Larger on the right: Honeybees represent quantities spatially.

Giurfa, Marcout, Hilpert, Thevenoy, and Rugani (PNAS, https://doi.org/10.1073/pnas.22035841192022 ) report the first evidence of spatial representation of quantity in invertebrates. In an exciting and well-controlled series of experiments, the authors present evidence that honeybees, like humans, non-human primates, and birds, represent small quantities on one side of space and large quantities on the other side of space.

Information seeking in western lowland gorillas (Gorilla gorilla gorilla).

Many animals will seek information when they do not know the answer to a problem, suggesting that they monitor their knowledge state. In the classic "tubes task," subjects are presented with a set of opaque tubes and either see (visible trials) or do not see (hidden trials) which tube holds a food reward on a given trial. Chimpanzees, bonobos, orangutans, and human children show information-seeking behavior on this task, looking into the tubes to find the reward more on hidden than on visible trials. However, evidence for information-seeking behavior in gorillas is limited. In Experiment 1, gorillas that were presented with a classic information-seeking tubes task showed performance patterns consistent with metacognitive behavior; they looked down tubes more on hidden than on visible trials, their accuracy on hidden trials on which they looked was higher than on hidden trials on which they did not look, and they primarily employed an appropriate search strategy when looking down the tubes. In Experiment 2, we decreased or increased the amount of effort required to look down the tubes by increasing or decreasing the height of the tubes, respectively. Gorillas were less likely to look in tubes on trials that required high effort, but continued to look more on hidden than on visible trials, indicating that their tendency to look was affected by both knowledge state and effort. Together these results provide strong evidence for logical, controlled information-seeking behavior by gorillas.

Thinking about order: a review of common processing of magnitude and learned orders in animals.

Rich behavioral and neurobiological evidence suggests cognitive and neural overlap in how quantitatively comparable dimensions such as quantity, time, and space are processed in humans and animals. While magnitude domains such as physical magnitude, time, and space represent information that can be quantitatively compared (4 "is half of" 8), they also represent information that can be organized ordinally (1→2→3→4). Recent evidence suggests that the common representations seen across physical magnitude, time, and space domains in humans may be due to their common ordinal features rather than their common quantitative features, as these common representations appear to extend beyond magnitude domains to include learned orders. In this review, we bring together separate lines of research on multiple ordinal domains including magnitude-based and learned orders in animals to explore the extent to which there is support for a common cognitive process underlying ordinal processing. Animals show similarities in performance patterns across natural quantitatively comparable ordered domains (physical magnitude, time, space, dominance) and learned orders (acquired through transitive inference or simultaneous chaining). Additionally, they show transfer and interference across tasks within and between ordinal domains that support the theory of a common ordinal representation across domains. This review provides some support for the development of a unified theory of ordinality and suggests areas for future research to better characterize the extent to which there are commonalities in cognitive processing of ordinal information generally.

ORDINAL PROBIT FUNCTIONAL OUTCOME REGRESSION WITH APPLICATION TO COMPUTER-USE BEHAVIOR IN RHESUS MONKEYS.

Research in functional regression has made great strides in expanding to non-Gaussian functional outcomes, but exploration of ordinal functional outcomes remains limited. Motivated by a study of computer-use behavior in rhesus macaques (Macaca mulatta), we introduce the Ordinal Probit Functional Outcome Regression model (OPFOR). OPFOR models can be fit using one of several basis functions including penalized B-splines, wavelets, and O'Sullivan splines-the last of which typically performs best. Simulation using a variety of underlying covariance patterns shows that the model performs reasonably well in estimation under multiple basis functions with near nominal coverage for joint credible intervals. Finally, in application, we use Bayesian model selection criteria adapted to functional outcome regression to best characterize the relation between several demographic factors of interest and the monkeys' computer use over the course of a year. In comparison with a standard ordinal longitudinal analysis, OPFOR outperforms a cumulative-link mixed-effects model in simulation and provides additional and more nuanced information on the nature of the monkeys' computer-use behavior.

Dominance and social interaction patterns in brown capuchin monkey (Cebus [Sapajus] apella) social networks.

