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Tonic Immobility: the Role of Fear and Predation
Abstract
Reviews data from a series of studies designed to test the hypothesis that tonic immobility (TI) represents an innate fear-potentiated response. In experiments using mostly 3–4 wk old Production Red chickens, fear was operationally defined by behavioral changes associated with long immobility reactions (i.e., defecation) and by certain manipulations, including (a) tranquilization, (b) intense auditory stimulation, (c) punishment, and (d) predatory confrontation with live and simulated stimuli, artificial eyes, and a visual cliff. Findings suggest that fear, while not the cause of TI, is an important antecedent condition for manipulating response duration and susceptibility. (61 ref) (PsycINFO Database Record (c) 2012 APA, all rights reserved)
... To assess aspects of bird personality, we used three challenging situations: tonic immobility, new environment, and new object tests. The tonic immobility (TI) test, which induces and measures 'playing dead' behaviour or thanatosis (Edelaar et al., 2012;Gallup, 1977), has been used to assess consistent individual behavioural traits in other wild bird species (e.g. Euplectes afer and Passer montanus, Edelaar et al., 2012). ...
... Euplectes afer and Passer montanus, Edelaar et al., 2012). TI behaviour may facilitate escape from potential predators (Gallup, 1977) and has also been viewed as a sign of fear-like states in domestic animals (Forkman et al., 2007). The ecological relevance of the TI behaviour lies in the fact that the integrity of this behavioural response likely contributes to the effectiveness of anti-predator strategies in wild animals (Edelaar et al., 2012), which can be decreased during domestication, as evidenced in the domesticated Bengalese finch (Lonchura striata var. ...
... Individual ability to perform defensive behaviours in response to environmental stimuli has high adaptive value, and is fundamental for survival (Blanchard et al., 1990). Tonic immobility may deter predators from killing an animal after it has been captured (Gallup, 1977;Thompson et al., 1981). Thompson et al. (1981) reported that as the duration of TI in Japanese quail increased, the time that a cat stalked or handled the bird decreased. ...
Environmental enrichment (EE) is used to promote natural behaviours in captive animals and may hold promise as a form of pre-release training, a strategy for improving coping skills of translocated birds. We investigated the use of EE to enhance foraging and vigilance behaviours of captive Sporophila angolensis, which may be related to post-release survival. We also evaluated whether consistent individual behavioural differences affected birds’ responses to EE. We submitted 19 captive seed-finches to three short-term challenges: tonic immobility (TI), new environment (NE) and new object (NO) tests. TI behaviour is related to fear/escape response to potential predators and novelty tests (NE and NO) assess neophobia, which are ecologically relevant personality traits influencing the shyness-boldness continuum. We noted a pronounced variability among the individuals’ personality traits, both in their fear and escape-related responses in the TI test and along shy/bold z-scores in NE and NO tests. During a period of enrichment, birds spent more time foraging and less time in vigilance states compared with both control phases. Personality traits of the birds affected their responses to enrichment with bolder birds spending more time foraging. The EE-related decrease in vigilance was independent of the birds’ personality traits. Our findings highlight interactions between personality and rearing environment that may impact post-release outcomes for translocated animals.
... In response, animals often avoid detection by predators and facilitate threat assessment by suppressing physical activity (1,2). Behavioral arrest is a common defensive strategy against predatory threat described in many vertebrate and invertebrate species (3)(4)(5) that forms part of the defense cascade, a continuum of behaviors that scale with perceived threat immediacy (6,7). Physical activity is suppressed at each end of the defense cascade as part of responses to both distant and immediate threat. ...
... The core circuit for freezing behavior consists of the periaqueductal gray, although additional regions including the parabrachial nuclei, cortex, and cerebellum have been implicated (2,4,(9)(10)(11). In contrast, very little is known about the neural circuit basis for tonic immobility, a last-resort defensive response, induced by imminent threat or actual restraint, in which animals show diminished sensory and reflex responsiveness (6,7). Tonic immobility has been described in a wide variety of animal species under different names, including "phasic immobility," "playing possum," "death feigning," and "thanatosis" (12). ...
... Given that tonic immobility follows inescapable threat stimuli, our data suggest that the defense cascade framework may be conserved across vertebrates (Fig. 8A). Moreover, the magnitude and persistence of tonic immobility in zebrafish is intensity dependent as described in chick and lizards (6,48). We note that tonic immobility is often accompanied by other behavioral and physiological correlates that we did not measure, including decreased heart rate, increased respiration, tremor, and changes in correlated neural activity (7,19). ...
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.
