Anim Cogn DOI 10.1007/s10071-012-0585-8 ORIGINAL PAPER Automated cognitive testing of monkeys in social groups yields results comparable to individual laboratory-based testing Regina Paxton Gazes • Emily Kathryn Brown • Benjamin M. Basile • Robert R. Hampton Received: 8 August 2012 / Revised: 26 November 2012 / Accepted: 30 November 2012 Ó Springer-Verlag Berlin Heidelberg 2012 Abstract Cognitive abilities likely evolved in response in housing, social environment, age, and sex, monkeys in to specific environmental and social challenges and are the two groups performed similarly in all tests. Semi-free therefore expected to be specialized for the life history of ranging monkeys living in complex social environments each species. Specialized cognitive abilities may be most are therefore viable subjects for cognitive testing designed readily engaged under conditions that approximate the to take advantage of the unique affordances of naturalistic natural environment of the species being studied. While testing environments. naturalistic environments might therefore have advantages over laboratory settings for cognitive research, it is diffi- Keywords Transitive inference Á Memory Á Classification Á cult to conduct certain types of cognitive tests in these Psychophysics Á Rhesus macaque Á Social housing Á RFID settings. We implemented methods for automated cogni- tive testing of monkeys (Macaca mulatta) in large social groups (Field station) and compared the performance to Many animals live complicated lives. They may spend that of laboratory-housed monkeys (Laboratory). The their days foraging, hunting, avoiding predators, social- Field station animals shared access to four touch-screen izing, fighting, mating, migrating, defending territories, or computers in a large naturalistic social group. Each Field caring for offspring. Cognitive abilities have likely station subject had an RFID chip implanted in each arm evolved in response to specific environmental and social for computerized identification and individualized challenges and are therefore expected to be specialized for assignment of cognitive tests. The Laboratory group was each species’ life history (Shettleworth 2009). Specialized housed and tested in a typical laboratory setting, with cognitive abilities may be most readily engaged and individual access to testing computers in their home measured under conditions that approximate critical cages. Monkeys in both groups voluntarily participated at aspects of the natural environment of a given species. their own pace for food rewards. We evaluated perfor- Most studies of cognition are conducted in laboratories, mance in two visual psychophysics tests, a perceptual devoid of many of the social and physical challenges classification test, a transitive inference test, and a delayed present in nature. Laboratory conditions afford excellent matching-to-sample memory test. Despite the differences control over developmental histories and testing condi- tions, facilitating studies of processes such as learning that may be more difficult or impossible to document under natural conditions. However, laboratory environments & R. P. Gazes ( ) often limit exposure to natural cognitive demands and Zoo Atlanta, 800 Cherokee Avenue, Atlanta, GA 30315, USA may deprive subjects of experiences necessary for normal e-mail: [email protected] cognitive development (Rommeck et al. 2011). Animals raised in more complex and natural physical and social R. P. Gazes Á E. K. Brown Á B. M. Basile Á R. R. Hampton conditions may therefore exhibit a more developed range Department of Psychology and Yerkes National Primate Research Center, Emory University, 954 Gatewood Road, of cognitive abilities and behaviors (Gersick et al. 2012; Atlanta, GA 30322, USA White et al. 2010, 2012). 123 Anim Cogn Creative field experiments have been successfully used 1999). These factors have the potential to impact the to explore complex cognitive process such as communi- acquisition and validity of cognitive data. cation (Biben and Bernhards 1994; Windfelder 2001; To assess the validity of data gathered from monkeys Zuberbuhler et al. 1999), individual recognition (Cheney housed in complex social environments, we compared and Seyfarth 1982; Fischer 2004), social cognition learning and performance on four cognitive tasks between (Bergman et al. 2003; Cheney and Seyfarth 1999), transi- monkeys living in a laboratory setting and monkeys living tive inference (Weiß et al. 2010), and memory (Henderson in a large, naturalistic social group. We used four tasks et al. 2001). However, the ability to conduct field studies from core areas of cognitive research: psychophysical and can be limited by difficulties controlling the location of perceptual classification tasks to assess