A retinoraphe projection regulates serotonergic activity and looming-evoked defensive behaviour

Huang, Lu; Yuan, Ti‐Fei; Tan, Minjie; Xi, Yue; Hu, Yu; Tao, Qian; Zhao, Zhikai; Zheng, Jiajun; Han, Yushui; Xu, Fuqiang; Luo, Minmin; Sollars, Patricia J.; Pu, Mingliang; Pickard, Gary E.; So, Kwok-Fai; Ren, Chaoran

doi:10.1038/ncomms14908

Cited by 85 publications

(80 citation statements)

References 52 publications

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“…[43][44][45]) provides the suitable substrate for the observed behavioural diversity. The presence of functional degeneracy is consistent with recent studies reporting that the expression of defensive responses can be affected by activation of multiple neuronal pathways [9,10,[46][47][48][49][50]. However our current understanding of the anatomical and functional substrates of this diversity is still insufficient and limited to the locomotion phenotype.…”

Section: The Mapping Between Stimulus and Response Is Not Uniquely Desupporting

confidence: 85%

A high dimensional quantification of mouse defensive behaviours reveals enhanced diversity and stimulus specificity

Storchi¹,

Milosavljevic²,

Allen³

et al. 2020

Preprint

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The ability of specific sensory stimuli to evoke spontaneous behavioural responses in the mouse represents a powerful approach to study how the mammalian brain processes sensory information and selects appropriate motor actions. For visually and auditory guided behaviours the relevant action has been empirically identified as a change in locomotion state. However, the extent to which locomotion alone captures the diversity of those behaviours and their sensory specificity is unknown.To tackle this problem we developed a method to obtain a faithful 3D reconstruction of the mouse body that enabled us to quantify a wide variety of movements and changes in postures. This higher dimensional description of behaviour revealed that responses to different sensory inputs is more stimulus-specific than indicated by locomotion data alone. Thus, equivalent locomotion patterns evoked by different stimuli (e.g. looming and sound evoking locomotion arrest) could be well separated along other dimensions. The enhanced stimulus-specificity was explained by a surprising diversity of behavioural responses. A clustering analysis revealed that distinct combinations of motor actions and postures, giving rise to at least 7 different behaviours, were required to account for stimulus-specificity. Moreover, each stimulus evoked more than one behaviour revealing a robust one-to-many mapping between sensations and behaviours that could not be detected from locomotion data.Our results challenge the current view of visually and auditory guided behaviours as purely locomotion-based actions (e.g. freeze, escape) and indicate that behavioural diversity and sensory specificity unfold in a higher dimensional space spanning multiple motor actions. `

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Section: The Mapping Between Stimulus and Response Is Not Uniquely Desupporting

confidence: 85%

A high dimensional quantification of mouse defensive behaviours reveals enhanced diversity and stimulus specificity

Storchi¹,

Milosavljevic²,

Allen³

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Looming-evoked defensive responses were tested with a behavioral assay of a rapidly expanding dark disk stimulus (looming stimulus of −2 degrees of the visual angle expanded to 20 degrees in 250 ms) presented overhead 15 times over 10.75 s (Fig. 1c ) 5 , 9 , 10 . Under this paradigm, 98.3 ± 0.7% of saline-mice responded by fleeing from the center of the arena and freezing (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Prior studies in rodents documented the role of midbrain structures for rapid processing of threatening stimuli, supporting an important role of subcortical pathway to amygdala 8 , 9 . Using looming stimulations that mimic an approaching aerial predator to initiate a rapid escape response 5 , 10 , a superior colliculus (SC)-lateral posterior nucleus (LP)-basolateral amygdala (BLA) pathway has been revealed for detecting visual threats in mice 9 . That is in agreement with neuroimaging studies in healthy human subjects report co-activation of subcortical structures of the amygdala, the SC, and the pulvinar nucleus of the thalamus during non-conscious visual perception of fearful stimuli 11 – 14 .…”