Strong, stable social bonds in primates are characterized by high levels of social affiliation, low levels of aggression, minimal stress, and affiliative reciprocity within the dyad. In relatively well-studied catarrhine monkeys, these bonds tend to form most frequently between kin, animals close in age, and animals close in rank. This results in patterns of affiliation in which kin, similarly aged animals, and like-ranked animals tend to affiliate and patterns of aggression and submission where animals tend to aggress more toward nonkin and closely ranked animals, and submit more toward distantly ranked animals. However, literature on how affiliative and agonistic relationships are organized in platyrrhine primate species like brown capuchin monkeys is limited and conflicting. In this study, we used social network analyses to characterize how age, sex, maternal kinship, and dominance rank relate to the patterns of submissive, aggressive, contact, and grooming interactions in a group of captive brown capuchin monkeys. Like catarrhine monkeys, brown capuchin monkeys showed a steep linear dominance hierarchy, tended to affiliate with kin, similarly aged animals, and like-ranked animals, and tended to aggress more toward nonkin. However, our monkeys showed a pattern of affiliation and grooming down the hierarchy that is inconsistent with grooming up the hierarchy patterns often seen in catarrhine monkey groups, suggesting that brown capuchins do not compete for access to higher ranking social partners. Higher ranking monkeys were most central to the aggression network, and lower ranking monkeys were most central to the submission network. Mid-ranking monkeys were the most central to the contact network, suggesting that they may play an important role in the affiliative cohesion of the group. These results inform our understanding of brown capuchin social behavior specifically, and of how demographic factors relate to social organization in platyrrhine primates generally.

Does cognition differ across species, and how do we know? Lessons from research in transitive inference.

Comparative psychologists study cognition by characterizing the behavior of individual species and explicitly comparing behavior across species. We use the extensive comparative literature on transitive inference (TI) as a case study to evaluate four central methodological questions that continue to be debated in the field of comparative psychology: 1) Are contextual variables sufficient to explain species differences in cognition? 2) Can cognitive performance be accounted for by associative processes alone? 3) Can we determine the cognitive mechanisms by which animals solve tasks? and 4) What is the role of ecologically driven hypotheses in comparative psychology? Although contextual variables and associative processes undeniably influence choice behavior in TI tasks, neither is sufficient to explain all performance. Instead, multiple distinct cognitive mechanisms, including associative processes, logical inference, and spatial representations, can and do result in successful TI performance. TI is not a unitary task solved using a single mechanism; multiple processes are recruited, with their degree of involvement dependent on context, species, and evolutionary pressures. This suggests that rather than asking whether animals possess a certain cognitive ability, research should focus on differences in when and how species employ tools from what is often a reasonably similar cognitive toolbox. We join others who have proposed that a main goal of comparative psychology should be to determine how animals solve cognitive tasks, through minimizing and studying the influence of contextual variables, evaluating the contributions of associative processes, clearly characterizing and testing alternative cognitive mechanisms, and using strong evolutionary hypotheses to guide predictions. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Social monkeys learn more slowly: Social network centrality and age are positively related to learning errors by capuchin monkeys (Cebus [Sapajus] apella).

The cognitive demand on animals to learn, maintain, and remember the complexities of social relationships is theoretically higher for individuals who live more complex social lives. Previous research has suggested that both across and within species, the cognitive ability to flexibly learn and manipulate information may increase with increased social complexity. In this study, we determined the relationship between social complexity and cognitive performance on 2 related tests of general learning: associative learning and reversal learning. Subjects were 16 members of a socially housed group of brown capuchin monkeys (Cebus [Sapajus] apella). A general learning score was extracted from a principal component analysis on learning rate across 5 repetitions of each of the 2 tasks. The complexity of each monkey's social life was characterised by their centrality in the grooming social network of the group. Generalised learning scores were predicted by age and network centrality, but in contrast to predictions, older monkeys and monkeys that were more central to the network made more errors. Future studies focusing on specific cognitive abilities that are theoretically linked to species-specific fitness and behavioural outcomes, rather than broad cognitive categories like learning, will be essential for clarifying the relationship between cognition and social complexity. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Preserved visual memory and relational cognition performance in monkeys with selective hippocampal lesions.

The theory that the hippocampus is critical for visual memory and relational cognition has been challenged by discovery of more spared hippocampal tissue than previously reported in H.M., previously unreported extra-hippocampal damage in developmental amnesiacs, and findings that the hippocampus is unnecessary for object-in-context memory in monkeys. These challenges highlight the need for causal tests of hippocampal function in nonhuman primate models. Here, we tested rhesus monkeys on a battery of cognitive tasks including transitive inference, temporal order memory, shape recall, source memory, and image recognition. Contrary to predictions, we observed no robust impairments in memory or relational cognition either within- or between-groups following hippocampal damage. These results caution against over-generalizing from human correlational studies or rodent experimental studies, compel a new generation of nonhuman primate studies, and indicate that we should reassess the relative contributions of the hippocampus proper compared to other regions in visual memory and relational cognition.

