Environmental enrichment has been widely studied in rodents, but there is no consensus on what enrichment should look like or what it should achieve. Inconsistent use of the term “enrichment” creates challenges in drawing conclusions about the quality of an environment, which may slow housing improvements for laboratory animals. Many review articles have addressed environmental enrichment for laboratory rats and mice (Rattus norvegicus and Mus musculus). We conducted a metareview of 29 review articles to assess how enrichment has been defined and what are commonly described as its goals or requirements. Recommendations from each article were summarised to illustrate the conditions generally considered suitable for laboratory rodents. While there is no consensus on alternative terminology, many articles acknowledged that the blanket use of the terms “enriched” and “enrichment” should be avoided. Environmental enrichment was most often conceptualised as a method to increase natural behaviour and improve animal welfare. Authors also commonly outlined perceived risks and requirements of environmental enrichment. We discuss these perceptions, make suggestions for future research, and advocate for the adoption of more specific and value-neutral terminology.
Rats (Rattus norvegicus) bred for research are typically confined with their litters until weaning, but will spend time away from pups when given the opportunity. We aimed to assess how dam welfare is affected by the ability to escape from their pups. Rat dams (n = 16) were housed in cages either with or without an elevated loft. We measured time dams spent in lofts, time spent nursing, and affective states using elevated plus maze and anticipatory behavior testing. We predicted that 1) dams housed with lofts would use them increasingly as pups aged, 2) dams without a loft would spend more time passively nursing (i.e. initiated by pups rather than the dam) and more total time nursing as pups aged, and 3) dams housed with lofts would show evidence of a more positive affective state. Dams housed with lofts spent more time in the loft with increasing pup age; dams spent on average (mean ± SE) 27 ± 5% of their time in the loft when pups were 1 wk old, increasing to 52 ± 5% of their time at 3 wks. When pups were 3 wks old, dams with lofts spent less time passively nursing (10 ± 2% of total time, compared to 27 ± 4% for dams without a loft) and less time nursing overall (36 ± 4% of time versus 59 ± 2% for dams without a loft). Rats without loft access showed increased anticipatory behavior potentially indicative of negative affective state (24.5±1.8 behaviors per minute in wk 3 compared to 18.8±1.0 in wk 1). These findings indicate that rat dams in laboratories choose to spend time away from their pups when provided the opportunity, particularly later in lactation; an inability to do so is associated with increased passive nursing and negative affect.
Carbon dioxide (CO2) is commonly used to kill laboratory rats. Rats find CO2 aversive and aversion varies between individuals, indicating that rats vary in CO2 sensitivity. Healthy humans experience feelings of anxiety at concentrations similar to those avoided by rats, and these feelings are diminished by the administration of benzodiazepines. Our aim was to assess the effects of the benzodiazepine midazolam on individual thresholds of rat aversion to CO2. Six female Sprague Dawley rats were repeatedly exposed to CO2 gradual-fill in approach-avoidance testing. The first three exposures were to a control-treatment followed by three exposures to midazolam (0.375 mg/kg). Within each treatment aversion to CO2 was not affected by exposure number; however, tolerance increased from an average of 10.7% CO2 avoided during control sessions, to 15.5% CO2 avoided when treated with midazolam. These results indicate that rats experience anxiety when exposed to CO2, and that variation in rat CO2 sensitivity is driven by individual differences in the onset of these feelings of anxiety. No rat tolerated CO2 concentrations required to induce loss of consciousness.
Laboratory mice are typically housed in “shoebox" cages that limit the expression of natural behaviours. Temporary access to more complex environments (playpens) may improve their welfare. We aimed to assess if access to playpens is rewarding for conventionally-housed mice and to document mouse behaviour during playpen access. Female C57BL/6J, BALB/cJ, and DBA/2J mice were provided temporary access to a large enriched playpen three times per week; control mice remained in their home cages. We measured latency to enter playpens and anticipatory behaviour to determine if access was rewarding, and recorded mouse behaviour during playpen sessions. Over time, playpen mice entered the playpen more quickly; latency declined from 168 ± 22 to 13 ± 2 s over the 14-d trial. As expected, playpen mice showed an increase in anticipatory behaviour before playpen access (mean ± SE = 19.7 ± 2.6 behavioural transitions), while control mice showed no change in anticipatory behaviour relative to baseline values (2.4 ± 1.6 transitions). Mice in the playpen performed more ambulatory behaviours than control mice who remained in home cages (21.5 ± 0.7 vs 6.9 ± 1.1 observations of 25 total observations). We conclude that conventionally-housed mice find voluntary playpen access rewarding, and suggest this as a useful option for providing laboratory mice with access to more complex environments.
Feelings of fear, anxiety, dyspnea and panic when inhaling carbon dioxide (CO2) are variable among humans, in part due to differences in CO2 sensitivity. Rat aversion to CO2 consistently varies between individuals; this variation in aversion may reflect CO2 sensitivity, but other personality traits could also account for individual differences in aversion. The aims of this study were to 1) assess the stability of individual differences in rat aversion to CO2, 2) determine if individual differences in sweet reward motivation are associated with variation in aversion to CO2, and 3) assess whether variation in aversion to CO2 is related to individual differences in motivation to approach gains (promotion focus) or maintain safety (prevention focus). Twelve female Sprague Dawley rats were exposed multiple times at three different ages (3, 9 and 16 months old) to CO2 in approach-avoidance testing to assess motivation to avoid CO2 against motivation to gain sweet rewards. Rats were also tested for motivation to find hidden sweet rewards, and for their motivation to approach rewards or darkness. Tolerance to CO2 increased with repeated exposures and was higher at older ages. Individual differences in aversion to CO2 were highly repeatable but unrelated to motivation for sweet rewards or the strength of promotion and prevention focus. These results indicate that individual differences in aversion to CO2 reflect variation in CO2 sensitivity.
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