... The TI test is a tool used to evaluate fearfulness in birds [35][36][37] and represents a defensive reaction that may be used to measure the wellbeing and/or stress levels in poultry [36]. The statistical trend, which was close to significant (p = 0.055), increased the duration of TI over time, suggesting that SFP was a stressful situation for the hens. ...
... The TI test is a tool used to evaluate fearfulness in birds [35][36][37] and represents a defensive reaction that may be used to measure the wellbeing and/or stress levels in poultry [36]. The statistical trend, which was close to significant (p = 0.055), increased the duration of TI over time, suggesting that SFP was a stressful situation for the hens. ...
The aim of the present study was to investigate the ability of two Italian slow-growing poultry breeds (namely, Bionda Piemontese, BP, and Bianca di Saluzzo, BS) to cope with a stressful event, such as collective grouping, using a multifactorial approach. A total of 120 hens of BP and BS breeds were homogenously distributed, according to breed, in 12 pens (10 hens/pen; 6 pens/breed), from 18 to 49 weeks of age. At 50 weeks of age, hens were regrouped (Stressful Farm Practice, SFP), by removing separators, both in indoor and outdoor areas. At 49 weeks of age, 24 hens/breed were randomly selected for the evaluation of welfare (ethological and physiological) parameters, at different time points: T0: 1-week pre-SPF; T1: 1-week post-SFP; T2: 3-week post-SFP; T3: 5-week post-SFP. Egg production was recorded from 38 to 56 weeks of age. Grouping produced a social stress in both BS and BP-laying hens, which was expressed in terms of productive traits (reduction of oviposition), behavioral modification (worsening of plumage condition due to feather peaking and extension of the duration of the tonic immobility test) and physiological modification (increased heterophil/lymphocyte ratio and corticosterone metabolites in droppings). Both breeds reacted in a similar way; in fact, no differences were attributed to the breed. At the end of the observation period, the egg rate fully recovered, while the behavioral and physiological parameters partially recovered but failed to recover to those recorded prior to the stressful event.
... TI can take several seconds to more than an hour (Gallup 1974). TI is an innate, not acquired, response to fear in various species of game birds (Gallup et al. 1971;Borchelt and Ratner 1973;Sargeant and Eberhardt 1975;Gallup 1977;Thompson et al. 1981;Odén et al. 2005). ...
... The pheasants need to maintain their escape reflexes and shyness. Freezing and immobility are reactions to fear and are typical examples of predator avoidance behaviour described in various game birds species (Gallup et al. 1971;Borchelt and Ratner 1973;Sargeant and Eberhardt 1975;Gallup 1977;Thompson et al. 1981;Odén et al. 2005). They present the last stage of various anti-predatory mechanisms leading to the predator losing its interest in the prey (Jones et al. 1991). ...
The survival of captive-reared pheasants in the wild depends primarily on their ability to avoid predators, therefore, pheasants need to maintain their innate anti-predatory behaviour. The aim of this study was to assess the effects of age and disturbance on tonic immobility (TI) in pheasants ( Phasianus colchicus ) kept in a commercial rearing facility. TI tests were performed in pheasants aged 8, 10, 12, 14 and 16 weeks. Randomly selected pheasants of the same age were tested either immediately after capture (group C) or after exposure to various stimuli/disturbance (group D). No significant differences in the number of attempts to induce TI were found between the observed groups of pheasants (the vast majority of pheasants remained immobile on the first attempt). The effect of age was found only in group D, where birds aged 14 and 16 weeks showed a reduction in the duration of TI compared to younger birds. In group C, the duration of TI in pheasants of different ages did not differ. The results document a change in the duration of TI in response to an intense stimulus depending on the age of captive-reared pheasants. Knowledge of changes in anti-predatory behaviour depending on age and habituation to the environment and new stimuli is essential when determining the optimal age for pheasants to be released into the wild considering its impact on the subsequent survival of the released birds. Birds released at an older age and thus accustomed to repeated disturbances during captive rearing may have impaired defence behaviour.
... In humans, behavioral arrest, or tonic immobility, may be linked to episodes of paralysis during traumatic events. [12][13][14] Emerging evidence suggests a strong correlation between trauma-induced tonic immobility and post-traumatic stress disorder (PTSD). 15, 16 Therefore, understanding how animals respond to threats and how their nervous system reacts to the state of restraint would help determine how serious threats are processed in animals and how emotional behaviors are encoded by the nervous system, both at the level of specific neural circuits and distinct subtypes of neurons that regulate them. ...
