- Proceedings. Biological sciences / The Royal Society
- Published over 3 years ago
The importance of exercise for health and neurogenesis is becoming increasingly clear. Wheel running is often used in the laboratory for triggering enhanced activity levels, despite the common objection that this behaviour is an artefact of captivity and merely signifies neurosis or stereotypy. If wheel running is indeed caused by captive housing, wild mice are not expected to use a running wheel in nature. This however, to our knowledge, has never been tested. Here, we show that when running wheels are placed in nature, they are frequently used by wild mice, also when no extrinsic reward is provided. Bout lengths of running wheel behaviour in the wild match those for captive mice. This finding falsifies one criterion for stereotypic behaviour, and suggests that running wheel activity is an elective behaviour. In a time when lifestyle in general and lack of exercise in particular are a major cause of disease in the modern world, research into physical activity is of utmost importance. Our findings may help alleviate the main concern regarding the use of running wheels in research on exercise.
Animals housed in impoverished cages are often labelled ‘bored’. They have also been called ‘apathetic’ or ‘depressed’, particularly when profoundly inactive. However, these terms are rarely operationally defined and validated. As a negative state caused by under-stimulation, boredom should increase interest in stimuli of all kinds. Apathy (lack of interest), by contrast, should manifest as decreased interest in all stimuli, while anhedonia (loss of pleasure, a depressive symptom) should specifically decrease interest in normally rewarding stimuli. We tested the hypotheses that mink, a model carnivore, experience more boredom, depression-like apathy, or anhedonia in non-enriched (NE) cages than in complex, enriched (E) cages. We exposed 29 subjects (13 E, 16 NE) to ten stimuli categorized a priori as aversive (e.g. air puffs), rewarding (e.g. evoking chasing) or ambiguous/neutral (e.g. candles). Interest in stimuli was assessed via latencies to contact, contact durations, and durations oriented to stimuli. NE mink contacted all stimuli faster (P = 0.003) than E mink, and spent longer oriented to/in contact with them, albeit only significantly so for ambiguous ones (treatment*type P<0.013). With stimulus category removed from statistical models, interest in all stimuli was consistently higher among NE mink (P<0.0001 for all measures). NE mink also consumed more food rewards (P = 0.037). Finally, we investigated whether lying down while awake and stereotypic behaviour (both increased by NE housing) predicted these responses. Lying awake positively co-varied with certain measures of increased exploration. In contrast, stereotypic 'scrabbling' or locomotion (e.g. pacing) did not. Overall, NE mink showed no evidence of apathy or depression, but instead a heightened investigation of diverse stimuli consistent with boredom. This state was potentially indicated by spending much time lying still but awake (although this result requires replication). Boredom can thus be operationalized and assessed empirically in non-human animals. It can also be reduced by environmental enrichment.
Wild carnivores in zoos, conservation breeding centres, and farms commonly live in relatively small, unstimulating enclosures. Under these captive conditions, in a range of species including giant pandas, black-footed ferrets, and European mink, male reproductive abilities are often poor. Such problems have long been hypothesized to be caused by these animals' housing conditions. We show for the first time that rearing under welfare-improving (i.e., highly valued and stress-reducing) environmental enrichments enhances male carnivores' copulatory performance: in mate choice competitions, enriched male American mink (Neovison vison) mated more often than non-enriched males. We screened for several potential mediators of this effect. First was physiological stress and its impact on reproductive physiology; second, stress-mediated changes in morphology and variables related to immunocompetence that could influence male attractiveness; and third, behavioural changes likely to affect social competence, particularly autistic-like excessive routine and repetition (‘perseveration’) as is reflected in the stereotypies common in captive animals. Consistent with physiological stress, excreted steroid metabolites revealed that non-enriched males had higher cortisol levels and lower androgen levels than enriched conspecifics. Their os penises (bacula) also tended to be less developed. Consistent with reduced attractiveness, non-enriched males were lighter, with comparatively small spleens and a trend to greater fluctuating asymmetry. Consistent with impaired social competence, non-enriched males performed more stereotypic behaviour (e.g., pacing) in their home cages. Of all these effects, the only significant predictor of copulation number was stereotypy (a trend suggesting that low bodyweights may also be influential): highly stereotypic males gained the fewest copulations. The neurophysiological changes underlying stereotypy thus handicap males sexually. We hypothesise that such males are abnormally perseverative when interacting with females. Investigating similar problems in other taxa would be worthwhile, since many vertebrates, wild and domestic, live in conditions that cause stereotypic behaviour and/or impair neurological development.
