A Direction-selective Cortico-brainstem Pathway Adaptively Modulates Innate Behaviors

Overview

Journal Nat Commun

Specialty Biology

Date 2023 Dec 20

PMID 38123558

Authors

Jiashu Liu

Yingtian He

Andreanne Lavoie

Guy Bouvier

Bao-Hua Liu

Affiliations

Soon will be listed here.

Abstract

Sensory cortices modulate innate behaviors through corticofugal projections targeting phylogenetically-old brainstem nuclei. However, the principles behind the functional connectivity of these projections remain poorly understood. Here, we show that in mice visual cortical neurons projecting to the optic-tract and dorsal-terminal nuclei (NOT-DTN) possess distinct response properties and anatomical connectivity, supporting the adaption of an essential innate eye movement, the optokinetic reflex (OKR). We find that these corticofugal neurons are enriched in specific visual areas, and they prefer temporo-nasal visual motion, matching the direction bias of downstream NOT-DTN neurons. Remarkably, continuous OKR stimulation selectively enhances the activity of these temporo-nasally biased cortical neurons, which can efficiently promote OKR plasticity. Lastly, we demonstrate that silencing downstream NOT-DTN neurons, which project specifically to the inferior olive-a key structure in oculomotor plasticity, impairs the cortical modulation of OKR and OKR plasticity. Our results unveil a direction-selective cortico-brainstem pathway that adaptively modulates innate behaviors.

Citing Articles

Probabilistically constrained vector summation of motion direction in the mouse superior colliculus.

Li C, DePiero V, Chen H, Tanabe S, Cang J Curr Biol. 2025; 35(4):723-733.e3.

PMID: 39842438 PMC: 11859768. DOI: 10.1016/j.cub.2024.12.029.

References

Makino H, Komiyama T . Learning enhances the relative impact of top-down processing in the visual cortex. Nat Neurosci. 2015; 18(8):1116-22. PMC: 4523093. DOI: 10.1038/nn.4061. View

Wang Q, Sporns O, Burkhalter A . Network analysis of corticocortical connections reveals ventral and dorsal processing streams in mouse visual cortex. J Neurosci. 2012; 32(13):4386-99. PMC: 3328193. DOI: 10.1523/JNEUROSCI.6063-11.2012. View

Gamlin P . The pretectum: connections and oculomotor-related roles. Prog Brain Res. 2005; 151:379-405. DOI: 10.1016/S0079-6123(05)51012-4. View

Lur G, Vinck M, Tang L, Cardin J, Higley M . Projection-Specific Visual Feature Encoding by Layer 5 Cortical Subnetworks. Cell Rep. 2016; 14(11):2538-45. PMC: 4805451. DOI: 10.1016/j.celrep.2016.02.050. View

Ringach D, Mineault P, Tring E, Olivas N, Garcia-Junco-Clemente P, Trachtenberg J . Spatial clustering of tuning in mouse primary visual cortex. Nat Commun. 2016; 7:12270. PMC: 4974656. DOI: 10.1038/ncomms12270. 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

Madisen L, Zwingman T, Sunkin S, Oh S, Zariwala H, Gu H . A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci. 2009; 13(1):133-40. PMC: 2840225. DOI: 10.1038/nn.2467. View

Wang Q, Burkhalter A . Stream-related preferences of inputs to the superior colliculus from areas of dorsal and ventral streams of mouse visual cortex. J Neurosci. 2013; 33(4):1696-705. PMC: 3711538. DOI: 10.1523/JNEUROSCI.3067-12.2013. View

Sit K, Goard M . Distributed and retinotopically asymmetric processing of coherent motion in mouse visual cortex. Nat Commun. 2020; 11(1):3565. PMC: 7366664. DOI: 10.1038/s41467-020-17283-5. View

10.

Distler C, Mustari M, Hoffmann K . Cortical projections to the nucleus of the optic tract and dorsal terminal nucleus and to the dorsolateral pontine nucleus in macaques: a dual retrograde tracing study. J Comp Neurol. 2002; 444(2):144-58. DOI: 10.1002/cne.10127. View

11.

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

12.

Kawato M, Gomi H . The cerebellum and VOR/OKR learning models. Trends Neurosci. 1992; 15(11):445-53. DOI: 10.1016/0166-2236(92)90008-v. View

13.

Hoffmann K, Bremmer F, Distler C . Visual response properties of neurons in cortical areas MT and MST projecting to the dorsolateral pontine nucleus or the nucleus of the optic tract in macaque monkeys. Eur J Neurosci. 2009; 29(2):411-23. DOI: 10.1111/j.1460-9568.2008.06585.x. View

14.

Yang T, Maunsell J . The effect of perceptual learning on neuronal responses in monkey visual area V4. J Neurosci. 2004; 24(7):1617-26. PMC: 6730469. DOI: 10.1523/JNEUROSCI.4442-03.2004. View

15.

Kaneko M, Fu Y, Stryker M . Locomotion Induces Stimulus-Specific Response Enhancement in Adult Visual Cortex. J Neurosci. 2017; 37(13):3532-3543. PMC: 5373133. DOI: 10.1523/JNEUROSCI.3760-16.2017. View

16.

Liu B, Huberman A, Scanziani M . Cortico-fugal output from visual cortex promotes plasticity of innate motor behaviour. Nature. 2016; 538(7625):383-387. PMC: 5460756. DOI: 10.1038/nature19818. View

17.

Faulstich B, Onori K, du Lac S . Comparison of plasticity and development of mouse optokinetic and vestibulo-ocular reflexes suggests differential gain control mechanisms. Vision Res. 2004; 44(28):3419-27. DOI: 10.1016/j.visres.2004.09.006. View

18.

Hofer S, Mrsic-Flogel T, Bonhoeffer T, Hubener M . Lifelong learning: ocular dominance plasticity in mouse visual cortex. Curr Opin Neurobiol. 2006; 16(4):451-9. DOI: 10.1016/j.conb.2006.06.007. View

19.

Hoffmann K, Distler C . Quantitative analysis of visual receptive fields of neurons in nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract in macaque monkey. J Neurophysiol. 1989; 62(2):416-28. DOI: 10.1152/jn.1989.62.2.416. View

20.

Foik A, Scholl L, Lean G, Lyon D . Visual Response Characteristics in Lateral and Medial Subdivisions of the Rat Pulvinar. Neuroscience. 2020; 441:117-130. PMC: 7398122. DOI: 10.1016/j.neuroscience.2020.06.030. View