Smaller on the left? Flexible association between space and magnitude in pigeons (Columba livia) and blue jays (Cyanocitta cristata).

Humans and other apes represent magnitudes spatially, demonstrated by their responding faster and more accurately to one side of space when presented with small quantities and to the other side of space when presented with large quantities. This representation is flexible and shows substantial variability between cultural groups in humans and between and within individuals in great apes. In contrast, recent findings suggest that chicks show a spatial representation of magnitude that is highly lateralized and inflexible, implying a qualitatively different underlying representation than in primates. Using methods similar to those used with great apes and humans, we trained adult domestic pigeons (Columba livia) and blue jays (Cyanocitta cristata) to select the smaller (or larger) of two nonadjacent quantity arrays; later, this task was reversed. At test, birds were presented with novel probe pairs consisting of adjacent quantity pairs (e.g., 2 vs. 3). Both species showed robust evidence for a flexible spatial representation of magnitude with considerable individual variability in the orientation of this representation. These results are not consistent with an inflexible, lateralized, left-to-right representation of magnitude in birds, but are consistent with the flexible spatial representation of magnitude observed in apes and humans. We conclude that the tendency to organize quantities spatially may be a fundamental and evolutionarily ancient feature of cognition that is widespread among vertebrates. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

Aggression and social support predict long-term cortisol levels in captive tufted capuchin monkeys (Cebus [Sapajus] apella).

Many nonhuman primates live in complex social groups in which they regularly encounter both social stressors such as aggression and social support such as that provided by long-term affiliative relationships. Repeated exposure to social stressors may result in chronically elevated cortisol levels that can have deleterious physical effects such as impaired immune function, cardiovascular disease, and reduced brain function. In contrast, affiliative social relationships may act as a buffer, dampening the release of cortisol in response to acute and chronic stressors. Understanding how social stressors and social support predict cortisol levels is therefore essential to understanding how social situations relate to health and welfare. We studied this relationship in 16 socially housed captive brown capuchin monkeys (Cebus [Sapajus] apella) by comparing long-term hair cortisol levels with behavioral measures of social stress (dominance rank, rank certainty, and amount of aggression received) and social support (amount of affiliation and centrality in the affiliative social network of the group). Dominance rank, rank certainty, amount of affiliation, and age were not significant predictors of long-term cortisol levels in this population. Instead, long-term cortisol levels were positively related to the amount of aggression received and negatively related to centrality in the affiliative social network of the group. This pattern may be attributed to the species' socially tolerant dominance system and to the availability of social support across the dominance hierarchy.

Influences of demographic, seasonal, and social factors on automated touchscreen computer use by rhesus monkeys (Macaca mulatta) in a large naturalistic group.

Animals housed in naturalistic social groups with access to automated cognitive testing vary in whether and how much they participate in cognitive testing. Understanding how demographic, seasonal, and social factors relate to participation is essential to evaluating the usefulness of these systems for studying cognition and in assessing the data produced. We evaluated how sex, age, reproductive experience, seasonality, and rank related to patterns of participation in a naturalistic group of rhesus monkeys over a 4-year period. Females interacted with the touchscreen systems more than males and were more likely to complete initial training. Age was positively correlated with touchscreen activity through adolescence in females, at which point seasonality and reproductive experience were stronger associates of participation. While monkeys in different rank categories did not differ in how much they interacted with the touchscreen systems, monkeys of different ranks tended not to work at the same times, perhaps reflecting avoidance of high ranking animals by those of lower rank. Automated cognitive testing systems for naturalistic social groups of rhesus monkeys can yield quality cognitive data from individuals of all ages and ranks, but participation biases may make it difficult to study sex differences or seasonal variation in cognition.

Co-operation of long-term and working memory representations in simultaneous chaining by rhesus monkeys (Macaca mulatta).

We studied the memory representations that control execution of action sequences by training rhesus monkeys (Macaca mulatta) to touch sets of five images in a predetermined arbitrary order (simultaneous chaining). In Experiment 1, we found that this training resulted in mental representations of ordinal position rather than learning associative chains, replicating the work of others. We conducted novel analyses of performance on probe tests consisting of two images "derived" from the full five-image lists (i.e., test B, D from list A→B→C→D→E). We found a "first item effect" such that monkeys responded most quickly to images that occurred early in the list in which they had been learned, indicating that monkeys covertly execute known lists mentally until an image on the screen matches the one stored in memory. Monkeys also made an ordinal comparison of the two images presented at test based on long-term memory of positional information, resulting in a "symbolic distance effect." Experiment 2 indicated that ordinal representations were based on absolute, rather than on relative, positional information because subjects did not link two lists into one large list after linking training, unlike what occurs in transitive inference. We further examined the contents of working memory during list execution in Experiments 3 and 4 and found evidence for a prospective, rather than a retrospective, coding of position in the lists. These results indicate that serial expertise in simultaneous chaining results in robust absolute ordinal coding in long-term memory, with rapidly updating prospective coding of position in working memory during list execution.