Intensive behavioral intervention for young children diagnosed with autism can produce large gains in social, cognitive, and language development. Although several studies have identified behaviors that are possible indicators of best outcome, changes in performance are typically measured using norm-referenced standardized scores referencing overall functioning level rather than via repeated observational measures of autism-specific deficits (i.e., social behavior). In the current study, 83 children with autism (CWA), aged 1, 2 and 3 years, and 58 same-aged typically developing children (TDC) were directly observed in the areas of cognitive skills, joint attention (JA), play, and stereotypic behavior using a measure called the Early Skills Assessment Tool (ESAT; MacDonald et al., 2006). CWA were assessed at entry into an EIBI program and again after 1 year of treatment. Changes in performance were compared pre- and post-treatment as well as to the normative data by age. Results indicate significant gains on the ESAT across all age groups with the greatest gains seen in the children who entered treatment prior to their second birthday. Increases were seen on direct measures of JA, play, imitation and language while decreases were seen in stereotypy regardless of level of performance at entry into EIBI. The ESAT, a direct measurement tool, served as a sensitive tool to measure changes in autism symptomatology following EIBI treatment.
Diverse motivational triggers, including diet, elicit stereotypic behavior. We investigated whether diets comprised of different protein levels but similar levels of energy were associated with the occurrence of locomotor stereotypies in the striped mouse Rhabdomys dilectus chakae. In a first experiment, 20 stereotypic and 20 non-stereotypic (10 subjects per sex and per group) juvenile (40 days old) subjects were placed on baseline (BP), high (HP) or low protein (LP) diet treatments (120 subjects in total). All subjects initially identified as stereotypic displayed stereotypic behavior in the BP and HP treatments on Days 60-63 and Days 80-83 compared to 35% and 12.5% of LP subjects, respectively. Moreover, LP subjects displayed lower levels of activity and stereotypic behavior than BP and HP subjects. Those identified as non-stereotypic never displayed stereotypy. In a second experiment, 48 individuals, bred and reared on LP and whose parents were stereotypic, were assigned to either HP (13 males, 12 females) or LP (12 males, 11 females) treatments at 50 days of age for 30 days. Stereotypy was three times less likely to occur in the LP than the HP treatment, and activity was greater in LP-HP individuals than LP-LP individuals. In both experiments, LP individuals had the lowest body mass. Striped mice adjusted their behaviors in response to dietary protein levels. Protein deficiency reduced activity and stereotypic behavior and prevalence, possibly related to an energy or neurological deficit.
Captive bears are housed in environments that differ greatly from their natural habitat, restricting their ability to perform normal species-specific behaviours. This may be detrimental to welfare, with disabled individuals at particular risk. The effect of physical disability on behaviour and enclosure utilisation was assessed in 12 adult Malayan sun bears (Helarctos malayanus) using 10minute interval scan sampling. Amputees spent less time performing locomotor behaviours than able-bodied bears, used their enclosures less evenly, but did not exhibit obvious stereotypies. This was possibly due to the increased energy demands of locomotion, or residual pain in amputated limbs. Amputees spent less time grooming, but did not differ in time spent climbing compared with non-amputees. Partially sighted bears did not differ from able-bodied controls in enclosure use or behaviour. Age was positively correlated with stereotypical behaviour, and negatively correlated with maintenance and resting. Medication use was associated with more resting and grooming, and reduced stereotypy. The findings suggest that enclosures for amputees can be smaller than those for able-bodied bears, but should still contain a variety of climbing structures. Partially sighted bears fare well in enclosures designed for able-bodied bears, not requiring any special provision.
Stereotypic behaviours are commonly observed in captive animals and are usually interpreted as a sign of poor welfare. Stereotypies have also been linked with brain abnormalities. However, stereotypies are a heterogeneous class of behaviours and mounting evidence indicates that different stereotypies can have different causes, and can be linked to different affective states. As a consequence, the implications of a specific stereotypy in a specific species cannot be safely inferred from evidence on other stereotypies or species. Here we review what is known about pacing behaviour in laboratory rhesus macaques, a common stereotypy in this species. Our review highlights the current lack of understanding of the causal factors underlying pacing behaviour. According to current knowledge, the welfare of pacing macaques could be either better, worse or equivalent to that of non-pacing individuals. It is also unclear whether pacing results from brain abnormalities. Since rhesus macaques are widely used as a model of healthy humans in neuroscience research, determining if pacing behaviour reflects an abnormal brain and/or poor welfare is urgent.