When trapped in a physical restraint, animals must select an escape strategy to increase their chances of survival. After falling into an inescapable trap, they react with stereotypical behaviors that differ from those displayed in escapable situations. Such behaviors involve either a wriggling response to unlock the trap or feigning death to fend off a predator attack. The neural mechanisms that regulate animal behaviors have been well-characterized for escapable situations but not for inescapable traps. We report that restrained vinegar flies exhibit alternating flailing and immobility to free themselves from the trap. We used optogenetics and intersectional genetic approaches to show that, while broader serotonin activation promotes immobility, serotonergic cells in the ventral nerve cord (VNC) regulate immobility states majorly via 5-HT7 receptors. Restrained and freely moving locomotor states are controlled by distinct mechanisms. Taken together, our study has identified serotonergic switches of the VNC that promote environment-specific adaptive behaviors.
... Exaggeratedly heightened tonicity and decreased postural sway create a tonic immobility or "freeze" response, exhibited by animals (Webster et al., 1981;Fleischmann and Urca, 1988;Porro and Carli, 1988) and humans (Suarez and Gallup, 1979;Heidt et al., 2005;Marx et al., 2008) who experience imminent threat (for a review, see Terpou et al., 2019b). This response is mediated by somatosensory and vestibular feedback (Klemm, 1971;Gallup, 1977;Fleischmann and Urca, 1988), and is hypothesized to deter predators who are wired to detect motion in their prey and enable the animal to monitor its environment and flee if necessary (Kozlowska et al., 2015). Tonic immobility has been reported by study participants with PTSD under traumatic memory recall (Volchan et al., 2011;Fragkaki et al., 2016;de Kleine et al., 2018), suggesting that traumatic memories remain connected to subconscious postural responses. ...
Although the manifestation of trauma in the body is a phenomenon well-endorsed by clinicians and traumatized individuals, the neurobiological underpinnings of this manifestation remain unclear. The notion of somatic sensory processing, which encompasses vestibular and somatosensory processing and relates to the sensory systems concerned with how the physical body exists in and relates to physical space, is introduced as a major contributor to overall regulatory, social-emotional, and self-referential functioning. From a phylogenetically and ontogenetically informed perspective, trauma-related symptomology is conceptualized to be grounded in brainstem-level somatic sensory processing dysfunction and its cascading influences on physiological arousal modulation, affect regulation, and higher-order capacities. Lastly, we introduce a novel hierarchical model bridging somatic sensory processes with limbic and neocortical mechanisms regulating an individual’s emotional experience and sense of a relational, agentive self. This model provides a working framework for the neurobiologically informed assessment and treatment of trauma-related conditions from a somatic sensory processing perspective.
... When a human being is confronted with an overwhelming danger, tonic immobility (TI) is one possible reaction. TI is characterized by a strong motoric inhibition, a paralysis of movement, thought, emotion, and vocalization (Gallup, 1977). TI occurs when the victim finds him-/herself at an impending threat to life and escape is perceived to be impossible , and when freezing, fight, or flight are no longer an option for survival, e.g. if there is physical contact with the perpetrator (Hagenaars & Hagenaars, 2020). ...
Background
Tonic Immobility (TI) is a peri-traumatic response that appear to play a vital role in the development of posttraumatic stress disorder (PTSD). TI is characterized by a strong motoric inhibition, a paralysis of movement, thought, emotion, and vocalization, and has primarily been studied in association with rape and childhood sexual assault.
Aim
The present study examines the role of TI in developing ICD-11 PTSD and disturbances in self-organization (DSO) following different types of intimate partner violence (IPV), i.e., physical, sexual, and psychological violence, in a clinical sample of N = 150 women.
Methods
A measurement model for ICD-11 PTSD and disturbances in self-organization (DSO) was constructed using confirmatory factor analysis and three models were computed to test whether the different subtypes of IPV were directly related to symptom severity, or whether they were partly or fully mediated by TI.
Results
Controlling for other types of violence, psychological violence was the only type of violence directly and indirectly related to ICD-11 PTSD and DSO. While most of the relationship consisted of a direct effect, TI acted as a partial mediator of the relationship between psychological violence and PTSD and DSO.
Discussion
Results are discussed regarding our understanding of trauma and how psychologically threatening events can elicit a peri-traumatic response of TI, which has previously been associated primarily with threats to life or physical integrity.
... In humans, behavioral arrest, or tonic immobility, may be linked to episodes of paralysis during traumatic events. [12][13][14] Emerging evidence suggests a strong correlation between trauma-induced tonic immobility and post-traumatic stress disorder (PTSD). 15, 16 Therefore, understanding how animals respond to threats and how their nervous system reacts to the state of restraint would help determine how serious threats are processed in animals and how emotional behaviors are encoded by the nervous system, both at the level of specific neural circuits and distinct subtypes of neurons that regulate them. ...
