Age-Related Changes in Chimpanzee (Pan troglodytes) Cognition: Cross-Sectional and Longitudinal Analyses

Abstract

0Chimpanzees are the species most closely related to humans yet age-related changes in brain and 3 1 cognition remain poorly understood. The lack of studies on age-related changes in cognition in 3 2 chimpanzees is particularly unfortunate in light of the recent evidence demonstrating that this 3 3 species naturally develops Alzheimer's disease (AD) neuropathology. Here, we tested 213 3 4 young, middle-aged, and elderly chimpanzees on the Primate Cognitive Test Battery (PCTB), a 3 5 set of 13 tasks that assess physical and social cognition in nonhuman primates. A subset of these 3 6 chimpanzees (n=146) were tested a second time on a portion of the PCTB tasks as a means of 3 7 evaluating longitudinal changes in cognition. Cross-sectional analyses revealed a significant 3 8 quadratic association between age and cognition with younger and older chimpanzees 3 9 performing more poorly than middle-aged individuals. Longitudinal analyses showed that, while 4 0 young chimpanzees' performance improved from test 1 to test 2, middle-aged and elderly 4 1 chimpanzees' performance showed significant decline over time. The collective data show that 4 2 chimpanzees, like other nonhuman primates, show age-related decline in cognition. Further 4 3 investigations into whether the observed cognitive decline is associated with AD pathologies in 4 4 chimpanzees would be invaluable in understanding the comparative biology of aging and 4 5 neuropathology in primates. 4 6 4 7

Nonhuman primates at the intersection of aging biology, chronic disease, and health: An introduction to the American Journal of Primatology Special Issue on aging, cognitive decline, and neuropathology in nonhuman primates

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Age‐ and cognition‐related differences in the gray matter volume of the chimpanzee brain (Pan troglodytes): A voxel‐based morphometry and conjunction analysis

“…Briefly, the tasks included spatial memory, object permanence, rotation, transposition, relative numbers, causality noise, and causality visual (all measuring physical cognition), and initiation of joint attention, attentional state, and gaze following/response to joint attention (all measuring social cognition). As reported in Hopkins et al (2020), the outcome measures for each task were converted to standardized z‐scores (separately for each colony). The z‐scores were then averaged across the 12 measures for each subject to create a unit weighted average (UWA) score that reflected their overall performance, or “g” (Woodley et al, 2015).…”

“…For a subsample of these chimpanzees, we have obtained a measure of general intelligence, “g,” using the Primate Cognition Test Battery (PCTB), a 13‐item test that assesses different dimensions of social and physical cognition in nonhuman primates (Herrmann et al, 2007; Herrmann, Hare, et al, 2010; Herrmann, Hernandez‐Lloreda, et al, 2010; Hopkins et al, 2014; Russell et al, 2011; Schmitt et al, 2011). In addition, Hopkins et al (2020) recently showed that the overall PCTB performance score, or “g,” showed a quadratic association with age (Figure 2); thus, younger and elderly chimpanzees performed more poorly than middle‐aged individuals.…”

“…Therefore, there may be health, management, and welfare challenges for aging chimpanzee populations currently residing in sanctuaries that might benefit from a better understanding of the factors that foster healthy aging. Indeed, consistent with findings in other nonhuman primate species (Darusman, Call, et al, 2014; Darusman, Pandelaki, et al, 2014; Herndon et al, 1997; Joly et al, 2014; Lacreuse et al, 2014, 2020; Lai et al, 1995; Picq, 2007; Rapp & Amaral, 1989; Workman et al, 2019), cross‐sectional and longitudinal data indicate that aged chimpanzees show a moderate loss in cognitive and motor functions compared with younger conspecifics (Hopkins et al, 2015, 2019, 2020; Lacreuse et al, 2014, 2018). The extent to which age‐related changes in cognition observed in aged chimpanzees are attributable to “normal” aging or to neuropathology remains unknown, but the cognitive data would certainly suggest that neurobiological changes should be evident in aging chimpanzees.…”

The marmoset as an important primate model for longitudinal studies of neurocognitive aging

“…Nonhuman primates (NHP) are arguably the best animal models of human cognitive aging due to their phylogenetic proximity and overlap with humans in many aspects of brain function and behavior (Baxter, 2001; Emery Thompson et al, 2020; Hara et al, 2012; Herndon et al, 1997; Lacreuse & Herndon, 2009; Voytko & Tinkler, 2004). To date, several NHP species have been used as models for human cognitive aging (Shively et al, this issue), but longitudinal studies remain remarkably rare (Hopkins et al, 2020; Lacreuse et al, 2014; Pifferi & Aujard, 2019; Suomi et al, 1996). A major challenge to longitudinal approaches in NHPs is their long lifespan; our closest great ape relatives, the chimpanzees, have a life expectancy in captivity of 28.3 years at birth, which increases to 34.6 for animals who reach 1 year of age, with an estimated maximum lifespan of 74 years (Havercamp et al, 2019).…”