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Processing of visually evoked innate fear by a non-canonical thalamic pathway.

Wei P, Liu N, Zhang Z, Liu X, Tang Y, He X, Wu B, Zhou Z, Liu Y, Li J, Zhang Y, Zhou X, Xu L, Chen L, Bi G, Hu X, Xu F, Wang L - Nat Commun (2015)

Bottom Line: Our results demonstrate that neurons in the superior colliculus (SC) are essential for a variety of acute and persistent defensive responses to overhead looming stimuli.Optogenetic mapping revealed that SC projections to the lateral posterior nucleus (LP) of the thalamus, a non-canonical polymodal sensory relay, are sufficient to mimic visually evoked fear responses.Our results reveal a novel collicular-thalamic-Amg circuit important for innate defensive responses to visual threats.

View Article: PubMed Central - PubMed

Affiliation: Shenzhen Key Lab of Neuropsychiatric Modulation and Collaborative Innovation Center for Brain Science, CAS Center for Excellence in Brain Science, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.

ABSTRACT
The ability of animals to respond to life-threatening stimuli is essential for survival. Although vision provides one of the major sensory inputs for detecting threats across animal species, the circuitry underlying defensive responses to visual stimuli remains poorly defined. Here, we investigate the circuitry underlying innate defensive behaviours elicited by predator-like visual stimuli in mice. Our results demonstrate that neurons in the superior colliculus (SC) are essential for a variety of acute and persistent defensive responses to overhead looming stimuli. Optogenetic mapping revealed that SC projections to the lateral posterior nucleus (LP) of the thalamus, a non-canonical polymodal sensory relay, are sufficient to mimic visually evoked fear responses. In vivo electrophysiology experiments identified a di-synaptic circuit from SC through LP to the lateral amygdale (Amg), and lesions of the Amg blocked the full range of visually evoked defensive responses. Our results reveal a novel collicular-thalamic-Amg circuit important for innate defensive responses to visual threats.

No MeSH data available.


Related in: MedlinePlus

The lateral posterior nucleus of the thalamus is the critical monosynaptic relay underlying the ILSCm–LA circuit.(a) Schematic of AAV–EYFP-mediated anterograde tracing in the SC and EnvA–RV–mCherry in combination with helper AAV-mediated trans-monosynaptic retrograde tracing in the LA. (b) Coronal brain section shows the anterograde projection pattern from the SC (green) and the distribution of trans-monosynaptically labelled neurons from the LA (red). (c) A magnified view of the LP shows the co-localization of axon terminals from the SC projection neurons and the soma of the LP neurons that project to the LA. Inset white box depicts the area. (d) Schematics of the PRV152–EGFP injection in the LA and of the ibotenic acid injection in the LP. (e) Coronal sections show PRV(+) cells (green) in the SC from an intact (top) and LP-lesioned mouse (bottom). (f) PRV(+) cells are mainly located in the ILSCm (n=12 slices; ***P<0.001 by Kruskal–Wallis one-way ANOVA with Dunn's post-hoc test). (g) Comparison of the PRV(+) cells in the medial and lateral ILSC between intact and LP-lesioned mice (n=12 slices per group; ***P<0.001 by two-way ANOVA with Holm–Sidak post-hoc test). Values are represented as mean±s.d.; Scale bars: (b) 1 mm; (c) 250 μm; (e) 500 μm.
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f5: The lateral posterior nucleus of the thalamus is the critical monosynaptic relay underlying the ILSCm–LA circuit.(a) Schematic of AAV–EYFP-mediated anterograde tracing in the SC and EnvA–RV–mCherry in combination with helper AAV-mediated trans-monosynaptic retrograde tracing in the LA. (b) Coronal brain section shows the anterograde projection pattern from the SC (green) and the distribution of trans-monosynaptically labelled neurons from the LA (red). (c) A magnified view of the LP shows the co-localization of axon terminals from the SC projection neurons and the soma of the LP neurons that project to the LA. Inset white box depicts the area. (d) Schematics of the PRV152–EGFP injection in the LA and of the ibotenic acid injection in the LP. (e) Coronal sections show PRV(+) cells (green) in the SC from an intact (top) and LP-lesioned mouse (bottom). (f) PRV(+) cells are mainly located in the ILSCm (n=12 slices; ***P<0.001 by Kruskal–Wallis one-way ANOVA with Dunn's post-hoc test). (g) Comparison of the PRV(+) cells in the medial and lateral ILSC between intact and LP-lesioned mice (n=12 slices per group; ***P<0.001 by two-way ANOVA with Holm–Sidak post-hoc test). Values are represented as mean±s.d.; Scale bars: (b) 1 mm; (c) 250 μm; (e) 500 μm.

Mentions: Anatomical evidence for subcortical pathway connections has been shown in rodents1631, nonhuman primates29 and humans49. In this study, we aimed to identify the connections of the ILSCm–LA subcortical pathway and to determine its function in the innate defensive behaviours of mice. To test the possible circuitry by which the ILSCm and LA interact, we injected the anterograde tracer, AAV–CaMKIIa–EYFP, in the ILSCm and the retrograde trans-monosynaptic tracer, EnvA–rabies virus (RV)–mCherry, in the LA (Fig. 5a and Supplementary Fig. 9a–c). The ILSCm CaMKIIa axons prominently project to the LP, a mouse Pulv-like structure (Fig. 5b). Retrograde RV-positive cells raised from the starter cells in the LA were simultaneously found in the LP, as shown by co-labelling them with green fluorescent protein (GFP) from AAV and with mCherry from rabies (Fig. 5b,c and Supplementary Movie 5), which were mostly confined in the LR and MC subdivisions of the LP (Supplementary Fig. 9d).