When trapped in a physical restraint, animals must select an escape strategy to increase their chances of survival. Falling into an inescapable trap, they react with stereotypical behaviors that differ from those displayed in escapable situations. Such behaviors involve either a wriggling response to unlock the trap or feigning death to fend off a predator attack. The neural mechanisms that regulate animal behaviors have been well-characterized for escapable situations but not for inescapable traps. We report that restrained vinegar flies exhibit alternating flailing and immobility to free themselves from the trap. We used optogenetics and intersectional genetic approaches to show that, while broader serotonin activation promotes immobility, serotonergic cells in distinct regions of the ventral nerve cord (VNC) regulate activity and immobility states via 5-HT1A and 5-HT7 receptors. Restraint states and free-moving locomotion are controlled by distinct mechanisms. Taken together, our study has identified serotonergic switches of the VNC subcircuits that promote environment-specific adaptive behaviors.
The concept of ‘coping strategies’ has received increasing attention over the last few years. Benus et al. (1991) reported two major types of strategy in rodents. These were the so-called active and passive strategies. The active strategy consists of being aggressive, forming behavioural routines and showing low responsiveness to changes in the environment, the passive strategy involves being low aggressive, flexible and responsive to changes in the environment. Hessing et al. (1993) reported similar findings in pigs. These strategies have potential implications for pig husbandry, since they may be more or less adaptive in specific farming environments.
On May 25, 2020, the death of George Floyd ignited the consciousness of many who were questioning the grave injustices of a society that is inequitable, unfair, and plagued with structural racism. For many students at Molloy College, an institution grounded in the Dominican pillars of community, study, spirituality, and service, Mr. Floyd's death marked a pivotal moment. Students called for the institution to provide guidance and action for how they could be transformation agents in addressing these issues. Responding to the call, and leading the way, four African American faculty coined Sistas in Action, created a workshop that focused on themes of anti-racism, and introduced their 3-C model for having conversations dealing with coded language. Results and impact of the workshops were demonstrated through student surveys showing greater confidence in talking about race and taking action. Discussion and recommendations concerning Black faculty leadership in partnership with the institution for the benefit of the education community is explored.
An effective tranquilizing agent for poultry could have practical use both commercially and experimentally. Such an agent should make chickens and turkeys easier to handle and should also reduce the injuries caused by excitement when they are being caught for weighing, marketing, blood testing, or other reasons. Its use might also be of value in reducing the cannibalistic tendency so prevalent in some flocks. An extremely useful tranquilizing agent for poultry should not only be effective when given in the feed or water, but should also be non-toxic and economical.
Secord in a personal communication as reported by Earl (1956) obtained results indicating that the tranquilizing agent reserpine decreased mortality in wild turkeys being transported from the hatchery to the releasing grounds.
In this laboratory, the effect of feeding two tranquilizing agents to young White Leghorns was investigated. One of these was Miltown1 and the other Sparine.2 The calming effect . . .
The researchers who, three centuries ago, applied the term “hypnosis” to catalepsy in animals most probably did so because of the similar appearance of these two conditions. From the results of subsequent investigations, it is justifiable to regard the term “animal hypnosis” as highly appropriate. Motor inhibition in animals and the state of hypnotic trance in man appear to be genetically interrelated, have a similar adaptive significance and, in all probability, possess certain common neurophysiological mechanisms.