visual perceptual subjects, their experience with particular stimuli, attrition, function, a transitive inference test to assess complex and other factors such as lighting, noise, and the presence cognitive function, and a delayed matching-to-sample task of predators or other distractions. Studies of learning, in to assess memory performance. particular, are difficult to conduct in natural settings because inferences about learning require comprehensive documentation and control of subjects’ experience. It Subjects and apparatus would therefore be advantageous to develop study settings that provide the benefits of complex group living while Subjects were rhesus macaque monkeys (Macaca mulatta) preserving much of the accessibility and experimental housed at the Yerkes National Primate Research Center in control afforded by standard laboratory settings. Atlanta, GA and Lawrenceville, GA. All procedures were Technological advances in radio frequency identification approved by the Institutional Animal Care and Use Com- (RFID) and computer technology have made automated mittee of Emory University and were in compliance with cognitive testing of primates living in complex environments National Institutes of Health guidelines for the care and use possible. Andrews and Rosenblum (1994), Wallen (Hasset of laboratory animals. Subjects were housed and tested in et al. 2007), and Fagot and Paleressompoulle 2009 have one of two environments: Laboratory and Field station. created cognitive testing systems that use RFID chips to identify individual monkeys as they complete computerized Laboratory subjects and apparatus motor, perceptual, and cognitive tasks. Monkeys living in small groups have been found to perform motor and cogni- Twenty-four laboratory-housed monkeys, aged 4–8 years, tive tasks (motor: Andrews and Rosenblum 1994; visual participated in this study, six in each of the four experi- search: Barbet and Fagot 2011; Bonte et al. 2011; Fagot and ments. All Laboratory subjects were adult male rhesus Bonte 2010; working memory: Fagot and De Lillo 2011; monkeys who had been raised by their biological mothers complex matching: Fagot and Paleressompoulle 2009; in a large social group until approximately 2.5 years of age. orthographic processing: Grainger et al. 2012), indicating the Whenever possible, monkeys were pair-housed, and all feasibility of this method of testing. monkeys received enrichment consisting of hard rubber However, no studies have compared learning and per- toys, puzzle feeders, foraging devices, and destructible formance between monkeys living in complex naturalistic items. All monkeys were kept on a 12:12-h light/dark cycle environments and monkeys living in traditional laboratory with light onset at 7:00 a.m. Animals received a full ration environments. Performance might differ between these of food daily, supplemented with fruits and vegetables, and groups of monkeys for either central or peripheral reasons. ad libitum access to water. All subjects had extensive For example, semi-natural environments may foster superior histories with computerized cognitive testing (e.g., Adachi cognitive development, leading to differences in central et al. 2009; Basile and Hampton 2010, 2011; Paxton et al. cognitive capacities and thus performance. Additionally 2010; Templer and Hampton 2012). ad libitum testing may lead to improved learning compared Laboratory testing occurred in the subjects’ home cages. to more restricted testing schedules (Fagot and Thompson Computerized touch-screen test systems, each consisting of 2011). By contrast, differences in housing conditions may a 15-inch LCD color monitor running at a resolution of affect performance but not central cognitive capacities, due 1,024 9 768 pixels, stereo speakers, two automated food to differences in the frequency of distractions, motivation to dispensers (Med Associates Inc. St. Albans, VT), and two participate in testing, and availability of alternative activi- food cups below the screen, were attached to the front of ties. Specifically, monkeys in complex environments have each monkey’s cage (Fig. 1). Computer screens were many behavioral options, may be distracted by other indi- locked to the front of each monkey’s cage and the door was viduals, are subject to changing weather and lighting con- raised, giving subjects full visual and tactile access to the ditions, and access to testing equipment may be limited by screen during testing. Correct responses were rewarded competition and dominance (Drea 1998; Drea and Wallen with nutritionally balanced fruit-flavored pellets on a 123 Anim Cogn young infants). Monkeys lived primarily outdoors in a 30 9 30 m enclosure with access to a temperature-mod- erated indoor housing area. Food and water were available