Processing of visually evoked innate fear by a non-canonical thalamic pathway.

Wei P, Liu N, Zhang Z, Liu X, Tang Y, He X, Wu B, Zhou Z, Liu Y, Li J, Zhang Y, Zhou X, Xu L, Chen L, Bi G, Hu X, Xu F, Wang L - Nat Commun (2015)

The lateral posterior nucleus of the thalamus is the critical monosynaptic relay underlying the ILSCm–LA circuit.(a) Schematic of AAV–EYFP-mediated anterograde tracing in the SC and EnvA–RV–mCherry in combination with helper AAV-mediated trans-monosynaptic retrograde tracing in the LA. (b) Coronal brain section shows the anterograde projection pattern from the SC (green) and the distribution of trans-monosynaptically labelled neurons from the LA (red). (c) A magnified view of the LP shows the co-localization of axon terminals from the SC projection neurons and the soma of the LP neurons that project to the LA. Inset white box depicts the area. (d) Schematics of the PRV152–EGFP injection in the LA and of the ibotenic acid injection in the LP. (e) Coronal sections show PRV(+) cells (green) in the SC from an intact (top) and LP-lesioned mouse (bottom). (f) PRV(+) cells are mainly located in the ILSCm (n=12 slices; ***P<0.001 by Kruskal–Wallis one-way ANOVA with Dunn's post-hoc test). (g) Comparison of the PRV(+) cells in the medial and lateral ILSC between intact and LP-lesioned mice (n=12 slices per group; ***P<0.001 by two-way ANOVA with Holm–Sidak post-hoc test). Values are represented as mean±s.d.; Scale bars: (b) 1 mm; (c) 250 μm; (e) 500 μm.
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f5: The lateral posterior nucleus of the thalamus is the critical monosynaptic relay underlying the ILSCm–LA circuit.(a) Schematic of AAV–EYFP-mediated anterograde tracing in the SC and EnvA–RV–mCherry in combination with helper AAV-mediated trans-monosynaptic retrograde tracing in the LA. (b) Coronal brain section shows the anterograde projection pattern from the SC (green) and the distribution of trans-monosynaptically labelled neurons from the LA (red). (c) A magnified view of the LP shows the co-localization of axon terminals from the SC projection neurons and the soma of the LP neurons that project to the LA. Inset white box depicts the area. (d) Schematics of the PRV152–EGFP injection in the LA and of the ibotenic acid injection in the LP. (e) Coronal sections show PRV(+) cells (green) in the SC from an intact (top) and LP-lesioned mouse (bottom). (f) PRV(+) cells are mainly located in the ILSCm (n=12 slices; ***P<0.001 by Kruskal–Wallis one-way ANOVA with Dunn's post-hoc test). (g) Comparison of the PRV(+) cells in the medial and lateral ILSC between intact and LP-lesioned mice (n=12 slices per group; ***P<0.001 by two-way ANOVA with Holm–Sidak post-hoc test). Values are represented as mean±s.d.; Scale bars: (b) 1 mm; (c) 250 μm; (e) 500 μm.
Mentions: Anatomical evidence for subcortical pathway connections has been shown in rodents1631, nonhuman primates29 and humans49. In this study, we aimed to identify the connections of the ILSCm–LA subcortical pathway and to determine its function in the innate defensive behaviours of mice. To test the possible circuitry by which the ILSCm and LA interact, we injected the anterograde tracer, AAV–CaMKIIa–EYFP, in the ILSCm and the retrograde trans-monosynaptic tracer, EnvA–rabies virus (RV)–mCherry, in the LA (Fig. 5a and Supplementary Fig. 9a–c). The ILSCm CaMKIIa axons prominently project to the LP, a mouse Pulv-like structure (Fig. 5b). Retrograde RV-positive cells raised from the starter cells in the LA were simultaneously found in the LP, as shown by co-labelling them with green fluorescent protein (GFP) from AAV and with mCherry from rabies (Fig. 5b,c and Supplementary Movie 5), which were mostly confined in the LR and MC subdivisions of the LP (Supplementary Fig. 9d).

Bottom Line: Our results demonstrate that neurons in the superior colliculus (SC) are essential for a variety of acute and persistent defensive responses to overhead looming stimuli.Optogenetic mapping revealed that SC projections to the lateral posterior nucleus (LP) of the thalamus, a non-canonical polymodal sensory relay, are sufficient to mimic visually evoked fear responses.Our results reveal a novel collicular-thalamic-Amg circuit important for innate defensive responses to visual threats.

View Article: PubMed Central - PubMed

Affiliation: Shenzhen Key Lab of Neuropsychiatric Modulation and Collaborative Innovation Center for Brain Science, CAS Center for Excellence in Brain Science, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.

ABSTRACT
The ability of animals to respond to life-threatening stimuli is essential for survival. Although vision provides one of the major sensory inputs for detecting threats across animal species, the circuitry underlying defensive responses to visual stimuli remains poorly defined. Here, we investigate the circuitry underlying innate defensive behaviours elicited by predator-like visual stimuli in mice. Our results demonstrate that neurons in the superior colliculus (SC) are essential for a variety of acute and persistent defensive responses to overhead looming stimuli. Optogenetic mapping revealed that SC projections to the lateral posterior nucleus (LP) of the thalamus, a non-canonical polymodal sensory relay, are sufficient to mimic visually evoked fear responses. In vivo electrophysiology experiments identified a di-synaptic circuit from SC through LP to the lateral amygdale (Amg), and lesions of the Amg blocked the full range of visually evoked defensive responses. Our results reveal a novel collicular-thalamic-Amg circuit important for innate defensive responses to visual threats.

No MeSH data available.


Related in: MedlinePlus