Functional (psychogenic) movement disorders (FMDs) may present with a broad spectrum of phenomenology including stereotypic movements. We aimed to characterize the phenomenology of functional stereotypies and compare these features with those observed in 65 patients with tardive dyskinesia (TD). From a cohort of 184 patients with FMDs, we identified 19 (10.3%) with functional stereotypies (FS). There were 15 women and 4 men, with a mean age at onset of 38.6 ± 17.4 years. Among the patients with FS, there were 9 (47%) with orolingual dyskinesia/stereotypy, 9 (47%) with limb stereotypies, 6 (32%) with trunk stereotypies, and 2 (11%) with respiratory dyskinesia as part of orofacial-laryngeal-trunk stereotypy. These patients showed signs commonly seen in FMDs such as sudden onset (84%), prominent distractibility (58%), and periods of unexplained improvement (84%) that were not reported in patients with TD. Besides a much lower frequency of exposure to potential offending drugs, patients with FS differed from those with classic TD by a younger age at onset, lack of self-biting, uncommon chewing movements, more frequent lingual movements without mouth dyskinesia, and associated functional tremor and abnormal speech. Lack of self-biting showed the highest sensitivity (1.0) and abnormal speech showed the highest specificity (0.9) for the diagnosis of functional orolingual dyskinesia. FS represent part of the clinical spectrum of FMDs. Clinical and demographic features are helpful in distinguishing patients with FS from those with TD.
Stereotypies are commonly observed in zoo animals, and it is necessary to better understand whether ambient environmental factors contribute to stereotypy and how to affect animal welfare in zoo settings. This study investigated the relationships between stereotypic behaviors and environmental factors including ambient temperatures, humidity, light intensity, sound intensity and number of visitors. Seven giant pandas were observed in three indoor enclosures and three outdoor enclosures. Environmental factors were measured for both indoor and outdoor enclosures and the effect they had on stereotypical behaviors was investigated. Our research found that light intensity significantly correlated with all stereotypies behaviors. Higher environmental temperature reduced the duration of pacing but increased the frequency of pacing, the duration and frequency of door-directed, meanwhile the duration of head-toss. However, we found no noticeable effect of humidity on stereotypic behaviors except for the frequency of head-toss. We also found that sound intensity was not correlated with stereotypies. Finally, the growth of visitors was negatively associated with the duration of door-directed. These results demonstrated that various environmental factors can have significant effects on stereotypic behaviors causing the expression of various stereotypies. Thus, stereotypies in zoo animals may not simply represent suboptimal welfare, but rather might be adopted as a means of coping with an aversive environment.
Beneficial effects of voluntary wheel running on hippocampal neurogenesis, morphology and hippocampal-dependent behavior have widely been studied in rodents, but also serious side effects and similarities to stereotypy have been reported. Some mouse strains run excessively when equipped with running wheels, complicating the comparability to human exercise regimes. Here, we investigated how exercise restriction to 6h/day affects hippocampal morphology and metabolism, stereotypic and basal behaviors, as well as the endocannabinoid system in wheel running C57BL/6 mice; the strain most commonly used for behavioral analyses and psychiatric disease models. Restricted and unrestricted wheel running had similar effects on immature hippocampal neuron numbers, thermoregulatory nest building and basal home-cage behaviors. Surprisingly, hippocampal gray matter volume, assessed with magnetic resonance (MR) imaging at 9.4 Tesla, was only increased in unrestricted but not in restricted runners. Moreover, unrestricted runners showed less stereotypic behavior than restricted runners did. However, after blockage of running wheels for 24h stereotypic behavior also increased in unrestricted runners, arguing against a long-term effect of wheel running on stereotypic behavior. Stereotypic behaviors correlated with frontal glutamate and glucose levels assessed by (1)H-MR spectroscopy. While acute running increased plasma levels of the endocannabinoid anandamide in former studies in mice and humans, we found an inverse correlation of anandamide with the daily running distance after long-term running. In conclusion, although there are some diverging effects of restricted and unrestricted running on brain and behavior, restricted running does not per se seem to be a better animal model for aerobic exercise in mice.