Section: Introductionmentioning

confidence: 99%

A translational study on looming-evoked defensive response and the underlying subcortical pathway in autism

Chen

Huang

et al. 2017

Sci Rep

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Rapidly approaching objects indicating threats can induce defensive response through activating a subcortical pathway comprising superior colliculus (SC), lateral posterior nucleus (LP), and basolateral amygdala (BLA). Abnormal defensive response has been reported in autism, and impaired synaptic connections could be the underlying mechanism. Whether the SC-LP-BLA pathway processes looming stimuli abnormally in autism is not clear. Here, we found that looming-evoked defensive response is impaired in a subgroup of the valproic acid (VPA) mouse model of autism. By combining the conventional neurotracer and transneuronal rabies virus tracing techniques, we demonstrated that synaptic connections in the SC-LP-BLA pathway were abnormal in VPA mice whose looming-evoked defensive responses were absent. Importantly, we further translated the finding to children with autism and observed that they did not present looming-evoked defensive response. Furthermore, the findings of the DTI with the probabilistic tractography showed that the structural connections of SC-pulvinar-amygdala in autism children were weak. The pulvinar is parallel to the LP in a mouse. Because looming-evoked defensive response is innate in humans and emerges much earlier than do social and language functions, the absence of defensive response could be an earlier sign of autism in children.

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“…Looming-evoked defensive behaviors in rodents mimicking response to aerial predators have recently been used to study the neural circuitry underlying instinctive defensive behaviors [4]. We have previously interpreted a cell-specific neural pathway, from the medial region of the intermediate layer of the superior colliculus (SC) that projects to the lateral posterior thalamic nucleus (LP), to mediate innate freezing behavior resulting from looming stimuli [5,6]. Additionally, another pathway in which PV + neurons in the superficial layer of SC project to the parabigeminal nucleus (PBGN) mediates innate flight behavior [7].…”

Section: Introductionmentioning

confidence: 99%

Stress Accelerates Defensive Responses to Looming in Mice and Involves a Locus Coeruleus-Superior Colliculus Projection

et al. 2018

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Defensive responses to threatening stimuli are crucial to the survival of species. While expression of these responses is considered to be instinctive and unconditional, their magnitude may be affected by environmental and internal factors. The neural circuits underlying this modulation are still largely unknown. In mice, looming-evoked defensive responses are mediated by the superior colliculus (SC), a subcortical sensorimotor integration center. We found that repeated stress caused an anxiety-like state in mice and accelerated defensive responses to looming. Stress also induced c-fos activation in locus coeruleus (LC) tyrosine hydroxylase (TH) neurons and modified adrenergic receptor expression in SC, suggesting a possible Th::LC-SC projection that may be involved in the accelerated defensive responses. Indeed, both anterograde and retrograde neural tracing confirmed the anatomical Th::LC-SC projection and that the SC-projecting TH neurons in LC were activated by repeated stress. Optogenetic stimulation of either LC TH neurons or the Th::LC-SC fibers also caused anxiety-like behaviors and accelerated defensive responses to looming. Meanwhile, chemogenetic inhibition of LC TH neurons and the infusion of an adrenergic receptor antagonist in SC abolished the enhanced looming defensive responses after repeated stress, confirming the necessity of this pathway. These findings suggest that the Th::LC-SC pathway plays a key role in the sophisticated adjustments of defensive behaviors induced by changes in physiological states.

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A retinoraphe projection regulates serotonergic activity and looming-evoked defensive behaviour

Cited by 85 publications

References 52 publications

A high dimensional quantification of mouse defensive behaviours reveals enhanced diversity and stimulus specificity

A high dimensional quantification of mouse defensive behaviours reveals enhanced diversity and stimulus specificity

A translational study on looming-evoked defensive response and the underlying subcortical pathway in autism

Stress Accelerates Defensive Responses to Looming in Mice and Involves a Locus Coeruleus-Superior Colliculus Projection

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