Coordination of escape and spatial navigation circuits orchestrates versatile flight from threats

Wang, Weisheng; Schuette, Peter J; Nagai, Jun; Tobias, Brooke C; Reis, Fernando M. C. V.; Ji, Shiyu; Lima, Miguel Antonio Xavier de; La-Vu, Mimi Q; Maesta‐Pereira, Sandra; Chakerian, Meghmik; Leonard, Saskia J; Lin, Lilly; Severino, Amie L.; Cahill, Catherine M.; Canteras, Newton S.; Khakh, Baljit S.; Kao, Jennifer L.; Adhikari, Avishek

doi:10.1016/j.neuron.2021.03.033

Cited by 58 publications

(50 citation statements)

References 62 publications

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“…Conversely, the hypothalamic dorsal premammillary nucleus projections to the dPAG control escape elicited by numerous innate threats (Wang et al, 2021). Recent work shows that the medial prefrontal cortex promotes aversion and might regulate defensive strategies through projections to the dPAG (Vander Weele et al, 2018).…”

Section: Resultsmentioning

confidence: 99%

Dorsal periaqueductal gray ensembles represent approach and avoidance states

Reis

Lee

Maesta‐Pereira

et al. 2021

eLife

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Animals must balance needs to approach threats for risk-assessment and to avoid danger. The dorsal periaqueductal gray (dPAG) controls defensive behaviors, but it is unknown how it represents states associated with threat approach and avoidance. We identified a dPAG threat-avoidance ensemble in mice that showed higher activity far from threats such as the open arms of the elevated plus maze and a live predator. These cells were also more active during threat-avoidance behaviors such as escape and freezing, even though these behaviors have antagonistic motor output. Conversely, the threat-approach ensemble was more active during risk-assessment behaviors and near threats. Furthermore, unsupervised methods showed that avoidance/approach states were encoded with shared activity patterns across threats. Lastly, the relative number of cells in each ensemble predicted threat-avoidance across mice. Thus, dPAG ensembles dynamically encode threat approach and avoidance states, providing a flexible mechanism to balance risk-assessment and danger avoidance.

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Section: Resultsmentioning

confidence: 99%

Dorsal periaqueductal gray ensembles represent approach and avoidance states

Reis

Lee

Maesta‐Pereira

et al. 2021

eLife

Self Cite

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“…Recent evidence indicates that dPAG also receives excitatory projections from CCK-expressing glutamatergic neurons residing in the PMD ( Wang et al, 2021 ). These CCK-expressing PMD neurons favor defensive escape ( Figure 1E ).…”

Section: Initiation Of Locomotionmentioning

confidence: 99%

“…However, the increase of c-fos at lPAG may also be due to the correlated activation of sensory cortical and collicular inputs for instance ( Shang et al, 2018 ; Li et al, 2021 ). Furthermore, whether the correlated conspecific-predator responses between PMD and d–lPAG rely on the activation of PMD-CCK-expressing glutamatergic neurons ( Wang et al, 2021 ) is still an open question. Analysis of defensive reactions in PMD-lesioned mice showed that defensive arresting behaviors (i.e., freezing and playing dead) were reduced while active defensive behaviors (i.e., standing upright position, boxing and fleeing) were unaffected in reference to control animals.…”

Section: Termination Of Locomotionmentioning

confidence: 99%

Circuits for State-Dependent Modulation of Locomotion

Pernía-Andrade

Wenger

Esposito

et al. 2021

Front. Hum. Neurosci.

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Brain-wide neural circuits enable bi- and quadrupeds to express adaptive locomotor behaviors in a context- and state-dependent manner, e.g., in response to threats or rewards. These behaviors include dynamic transitions between initiation, maintenance and termination of locomotion. Advances within the last decade have revealed an intricate coordination of these individual locomotion phases by complex interaction of multiple brain circuits. This review provides an overview of the neural basis of state-dependent modulation of locomotion initiation, maintenance and termination, with a focus on insights from circuit-centered studies in rodents. The reviewed evidence indicates that a brain-wide network involving excitatory circuit elements connecting cortex, midbrain and medullary areas appears to be the common substrate for the initiation of locomotion across different higher-order states. Specific network elements within motor cortex and the mesencephalic locomotor region drive the initial postural adjustment and the initiation of locomotion. Microcircuits of the basal ganglia, by implementing action-selection computations, trigger goal-directed locomotion. The initiation of locomotion is regulated by neuromodulatory circuits residing in the basal forebrain, the hypothalamus, and medullary regions such as locus coeruleus. The maintenance of locomotion requires the interaction of an even larger neuronal network involving motor, sensory and associative cortical elements, as well as defined circuits within the superior colliculus, the cerebellum, the periaqueductal gray, the mesencephalic locomotor region and the medullary reticular formation. Finally, locomotor arrest as an important component of defensive emotional states, such as acute anxiety, is mediated via a network of survival circuits involving hypothalamus, amygdala, periaqueductal gray and medullary premotor centers. By moving beyond the organizational principle of functional brain regions, this review promotes a circuit-centered perspective of locomotor regulation by higher-order states, and emphasizes the importance of individual network elements such as cell types and projection pathways. The realization that dysfunction within smaller, identifiable circuit elements can affect the larger network function supports more mechanistic and targeted therapeutic intervention in the treatment of motor network disorders.

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“…(behaviour/anatomy) Inhibition of these SC terminals (Haitao Wang, Chen, et al, 2019), or bilateral activation of GABAergic rostral zona incerta terminals in the dlPAG (Chou et al, 2018), reduces the speed of running evoked by loud noises in head-fixed mice. GABAergic rostral zona incerta neurons innervate glutamatergic (VGLUT2+) neurons in the dlPAG (anatomy / behaviour) The general role of the dlPAG in triggering movement towards refuge, rather than merely running, is indicated by the fact that inhibition of an excitatory input to the dlPAG impairs escape in circumstances in which escape involves jumping or climbing (Wang et al, 2021).…”

Section: Dorsal Periaqueductal Graymentioning

confidence: 99%

Functional Organisation of the Mouse Superior Colliculus

Wheatcroft¹,

Saleem²,

Solomon³

2021

Preprint

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The superior colliculus (SC) is a highly conserved area of the mammalian midbrain that is widely implicated in the organisation and control of behaviour. SC receives input from a large number of brain areas, and provides outputs to a large number of areas. The convergence and divergence of anatomical connections with different areas and systems provides challenges for understanding how SC contributes to behaviours. Recent work in mouse has provided large anatomical datasets, and a wealth of new data from experiments that identify and manipulate different cells within SC, and its inputs and outputs. These data offer an opportunity to better understand the functional roles of SC. However, some of the observations appear, at first sight, to be contradictory. Here we review this recent work and suggest a simple framework which can capture the observations, and that requires only a small change to previous models. Specifically, the functional organisation of SC can be explained by supposing that three largely distinct circuits support three largely distinct classes of behaviour - arrest, turning towards, and the triggering of escape or pursuit. These behavioural classes are supported by the optic, intermediate and deep layers respectively.

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Coordination of escape and spatial navigation circuits orchestrates versatile flight from threats

Cited by 58 publications

References 62 publications

Dorsal periaqueductal gray ensembles represent approach and avoidance states

Dorsal periaqueductal gray ensembles represent approach and avoidance states

Circuits for State-Dependent Modulation of Locomotion

Functional Organisation of the Mouse Superior Colliculus

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