J Comp Physiol A (2014) 200:305–310 DOI 10.1007/s00359-014-0884-4
Original Paper
Proven cardiac changes during death‑feigning (tonic immobility) in rabbits (Oryctolagus cuniculus) Amália Turner Giannico · Leandro Lima · Rogério Ribas Lange · Tilde Rodrigues Froes · Fabiano Montiani‑Ferreira
Received: 2 July 2013 / Revised: 21 November 2013 / Accepted: 22 January 2014 / Published online: 11 February 2014 © Springer-Verlag Berlin Heidelberg 2014
Abstract Tonic immobility (TI) is a response to fear or threat by remaining motionless, principally when attacked by predators from which there is no possibility of escape. Thus, here we demonstrate a way of easily reproducing this phenomenon in a laboratory setting and characterize the cardiac electromechanical alterations during TI. We observed a significant decrease in heart rate (HR) and changes of rhythm in electrocardiogram during TI in rabbits. Echocardiogram showed a significant increase in the left ventricle chamber diameter during systole and a consequent decrease in fractional shortening and ejection fraction, in addition to the HR and rhythm changes. There was also a significant decrease in aortic and pulmonary artery blood flow. Diastolic functional changes included a significant decrease of the peak atrial contraction velocity (A peak) and consequent increase in the ratio of peak early diastolic velocity to A peak and increased isovolumetric relaxation time. We were able to prove that TI changes the cardiac function considerably. Although the “fightor-flight” response is the most common response to fear, which is characterized by the action of sympathetic nervous system with tachycardia and increased physical activity, TI is an alternative anti-predator behavior causing cardiac changes opposite to the “fight-or-flight” phenomenon.
A. T. Giannico · L. Lima · R. R. Lange · T. R. Froes · F. Montiani‑Ferreira (*) Department of Veterinary Medicine, Federal University of Paraná, Rua dos Funcionários, 1540, Curitiba, PR 80035‑050, Brazil e-mail: [email protected] A. T. Giannico e-mail: [email protected]
Keywords Cardiology · Fear behavior · Defensive behavior · Tonic immobility
Introduction The most common animal response to fear or threat is the “fight-or-flight” response, in which the action of the sympathetic nervous system induces increased physical activity and systolic blood pressure, tachycardia and dilatation of vessels feeding skeletal muscle (Alboni et al. 2008). However, many animals can show a different response to fear or threat by remaining motionless, principally when attacked by predators from which there is no possibility of escape (Alboni et al. 2008). This phenomenon caused by a fear response is called tonic immobility (TI) in which a transitory and reversible state of profound motor inhibition can be induced in susceptible species (Klemm 1971; Valance et al. 2008). TI might be also known by other names such as “animal hypnosis”, “immobilization catatonia” or “death-feigning” (Rusinova and Davydov 2010). Some physiological changes observed during TI suggest that the autonomic nervous system (ANS) is strongly implicated in this process (Alboni et al. 2008). However, the differing contributions of the ANS’s subsystems (sympathetic and parasympathetic) are unclear during the TI process (Valance et al. 2008). Evidence suggests that TI is not associated with any suspension of consciousness (Marx et al. 2008) and, although the animals appear incapable of resisting or escaping, they seem to actively process the event and the environment (Gallup et al. 1972; Richardson et al. 1977; Sigman and Prestrude 1981). Thus, induction of TI appears to be influenced by the autonomic changes induced by the emotional response such as the mere presence of a predator or the situation where the animal is
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subdued (Gilman et al. 1950; Nash and Gallup 1975; Valance et al. 2008). It seems like TI evolved in some animal species as an alternative anti-predator behavior to ‘‘fight-or-flight’ response designed to increase the chance of survival. It was first suggested by Charles Darwin (1900) and has been suggested by some authors that TI is a fear-motivated terminal defense mechanism employed by some prey animals that serves to limit injury and provide the possibility of escape (Sergeant and Eberhardt 1975; Ewell et al. 1981; Thompson et al. 1981). The probable adaptive advantage of TI lies in the induced lack of motion. This behavior can deceive the predator into believing the prey is already dead and reduces the probability of a predator continuing its attack (Valance et al. 2008; Silva et al. 2012). The predator may then relax or change its grip, giving the prey animal a last chance to escape. Some experimental studies suggest that the survival rate is indeed increased by this behavior (Alboni et al. 2008). The occurrence of this response in the animal kingdom is not completely understood and the laboratory reproducibility of bradycardia during TI in animals requires further investigation (Carli 1974; Alboni et al. 2008). Cardiac mechanical changes during this phenomenon have never been described before.
