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Excessive aggression as model of violence: a critical evaluation of current preclinical methods

  • Theoretical and Methodological Perspectives
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Abstract

Rationale

Preclinical experimental models of pathological aggressive behavior are a sorely understudied and difficult research area.

Objectives

How valid, reliable, productive, and informative are the most frequently used animal models of excessive aggressive behavior?

Methods

The rationale, key methodological features, supporting data, and arguments as well as their disadvantages and limitations of the most frequently used animal models for excessive aggressive behavior are summarized and their validity and reliability are evaluated.

Results

Excessive aggressive behavior is validly and reliably seen in (1) a proportion of feral-derived rats and selectively bred mice; (2) rats with compromised adrenal function resulting in a hypoglucocorticoid state; (3) a significant minority of mice, rats, and monkeys after consumption of a moderate dose of alcohol; and (4) resident animals of various species after social instigation. Limitations of these procedures include restrictive animal research regulations, the requirement of expertise in surgical, pharmacological, and behavioral techniques, and the behaviorally impoverished mouse strains that are used in molecular genetics research. Promising recent initiatives for novel experimental models include aggressive behaviors that are evoked by optogenetic stimulation and induced by the manipulation of early social experiences such as isolation rearing or social stress.

Conclusions

One of the most significant challenges for animal models of excessive, potentially abnormal aggressive behavior is the characterization of distinctive neurobiological mechanisms that differ from those governing species-typical aggressive behavior. Identifying novel targets for effective intervention requires increased understanding of the distinctive molecular, cellular, and circuit mechanisms for each type of abnormal aggressive behavior.

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Authors and Affiliations

  1. Department of Psychology, Tufts University, Bacon Hall, 530 Boston Ave, Medford, MA, 02155, USA

    Klaus A. Miczek

  2. Departments of Psychiatry, Pharmacology and Neuroscience, Tufts University School of Medicine, Boston, MA, 02110, USA

    Klaus A. Miczek

  3. Department of Behavioral Physiology, University of Groningen, PO Box 11103, 9700, CC, Groningen, The Netherlands

    Sietse F. de Boer

  4. Institute of Experimental Medicine, 1450, Budapest, PO Box 67, Hungary

    Jozsef Haller

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  1. Klaus A. Miczek
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  2. Sietse F. de Boer
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  3. Jozsef Haller
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Corresponding author

Correspondence to Klaus A. Miczek.

Additional information

This research was supported by NIH grants DA031734 and AA013983 to KAM.

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Video 1

Non-vulnerable area attack. The recording shows a short episode of an aggressive encounter between a sham-operated resident and a naive intruder. The attack episode was recorded in low light; the opponents were illuminated by the infrared light source of the camcorder. The biting attack starts by lateral or sideways threat, after which the resident bends over the intruder in an attempt to bite. Accidentally, however, the mouth of the resident comes close to the belly of the opponent, i.e., a vulnerable target (see the fourth second of the recording). The deliberate avoidance of vulnerable targets by control rats is depicted by the behavior of the resident, which quickly corrects the position of its mouth, and bites the left flank of the intruder. The intruder immediately submits. This reaction to the bite is indicative of a “hard bite”. Note that the resident avoids biting the belly of the submissive opponent, despite the fact that this body area is clearly exposed and easy to bite. At the end of the bite, the intruder recovers relatively quickly, and resumes the exploration of the environment. (MPG 4845 kb)

Video 2

Vulnerable area attacks. The recording shows a short episode of an aggressive encounter between an ADXr resident and a naive intruder. The attack episode was recorded in low light; the opponents were illuminated by the infrared light source of the camcorder. At the start of the episode, both rats are in an upright posture, and reciprocally sniff each other. The resident suddenly delivers a soft bite targeting the nose of the intruder (i.e., a vulnerable area). Note that the intruder responds by upright freezing to the next approach by the resident, despite the fact that the bite was clearly soft. After a short episode of offense by the resident, the opponent falls back into submission, and is immediately bitten just above the right paw, at the border between the throat and abdomen (i.e., a vulnerable target). After this bite, the opponent remains in supine posture even after the resident stops keeping it down. Albeit not reported in earlier studies, vulnerable area attacks usually intimidate the intruder as shown by this recording. (MPG 4886 kb)

Video 3

The first segment of the video captures a resident–intruder confrontation in which the resident male displays species-typical aggressive behavior. Within seconds, the resident male initiates the attack with a bite to the posterior left flank of the intruder. Following the first attack bite, the intruder escapes and the resident pursues, attempting to nip at his hind flanks. The intruder turns to exhibit an upright defensive posture, but the resident bites several times, pauses briefly to reposition and aims the next bite at the posterior flanks of the intruder. After a short interval, the resident exhibits a sideways threat, which is rapidly followed by the delivery of two more attack bites. The resident walks away from the intruder, marking the end of the aggressive bout. Microanalysis of the resident’s species-typical aggressive behavior revealed a distinct bout of aggression and precise delivery of attack bites to the posterior flanks of the intruder. The second segment of the video captures a confrontation in which the resident male mouse displays alcohol-heightened aggression after rapidly self-administering 1 g/kg of 6 % ethanol solution (w/v). Following a brief latency, the resident delivers an initial bite to the intruder’s right forearm. As the intruder turns to escape, the resident pursues and bites the posterior flank of the intruder twice. The intruder reacts by displaying a prolonged defensive upright posture, and the resident circles the intruder to bite his flank again. Assuming a defensive position on his back, the intruder exposes his abdomen, which the resident bites repeatedly. To avoid attacks to his vulnerable underside, the intruder attempts to escape, which provokes the resident to pursue and bite the intruder’s hind flanks. After cornering the intruder, the resident pins the intruder and continues to bite the intruder’s abdomen and flanks. The intruder persists in his defensive display, and eventually resumes escape behavior. As before, the resident pursues while biting the hind flanks of the intruder. Finally, the resident walks away from the intruder to groom briefly, marking the end of the aggressive bout. From this analysis, it is evident that there are qualitative differences between species-typical and alcohol-heightened aggression. Alcohol-heightened aggression is characterized by prolonged, intense aggressive bouts and targeting attack bites at vulnerable regions. (WMV 8857 kb)

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Miczek, K.A., de Boer, S.F. & Haller, J. Excessive aggression as model of violence: a critical evaluation of current preclinical methods. Psychopharmacology 226, 445–458 (2013). https://doi.org/10.1007/s00213-013-3008-x

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