Impact of stimulus format and reward value on quantity discrimination in capuchin and squirrel monkeys.

Quantity discrimination abilities are seen in a diverse range of species with similarities in performance patterns, suggesting common underlying cognitive mechanisms. However, methodological factors that impact performance make it difficult to draw broad phylogenetic comparisons of numerical cognition across studies. For example, some Old World monkeys selected a higher quantity stimulus more frequently when choosing between inedible (pebbles) than edible (food) stimuli. In Experiment 1 we presented brown capuchin (Cebus [Sapajus] paella) and squirrel monkeys (Saimiri sciureus) with the same two-choice quantity discrimination task in three different stimulus conditions: edible, inedible, and edible replaced (in which choice stimuli were food items that stood in for the same quantity of food items that were given as a reward). Unlike Old World monkeys, capuchins selected the higher quantity stimulus more in the edible condition and squirrel monkeys showed generally poor performance across all stimulus types. Performance patterns suggested that differences in subjective reward value might motivate differences in choice behavior between and within species. In Experiment 2 we manipulated the subjective reinforcement value of the reward by varying reward type and delay to reinforcement and found that delay to reinforcement had no impact on choice behavior, while increasing the value of the reward significantly improved performance by both species. The results of this study indicate that species presented with identical tasks may respond differently to methodological factors such as stimulus and reward types, resulting in significant differences in choice behavior that may lead to spurious suggestions of species differences in cognitive abilities.

Monkeys choose, but do not learn, through exclusion.

Human children will select a novel object from among a group of known objects when presented with a novel object name. This disambiguation by exclusion may facilitate new name-object mappings and may play a role in the rapid word learning shown by young children. Animals including dogs, apes, monkeys, and birds make similar exclusion choices. However, evidence regarding whether children and nonhuman animals learn new associations through choice by exclusion is mixed. In the present study we dissociate choice by exclusion from learning by exclusion in rhesus monkeys using a paired-associate task. In experiment 1, monkeys demonstrated choice by exclusion by choosing a novel comparison image from among known comparison images when presented with a novel sample image. In experiment 2, monkeys failed to benefit from choice by exclusion in learning new sets of paired associates. Monkeys learned new sets of four paired associates by trial and error alone or by a combination of exclusion and trial and error. Despite choosing correctly by exclusion on almost 100% of opportunities, monkeys did not learn any faster by exclusion than by trial and error alone. These results indicate that monkeys chose, but do not learn, through exclusion, highlighting the importance of separately evaluating choice and learning in studies of exclusion in word learning.

Spatial representation of magnitude in gorillas and orangutans.

Humans mentally represent magnitudes spatially; we respond faster to one side of space when processing small quantities and to the other side of space when processing large quantities. We determined whether spatial representation of magnitude is a fundamental feature of primate cognition by testing for such space-magnitude correspondence in gorillas and orangutans. Subjects picked the larger quantity in a pair of dot arrays in one condition, and the smaller in another. Response latencies to the left and right sides of the screen were compared across the magnitude range. Apes showed evidence of spatial representation of magnitude. While all subjects did not adopt the same orientation, apes showed consistent tendencies for spatial representations within individuals and systematically reversed these orientations in response to reversal of the task instruction. Results suggest that spatial representation of magnitude is phylogenetically ancient and that consistency in the orientation of these representations in humans is likely culturally mediated.

Transitive inference of social dominance by human infants.

It is surprising that there are inconsistent findings of transitive inference (TI) in young infants given that non-linguistic species succeed on TI tests. To conclusively test for TI in infants, we developed a task within the social domain, with which infants are known to show sophistication. We familiarized 10- to 13-month-olds (M = 11.53 months) to a video of two dominance interactions between three puppets (bear > elephant; hippo > bear) consistent with a dominance hierarchy (hippo > bear > elephant; where '>' denotes greater dominance). Infants then viewed interactions between the two puppets that had not interacted during familiarization. These interactions were either congruent (hippo > elephant) or incongruent (elephant > hippo) with the inferred hierarchy. Consistent with TI, infants looked longer to incongruent than congruent displays. Control conditions ruled out the possibility that infants' expectations were based on stable behaviors specific to individual puppets rather than their inferred transitive dominance relations. We suggest that TI may be supported by phylogenetically ancient mechanisms of ordinal representation and visuospatial processing that come online early in human development.