Materials and methods We used clinically healthy 6-month-old New Zealand white rabbits (Oryctolagus cuniculus) weighing between 2 and 3 kg. Electrocardiography (ECG) was performed on 60 animals (27 males and 33 females). Echocardiography was performed in 37 of these animals (13 males and 24 females). Tonic immobility was induced after physical restraint by the skin over the neck (“scruffing”) and then quickly putting the animal on its right side (right lateral recumbency), emulating the subjugation produced by a predator’s jaw. The ECG was performed using an ECGP system computerized electrocardiograph (Brazilian Electronic Technology, Brazil). Before each ECG recording procedure, the electrodes were positioned on each animal, and after 5 min to allow the animals to calm down, the procedures were started. ECG tracings were recorded continuously and uninterrupted during the whole procedure on each animal. The heart rate (HR) evaluation period on each animal’s ECG was divided into three 1-minute-long stages: prerestraint (Pre-R), physical restraint (R) and post-restraint (Post-R). HR was subsequently calculated using the number of QRS complexes in each stage. To perform the echocardiography the animals were restrained in the same way and the animals were maintained
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J Comp Physiol A (2014) 200:305–310
either in left or right lateral recumbency. For each animal, the echocardiographic exam was performed on a different day than the ECG was recorded and thus, one procedure did not alter the response to handling for the second. The echocardiographic exam included recording of morphologic and functional parameters before and during TI. The echocardiography with M-mode, two-dimensional and Doppler analysis was performed using an ultrasound system (Esaote, Italy) equipped with a 10-MHz setorial transducer. ECG procedures required an average time of 8 min and each echocardiographic exam required about 10 min. The parameters were statistically analyzed with t tests using statistical software (StatView, SAS Institute, Cary, NC, USA). Values of P
Original Paper
Proven cardiac changes during death‑feigning (tonic immobility) in rabbits (Oryctolagus cuniculus) Amália Turner Giannico · Leandro Lima · Rogério Ribas Lange · Tilde Rodrigues Froes · Fabiano Montiani‑Ferreira
Received: 2 July 2013 / Revised: 21 November 2013 / Accepted: 22 January 2014 / Published online: 11 February 2014 © Springer-Verlag Berlin Heidelberg 2014
Abstract Tonic immobility (TI) is a response to fear or threat by remaining motionless, principally when attacked by predators from which there is no possibility of escape. Thus, here we demonstrate a way of easily reproducing this phenomenon in a laboratory setting and characterize the cardiac electromechanical alterations during TI. We observed a significant decrease in heart rate (HR) and changes of rhythm in electrocardiogram during TI in rabbits. Echocardiogram showed a significant increase in the left ventricle chamber diameter during systole and a consequent decrease in fractional shortening and ejection fraction, in addition to the HR and rhythm changes. There was also a significant decrease in aortic and pulmonary artery blood flow. Diastolic functional changes included a significant decrease of the peak atrial contraction velocity (A peak) and consequent increase in the ratio of peak early diastolic velocity to A peak and increased isovolumetric relaxation time. We were able to prove that TI changes the cardiac function considerably. Although the “fightor-flight” response is the most common response to fear, which is characterized by the action of sympathetic nervous system with tachycardia and increased physical activity, TI is an alternative anti-predator behavior causing cardiac changes opposite to the “fight-or-flight” phenomenon.
