4109642. DOI: 10.1016/j.neuron.2014.05.002. View

Perier C, Tremblay L, Feger J, Hirsch E . Behavioral consequences of bicuculline injection in the subthalamic nucleus and the zona incerta in rat. J Neurosci. 2002; 22(19):8711-9. PMC: 6757788. View

Sofroniew N, Cohen J, Lee A, Svoboda K . Natural whisker-guided behavior by head-fixed mice in tactile virtual reality. J Neurosci. 2014; 34(29):9537-50. PMC: 4099538. DOI: 10.1523/JNEUROSCI.0712-14.2014. View

Xiong X, Liang F, Zingg B, Ji X, Ibrahim L, Tao H . Auditory cortex controls sound-driven innate defense behaviour through corticofugal projections to inferior colliculus. Nat Commun. 2015; 6:7224. PMC: 4467028. DOI: 10.1038/ncomms8224. View

10.

Trageser J, Keller A . Reducing the uncertainty: gating of peripheral inputs by zona incerta. J Neurosci. 2004; 24(40):8911-5. PMC: 1388274. DOI: 10.1523/JNEUROSCI.3218-04.2004. View

11.

Nicolelis M, Chapin J, Lin R . Somatotopic maps within the zona incerta relay parallel GABAergic somatosensory pathways to the neocortex, superior colliculus, and brainstem. Brain Res. 1992; 577(1):134-41. DOI: 10.1016/0006-8993(92)90546-l. View

12.

Zhou M, Liu Z, Melin M, Ng Y, Xu W, Sudhof T . A central amygdala to zona incerta projection is required for acquisition and remote recall of conditioned fear memory. Nat Neurosci. 2018; 21(11):1515-1519. PMC: 7261007. DOI: 10.1038/s41593-018-0248-4. View

13.

Plaha P, Khan S, Gill S . Bilateral stimulation of the caudal zona incerta nucleus for tremor control. J Neurol Neurosurg Psychiatry. 2007; 79(5):504-13. DOI: 10.1136/jnnp.2006.112334. View

14.

Mitrofanis J, Ashkan K, Wallace B, Benabid A . Chemoarchitectonic heterogeneities in the primate zona incerta: clinical and functional implications. J Neurocytol. 2004; 33(4):429-40. DOI: 10.1023/B:NEUR.0000046573.28081.dd. View

15.

Kreitzer A, Malenka R . Striatal plasticity and basal ganglia circuit function. Neuron. 2008; 60(4):543-54. PMC: 2724179. DOI: 10.1016/j.neuron.2008.11.005. View

16.

Ohno S, Kuramoto E, Furuta T, Hioki H, Tanaka Y, Fujiyama F . A morphological analysis of thalamocortical axon fibers of rat posterior thalamic nuclei: a single neuron tracing study with viral vectors. Cereb Cortex. 2011; 22(12):2840-57. DOI: 10.1093/cercor/bhr356. View

17.

Ma T, Johnson J, Hoskins G . Organization of the zona incerta in the macaque: an electron microscopic study. Anat Rec. 1997; 249(2):259-75. DOI: 10.1002/(SICI)1097-0185(199710)249:2<259::AID-AR14>3.0.CO;2-N. View

18.

Liu K, Kim J, Kim D, Zhang Y, Bao H, Denaxa M . Lhx6-positive GABA-releasing neurons of the zona incerta promote sleep. Nature. 2017; 548(7669):582-587. PMC: 5958617. DOI: 10.1038/nature23663. View

19.

Gross C, Canteras N . The many paths to fear. Nat Rev Neurosci. 2012; 13(9):651-8. DOI: 10.1038/nrn3301. View

20.

Urbain N, Deschenes M . Motor cortex gates vibrissal responses in a thalamocortical projection pathway. Neuron. 2007; 56(4):714-25. DOI: 10.1016/j.neuron.2007.10.023. View