Similar stimulus features control visual classification in orangutans and rhesus monkeys.

Many species classify images according to visual attributes. In pigeons, local features may disproportionately control classification, whereas in primates global features may exert greater control. In the absence of explicitly comparative studies, in which different species are tested with the same stimuli under similar conditions, it is not possible to determine how much of the variation in the control of classification is due to species differences and how much is due to differences in the stimuli, training, or testing conditions. We tested rhesus monkeys (Macaca mulatta) and orangutans (Pongo pygmaeus and Pongo abelii) in identical tests in which images were modified to determine which stimulus features controlled classification. Monkeys and orangutans were trained to classify full color images of birds, fish, flowers, and people; they were later given generalization tests in which images were novel, black and white, black and white line drawings, or scrambled. Classification in these primate species was controlled by multiple stimulus attributes, both global and local, and the species behaved similarly.

Effects of spatial training on transitive inference performance in humans and rhesus monkeys.

It is often suggested that transitive inference (TI; if A > B and B > C, then A > C) involves mentally representing overlapping pairs of stimuli in a spatial series. However, there is little direct evidence to unequivocally determine the role of spatial representation in TI. We tested whether humans and rhesus monkeys use spatial representations in TI by training them to organize 7 images in a vertical spatial array. Then, we presented subjects with a TI task using these same images. The implied TI order was either congruent or incongruent with the order of the trained spatial array. Humans in the congruent condition learned premise pairs more quickly, and were faster and more accurate in critical probe tests, suggesting that the spatial arrangement of images learned during spatial training influenced subsequent TI performance. Monkeys first trained in the congruent condition also showed higher test trial accuracy when the spatial and inferred orders were congruent. These results directly support the hypothesis that humans solve TI problems by spatial organization, and suggest that this cognitive mechanism for inference may have ancient evolutionary roots.

Automated cognitive testing of monkeys in social groups yields results comparable to individual laboratory-based testing.

Cognitive abilities likely evolved in response to specific environmental and social challenges and are therefore expected to be specialized for the life history of each species. Specialized cognitive abilities may be most readily engaged under conditions that approximate the natural environment of the species being studied. While naturalistic environments might therefore have advantages over laboratory settings for cognitive research, it is difficult to conduct certain types of cognitive tests in these settings. We implemented methods for automated cognitive testing of monkeys (Macaca mulatta) in large social groups (Field station) and compared the performance to that of laboratory-housed monkeys (Laboratory). The Field station animals shared access to four touch-screen computers in a large naturalistic social group. Each Field station subject had an RFID chip implanted in each arm for computerized identification and individualized assignment of cognitive tests. The Laboratory group was housed and tested in a typical laboratory setting, with individual access to testing computers in their home cages. Monkeys in both groups voluntarily participated at their own pace for food rewards. We evaluated performance in two visual psychophysics tests, a perceptual classification test, a transitive inference test, and a delayed matching-to-sample memory test. Despite the differences in housing, social environment, age, and sex, monkeys in the two groups performed similarly in all tests. Semi-free ranging monkeys living in complex social environments are therefore viable subjects for cognitive testing designed to take advantage of the unique affordances of naturalistic testing environments.

Cognitive mechanisms for transitive inference performance in rhesus monkeys: measuring the influence of associative strength and inferred order.

If Ben is taller than Emily and Emily is taller than Dina, one can infer that Ben is taller than Dina. This process of inferring relations between stimuli based on shared relations with other stimuli is called transitive inference (TI). Many species solve TI tasks in which they learn pairs of overlapping stimulus discriminations (A+B-, B+C-, etc.) and are tested with non-adjacent novel test pairings (BD). When relations between stimuli are determined by reinforcement (A is reinforced when paired with B, B when paired with C), performance can be controlled by the associative values of individual stimuli or by logical inference. In Experiment 1 rhesus monkeys (Macaca mulatta) chose the higher ranked item on non-adjacent test trials after training on a 7-image TI task. In Experiment 2 we measured the associative values of 7 TI images and found that these values did not correlate with choice in TI tests. In Experiment 3 large experimental manipulations of the associative value of images did influence performance in some TI test pairings, but performance on other pairs was consistent with the implied order. In Experiment 4 monkeys linked two previously learned 7-item lists into one 14-item list after training with a single linking pair. Linking cannot be explained by associative values. Associative value can control choice in TI tests in at least some extreme circumstances. Implied order better explains most TI choices in monkeys, and is a more viable mechanism for TI of social dominance, which has been observed in birds and fish.