A. T. Giannico · L. Lima · R. R. Lange · T. R. Froes · F. Montiani‑Ferreira (*) Department of Veterinary Medicine, Federal University of Paraná, Rua dos Funcionários, 1540, Curitiba, PR 80035‑050, Brazil e-mail: [email protected] A. T. Giannico e-mail: [email protected]
Keywords Cardiology · Fear behavior · Defensive behavior · Tonic immobility
Introduction The most common animal response to fear or threat is the “fight-or-flight” response, in which the action of the sympathetic nervous system induces increased physical activity and systolic blood pressure, tachycardia and dilatation of vessels feeding skeletal muscle (Alboni et al. 2008). However, many animals can show a different response to fear or threat by remaining motionless, principally when attacked by predators from which there is no possibility of escape (Alboni et al. 2008). This phenomenon caused by a fear response is called tonic immobility (TI) in which a transitory and reversible state of profound motor inhibition can be induced in susceptible species (Klemm 1971; Valance et al. 2008). TI might be also known by other names such as “animal hypnosis”, “immobilization catatonia” or “death-feigning” (Rusinova and Davydov 2010). Some physiological changes observed during TI suggest that the autonomic nervous system (ANS) is strongly implicated in this process (Alboni et al. 2008). However, the differing contributions of the ANS’s subsystems (sympathetic and parasympathetic) are unclear during the TI process (Valance et al. 2008). Evidence suggests that TI is not associated with any suspension of consciousness (Marx et al. 2008) and, although the animals appear incapable of resisting or escaping, they seem to actively process the event and the environment (Gallup et al. 1972; Richardson et al. 1977; Sigman and Prestrude 1981). Thus, induction of TI appears to be influenced by the autonomic changes induced by the emotional response such as the mere presence of a predator or the situation where the animal is
13
306
subdued (Gilman et al. 1950; Nash and Gallup 1975; Valance et al. 2008). It seems like TI evolved in some animal species as an alternative anti-predator behavior to ‘‘fight-or-flight’ response designed to increase the chance of survival. It was first suggested by Charles Darwin (1900) and has been suggested by some authors that TI is a fear-motivated terminal defense mechanism employed by some prey animals that serves to limit injury and provide the possibility of escape (Sergeant and Eberhardt 1975; Ewell et al. 1981; Thompson et al. 1981). The probable adaptive advantage of TI lies in the induced lack of motion. This behavior can deceive the predator into believing the prey is already dead and reduces the probability of a predator continuing its attack (Valance et al. 2008; Silva et al. 2012). The predator may then relax or change its grip, giving the prey animal a last chance to escape. Some experimental studies suggest that the survival rate is indeed increased by this behavior (Alboni et al. 2008). The occurrence of this response in the animal kingdom is not completely understood and the laboratory reproducibility of bradycardia during TI in animals requires further investigation (Carli 1974; Alboni et al. 2008). Cardiac mechanical changes during this phenomenon have never been described before.
Materials and methods We used clinically healthy 6-month-old New Zealand white rabbits (Oryctolagus cuniculus) weighing between 2 and 3 kg. Electrocardiography (ECG) was performed on 60 animals (27 males and 33 females). Echocardiography was performed in 37 of these animals (13 males and 24 females). Tonic immobility was induced after physical restraint by the skin over the neck (“scruffing”) and then quickly putting the animal on its right side (right lateral recumbency), emulating the subjugation produced by a predator’s jaw. The ECG was performed using an ECGP system computerized electrocardiograph (Brazilian Electronic Technology, Brazil). Before each ECG recording procedure, the electrodes were positioned on each animal, and after 5 min to allow the animals to calm down, the procedures were started. ECG tracings were recorded continuously and uninterrupted during the whole procedure on each animal. The heart rate (HR) evaluation period on each animal’s ECG was divided into three 1-minute-long stages: prerestraint (Pre-R), physical restraint (R) and post-restraint (Post-R). HR was subsequently calculated using the number of QRS complexes in each stage. To perform the echocardiography the animals were restrained in the same way and the animals were maintained
13
J Comp Physiol A (2014) 200:305–310
either in left or right lateral recumbency. For each animal, the echocardiographic exam was performed on a different day than the ECG was recorded and thus, one procedure did not alter the response to handling for the second. The echocardiographic exam included recording of morphologic and functional parameters before and during TI. The echocardiography with M-mode, two-dimensional and Doppler analysis was performed using an ultrasound system (Esaote, Italy) equipped with a 10-MHz setorial transducer. ECG procedures required an average time of 8 min and each echocardiographic exam required about 10 min. The parameters were statistically analyzed with t tests using statistical software (StatView, SAS Institute, Cary, NC, USA). Values of P
