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A cerebellar-prepontine circuit for tonic immobility triggered by an inescapable threat.

ABSTRACT: Sudden changes in the environment are frequently perceived as threats and provoke defensive behavioral states. One such state is tonic immobility, a conserved defensive strategy characterized by powerful suppression of movement and motor reflexes. Tonic immobility has been associated with multiple brainstem regions, but the underlying circuit is unknown. Here, we demonstrate that a strong vibratory stimulus evokes tonic immobility in larval zebrafish defined by suppressed locomotion and sensorimotor responses. Using a circuit-breaking screen and targeted neuron ablations, we show that cerebellar granule cells and a cluster of glutamatergic ventral prepontine neurons (vPPNs) that express key stress-associated neuropeptides are critical components of the circuit that suppresses movement. The complete sensorimotor circuit transmits information from sensory ganglia through the cerebellum to vPPNs to regulate reticulospinal premotor neurons. These results show that cerebellar regulation of a neuropeptide-rich prepontine structure governs a conserved and ancestral defensive behavior that is triggered by an inescapable threat.

SUBMITTER: Bhandiwad AA

PROVIDER: S-EPMC9519051 | biostudies-literature | 2022 Sep

REPOSITORIES: biostudies-literature

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A cerebellar-prepontine circuit for tonic immobility triggered by an inescapable threat.

Bhandiwad Ashwin A AA Chu Nickolas C NC Semenova Svetlana A SA Holmes George A GA Burgess Harold A HA

Science advances 20220928 39

Sudden changes in the environment are frequently perceived as threats and provoke defensive behavioral states. One such state is tonic immobility, a conserved defensive strategy characterized by powerful suppression of movement and motor reflexes. Tonic immobility has been associated with multiple brainstem regions, but the underlying circuit is unknown. Here, we demonstrate that a strong vibratory stimulus evokes tonic immobility in larval zebrafish defined by suppressed locomotion and sensorim ...[more]

PMID: 36170356

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Project description:BackgroundOne priority for animal welfare is for animals to experience less fear, especially during human contact. For domestic animals, breeds that are less fearful may provide genetic resources to develop strains with improved welfare due to lower susceptibility to fear. Genetic predispositions inherited in these breeds might reflect the large diversity of chicken breeds. The goal of the present study was to systematically test a diverse group of chicken breeds to search for breeds that experience less fear.MethodsNineteen chicken breeds from commercial hybrid lines, native layer-type, meat-type and dual-purpose breeds, ornamental breeds as well as bantam breeds were tested in a standardized tonic immobility (TI) test. Chickens were manually restrained on their back, and the time to first head movement and first leg movement, the duration of TI, as well as the number of attempts needed to induce TI were measured.ResultsThe TI response differed among chicken breeds (p ≤ 0.001) for naïve, mature hens. The median number of attempts required to induce TI ranged from 1 to 2 and did not differ significantly among breeds. Median durations were much more variable, with Lohmann Brown showing shortest durations (6 s, 12 s, 58 s for time to first head movement, first leg movement and total duration of TI, respectively). In contrast, medians reached the maximum of 600 s for all three measures in German Creepers. Repeated tests on the same individuals did not affect attempts needed to induce TI nor TI durations. Breeds clustered into two main groups, with layer-type native breeds and ornamental breeds having longer TI durations, and bantam, dual-purpose and meat-type native breeds having shorter TI durations.ConclusionsOur findings provide evidence for substantial variation of fearfulness among breeds. This variation could be linked to the intended use during the breed's specific history. Knowledge and quantitative measurement of these behavioural responses provide the opportunity to improve welfare through selection and future breeding.

Project description:Assessment of negative affective states is a key component of animal welfare research. In laying hens, excessive fearfulness results in reduced production and increased sensitivity to stress. Fearfulness can be defined as a response to a known threat, but anxiety is a response to an unknown threat and may have similar negative consequences. The open field test and tonic immobility test are commonly applied to measure fearfulness in laying hens. An attention bias test that measured individual hen's responses to playback of a conspecific alarm call in the presence of food was recently pharmacologically validated using an anxiogenic drug but was confounded by the hen's typical motionless response in a novel environment. The current study used 56-week old free-range layers to further assess the validity of an attention bias test to differentiate ranging treatment groups in comparison with the open field and tonic immobility tests. The selected hens varied in their range use patterns as tracked by radio-frequency identification technology. 'Indoor' hens did not access the range and 'outdoor' hens ranged daily; previous research has confirmed higher fearfulness in hens that remain indoors. The tonic immobility test did not differentiate ranging groups (P = 0.34), but indoor birds were slower to first step (P = 0.03) and stepped less (P = 0.02) in the open field test. The attention bias test occurred in an isolated wooden box using a conspecific alarm call playback (a threat) and mixed grain (a positive stimulus). The behavioural response of latency to resume eating following playback of the alarm call was measured to differentiate the anxiety states of the indoor and outdoor ranging birds. Before the attention bias test could occur, birds had to be habituated to the test box across three separate 5-minute sessions to increase the willingness to feed within the novel test environment. All birds ate faster across time (P < 0.001) but the indoor birds were slower to eat than the outdoor birds (P < 0.001). In this study, the latency to resume eating following an alarm call was determined to be a poor measure for highly anxious birds as they failed to eat at all. Forty-six percent of indoor hens were excluded for not eating across the 5-minute test. Of the birds that did eat, only 7% of indoor hens ate following playback of the alarm call, compared with 36% of outdoor hens. This repetition of an attention bias test for laying hens highlights the challenges in assessing hens with extreme fearful/anxious responses and that information may be missed when non-performing hens are excluded from behavioural tests. We suggest that latency to eat in a novel arena without any alarm call playback is an informative measure of anxious state that can be applied to all hens but consideration must be made of potential differences in food motivation.

Dataset Information

A cerebellar-prepontine circuit for tonic immobility triggered by an inescapable threat.

Publications

A cerebellar-prepontine circuit for tonic immobility triggered by an inescapable threat.

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