Seasonal variation in reversal learning reveals greater female cognitive flexibility in African striped mice

Abstract

Cognitive flexibility describes the ability of animals to alter cognitively mediated behaviour in response to changing situational demands, and can vary according to prevailing environemental conditions and individual caracteristics. In the present study, we investigated (1) how learning and reversal learning performance changes between seasons, and (2) how cognitive flexibility is related to sex in a free-living small mammal. We studied 107 African striped mice, Rhabdomys pumilio, in an arid semi-desert, 58 during the hot dry summer with low food availability, and 49 during the cold wet winter with higher food availability. We used an escape box task to test for learning and reversal learning performance. We found that learning and reversal learning efficiency varied seasonally by sex: females tested in summer were faster at solving both learning and reversal tasks than males tested in winter. Performance varied within sex: males tested in winter showed faster learning compared to males tested in summer. During reversal learning, females tested in summer were more efficient and solve the task faster compared to females tested in winter. We suggest that seasonal cognitive performance could be related to sex-specific behavioural characteristics of the species, resulting in adaptation for living in harsh environmental conditions.

Variation in brain volume in nine populations and three taxa of the African striped mouse Rhabdomys

“…Given the more seasonally variable environment of the grasslands than the Succulent Karoo and Fynbos, under the Cognitive Buffer Hypothesis, it would be expected that larger relative total volumes would occur in R. dilectus , but this was not the case (but see Section 4.2). The presence of behavioural flexibility in R. pumilio due to the variability of territories and resource availability (Rochais et al, 2021; Schoepf & Schradin, 2012) would support the Cognitive Buffer Hypothesis. However, behavioural flexibility has been studied only in the Succulent Karoo population and it is unknown whether fynbos R. pumilio are similarly capable of flexible social organisation.…”

“…Interestingly, R. pumilio females from the Succulent Karoo had larger relative total endocranial volumes and anterior cerebrum volumes than male conspecifics, and succulent karoo males had relative total endocranial volumes similar to the relative endocranial volumes in R. dilectus . Female R. pumilio tested in the summer (when food availability is low) outperformed females tested in winter in a reversal‐learning task under harsh summer conditions, suggesting cognitive flexibility due to environmental variability and the unpredictability of resources (Rochais et al, 2021). In contrast, males tested in the learning and reversal learning task learned more quickly and made fewer errors than males tested in the summer but took longer to complete the task than females did in the summer (Rochais et al, 2021).…”

“…Female R. pumilio tested in the summer (when food availability is low) outperformed females tested in winter in a reversal‐learning task under harsh summer conditions, suggesting cognitive flexibility due to environmental variability and the unpredictability of resources (Rochais et al, 2021). In contrast, males tested in the learning and reversal learning task learned more quickly and made fewer errors than males tested in the summer but took longer to complete the task than females did in the summer (Rochais et al, 2021). Similarly, female rats show greater flexibility in a reversal‐learning task whereas males showed behavioural persistence linked to the influence of testosterone on regions related to memory (Valencia et al, 1986).…”

“…The presence of behavioural flexibility in R. pumilio due to the variability of territories and resource availability (Rochais et al, 2021; Additionally, it is important to recognise that even should other R. pumilio populations have the capacity for social flexibility, the nature of this flexibility (i.e., the influence of social organisation) would make it difficult to separate the influence of sociality from the influence of the variability of the environment.…”

Cognitive performance is linked to survival in free-living African striped mice

“…Furthermore, attention, spatial learning and memory, problem-solving and reversal learning varied seasonally by sex: in summer, males showed faster attention towards a predator stimulus, solved more novel problems, but made more errors and took longer in a spatial learning and memory tasks than males tested during winter [44,45]. By contrast, females tested in summer solved a reversal learning task faster but their attention, problem-solving and spatial learning and memory performance did not differ seasonally [44–46]. Female survival was correlated with faster attention to a predator stimulus, whereas male survival was correlated with greater spatial memory [47].…”