Résumé On donne la description du phénomène de l'immobilité tonique, appelée fréquemment “l'hypnose animale,” ou “faisant le mort.” On discute cet état au point de vue de sa signification biologique et aussi comme moyen pour l'étude des processus nerveux centraux. On présente ici une analyse du mécanisme physiologique de l'immobilité tonique chez le lésard Anolis carolinensis. Puisque ce travail exige, entre autres choses, la détermination de l'effet de la température sur la durée des périodes de l'immobilité comme indice de la dynamique, on donne un résumé général de la méthode d'analyse selon la température appliquée aux systèmes vivants. Selon diverses expériences on suggère que l'immobilité tonique chez Anolis est produite par une décharge diffuse des neurones internonces de la medulla oblongata lesquels sont engagés dans la maintenance du tonus postural. On suggère que cette décharge dans les cas de l'immobilité causée par la manipulation est due à la désorganisation des impulsions afférentes proprioceptives par le stimulus immobilisant. Cette décharge en masse des centres médullaires, on suppose, cause la contraction des muscles du squelette et l'inhibition des centres plus élevés. On suggère que l'adrénaline libérée au même temps par une irradiation d'impulsions aux centres sympathiques tend à prolonger cet équilibre fonctionnel du système nerveux jusqu'à ce que la concentration de l'adrénaline tombe au-dessous d'une valeur de seuil. Referat Man heschreibt die Erscheinung der tonischen Unbeweglichkeit, auch als “Tierhypnose,” “sich tot stellen” und “playing ‘possum” bekannt. Dieser Zustand wird in seiner biologischen Bedeutung beleuchtet, sowie als Mittel zur Untersuchung der Centralnervenfunktionen. Eine experimentelle Analyse des physiologischen Mechanismus der tonischen Unbeweglichkeit in der Eidechse, Anolis carolinensis, wird dargelegt. Da diese Arbeit-unter andern Vorgängen-auch die Bestimmung der Wirkung der Temperatur auf die Zeitdauer der Unbeweglichkeit, als Nachweis der zugrunde liegenden Dynamik, mit einschliesst, so wird ein allgemeines Resumé der Temperaturmethode der Analyse, und ihre Anwendung auf den lebenden Organismus, mitgeteilt. Verschiedene, experimentelle Ergebnisse deuten darauf hin, dass die tonische Unbeweglichkeit in Anolis, durch eine starke Entladung internunzialer Neuronen in die Medulla oblongata hervorgerufen wird, welche zur Erhaltung des Stellungstonus beitragen. Man vermutet das diese Entladung-in Fällen wo die Unbeweglichkeit durch Manipulation erzeugt wird-durch die Auflösung der propriozeptiven Impulse hervogebracht wird, ausgelöst durch den Reiz der die Unbeweglichkeit verursacht. Diese Massenentladung der medularen Zentern verursacht vermutlich, Kontraktion der Hauptmuskeln und Hemmung der höhern Nervenzentern. Man deutet an, dass Adrenalin, gleichzeitig ausgelöst durch die Ausstrahlung der Impulse zu sympathischen Nervenzentern, eine Verlängerung dieses “Gleichgewichts” der Funktionen des Nerven-systems bewirkt, bis das die Adrenalinkonzentration unter den Schwellenwert sinkt.
Six week old domestic chickens were either given electric shock or no shock prior to manual restraint. Animals receiving pre-induction shock remained immobile appreciably longer than Ss given no shock. Results were interpreted as supporting the notion that fear is what underlies hypnotic or immobility reactions in animals.
Predation by captive red foxes (Vulpes fulva) on approximately 50 ducks comprised of five species was observed in tests conducted at the Northern Prairie Wildlife Research Center, Jamestown, North Dakota. Most ducks were attacked from a rear or lateral position and seized in the cervical or thoracic region. All birds became immobile (death-feigned) immediately when seized and with few exceptions remained motionless during prey-handling and for varying lengths of time thereafter. Initial death feints lasted from 20 sec to 14 min. Recovery was delayed by tactile, visual and, possibly, auditory cues from the foxes. Death-feigning birds appeared alert and often took advantage of escape opportunities. Twenty-nine birds survived initial capture and handling by the foxes. Naive foxes were wary of ducks during initial confrontations, but experienced foxes showed little hesitation in attacking them. After capture, most ducks were taken alive to lay-down sites where they were mouthed and often killed. Then the ducks were usually cached or taken to dens or pups. Several birds were cached alive. Red foxes appear to have adapted to the escape of death-feigning ducks by learning to kill some birds soon after capture and by the evolution of an appendage-severing behavior. Death feigning appears to be a highly developed antipredator behavior of ducks that facilitates the escape of some birds after capture by red foxes.
Two experiments were performed to investigate the effects of age and prior testing on immobility reactions of chickens from two through 66 days of age. In each experiment, one group was tested repeatedly while different subgroups were tested only once at the ages of the repeated test group and then discarded. Tests were conducted by turning each of the 305 birds on its side and holding it down for 15 seconds after which the immobility reactions were observed and timed. The immobility reaction was found to be virtually absent until seven to ten days of age, after which the response reached and maintained the arbitrary maximum duration of twelve minutes until birds were 59 days of age. Prior testing and the handling associated with it significantly reduced duration and incidence of immobility at all ages after nine days. The results are interpreted in terms of immobility as part of a fear reaction.
Notes that, because of its sensitivity to various manipulations associated with either increases or decreases in aversive stimulation, tonic immobility seems to qualify as a fear reaction. The present experiments provided an independent assessment of the aversive properties of immobility induction. In Exp I, using 32 Production Red day-old chickens, a cue previously paired with onset of immobility suppressed activity in a stabilimeter. Similarly, in Exp II, with 24 Production Red day-old chickens, response-contingent immobilization produced punishmentlike effects in an instrumental conditioning paradigm. Taken together, results support the notion that the physical restraint involved in immobility induction is an aversive event.