Spatial concepts of number, size, and time in an indigenous culture.

In industrialized groups, adults implicitly map numbers, time, and size onto space according to cultural practices like reading and counting (e.g., from left to right). Here, we tested the mental mappings of the Tsimane', an indigenous population with few such cultural practices. Tsimane' adults spatially arranged number, size, and time stimuli according to their relative magnitudes but showed no directional bias for any domain on any spatial axis; different mappings went in different directions, even in the same participant. These findings challenge claims that people have an innate left-to-right mapping of numbers and that these mappings arise from a domain-general magnitude system. Rather, the direction-specific mappings found in industrialized cultures may originate from direction-agnostic mappings that reflect the correlational structure of the natural world.

Reasoning Through the Disjunctive Syllogism in Monkeys.

The capacity for logical inference is a critical aspect of human learning, reasoning, and decision-making. One important logical inference is the disjunctive syllogism: given A or B, if not A, then B. Although the explicit formation of this logic requires symbolic thought, previous work has shown that nonhuman animals are capable of reasoning by exclusion, one aspect of the disjunctive syllogism (e.g., not A = avoid empty). However, it is unknown whether nonhuman animals are capable of the deductive aspects of a disjunctive syllogism (the dependent relation between A and B and the inference that "if not A, then B" must be true). Here, we used a food-choice task to test whether monkeys can reason through an entire disjunctive syllogism. Our results show that monkeys do have this capacity. Therefore, the capacity is not unique to humans and does not require language.

Recursive sequence generation in monkeys, children, U.S. adults, and native Amazonians.

The question of what computational capacities, if any, differ between humans and nonhuman animals has been at the core of foundational debates in cognitive psychology, anthropology, linguistics, and animal behavior. The capacity to form nested hierarchical representations is hypothesized to be essential to uniquely human thought, but its origins in evolution, development, and culture are controversial. We used a nonlinguistic sequence generation task to test whether subjects generalize sequential groupings of items to a center-embedded, recursive structure. Children (3 to 5 years old), U.S. adults, and adults from a Bolivian indigenous group spontaneously induced recursive structures from ambiguous training data. In contrast, monkeys did so only with additional exposure. We quantify these patterns using a Bayesian mixture model over logically possible strategies. Our results show that recursive hierarchical strategies are robust in human thought, both early in development and across cultures, but the capacity itself is not unique to humans.

A metacognitive illusion in monkeys.

Like humans, monkeys can make accurate judgements about their own memory by reporting their confidence during cognitive tasks. Some have suggested that animals use associative learning to make accurate confidence judgements, while others have suggested animals directly access and estimate the strength of their memories. Here we test a third, non-exclusive possibility: perhaps monkeys, like humans, base metacognitive inferences on heuristic cues. Humans are known to use cues like perceptual fluency (e.g. how easy something is to see) when making metacognitive judgements. We tested monkeys using a match-to-sample task in which the perceptual fluency of the stimuli was manipulated. The monkeys made confidence wagers on their accuracy before or after each trial. We found that monkeys' wagers were affected by perceptual fluency even when their accuracy was not. This is novel evidence that animals are susceptible to metacognitive illusions similar to those experienced by humans.

Universal and uniquely human factors in spontaneous number perception.

A capacity for nonverbal numerical estimation is widespread among humans and animals. However, it is currently unclear whether numerical percepts are spontaneously extracted from the environment and whether nonverbal perception is influenced by human exposure to formal mathematics. We tested US adults and children, non-human primates, and numerate and innumerate Tsimane' adults on a quantity task in which they could choose to categorize sets of dots on the basis of number alone, surface area alone or a combination of the two. Despite differences in age, species and education, subjects are universally biased to base their judgments on number as opposed to the alternatives. Numerical biases are uniquely enhanced in humans compared to non-human primates, and correlated with degree of mathematics experience in both the US and Tsimane' groups. We conclude that humans universally and spontaneously extract numerical information, and that human nonverbal numerical perception is enhanced by symbolic numeracy.

Precocious quantitative cognition in monkeys.

Basic quantitative abilities are thought to have an innate basis in humans partly because the ability to discriminate quantities emerges early in child development. If humans and nonhuman primates share this developmentally primitive foundation of quantitative reasoning, then this ability should be present early in development across species and should emerge earlier in monkeys than in humans because monkeys mature faster than humans. We report that monkeys spontaneously make accurate quantity choices by 1 year of age in a task that human children begin to perform only at 2.5 to 3 years of age. Additionally, we report that the quantitative sensitivity of infant monkeys is equal to that of the adult animals in their group and that rates of learning do not differ between infant and adult animals. This novel evidence of precocious quantitative reasoning in infant monkeys suggests that human quantitative reasoning shares its early developing foundation with other primates. The data further suggest that early developing components of primate quantitative reasoning are constrained by maturational factors related to genetic development as opposed to learning experience alone.

The origins of counting algorithms.

Humans' ability to count by verbally labeling discrete quantities is unique in animal cognition. The evolutionary origins of counting algorithms are not understood. We report that nonhuman primates exhibit a cognitive ability that is algorithmically and logically similar to human counting. Monkeys were given the task of choosing between two food caches. First, they saw one cache baited with some number of food items, one item at a time. Then, a second cache was baited with food items, one at a time. At the point when the second set was approximately equal to the first set, the monkeys spontaneously moved to choose the second set even before that cache was completely baited. Using a novel Bayesian analysis, we show that the monkeys used an approximate counting algorithm for comparing quantities in sequence that is incremental, iterative, and condition controlled. This proto-counting algorithm is structurally similar to formal counting in humans and thus may have been an important evolutionary precursor to human counting.

Short-term testosterone manipulations do not affect cognition or motor function but differentially modulate emotions in young and older male rhesus monkeys.

Human aging is characterized by declines in cognition and fine motor function as well as improved emotional regulation. In men, declining levels of testosterone (T) with age have been implicated in the development of these age-related changes. However, studies examining the effects of T replacement on cognition, emotion and fine motor function in older men have not provided consistent results. Rhesus monkeys (Macaca mulatta) are excellent models for human cognitive aging and may provide novel insights on this issue. We tested 10 aged intact male rhesus monkeys (mean age=19, range 15-25) on a battery of cognitive, motor and emotional tasks at baseline and under low or high T experimental conditions. Their performance was compared to that of 6 young males previously tested in the same paradigm (Lacreuse et al., 2009; Lacreuse et al., 2010). Following a 4-week baseline testing period, monkeys were treated with a gonadotropin releasing hormone agonist (Depot Lupron, 200 µg/kg) to suppress endogenous T and were tested on the task battery under a 4-week high T condition (injection of Lupron+T enanthate, 20 mg/kg, n=8) or 4-week low T condition (injection of Lupron+oil vehicle, n=8) before crossing over to the opposite treatment. The cognitive tasks consisted of the Delayed Non-Matching-to-Sample (DNMS), the Delayed Response (DR), and the Delayed Recognition Span Test (spatial-DRST). The emotional tasks included an object Approach-Avoidance task and a task in which monkeys were played videos of unfamiliar conspecifics in different emotional context (Social Playbacks). The fine motor task was the Lifesaver task that required monkeys to remove a Lifesaver candy from rods of different complexity. T manipulations did not significantly affect visual recognition memory, working memory, reference memory or fine motor function at any age. In the Approach-Avoidance task, older monkeys, but not younger monkeys, spent more time in proximity of novel objects in the high T condition relative to the low T condition. In both age groups, high T increased watching time of threatening social stimuli in the Social Playbacks. These results suggest that T affects some aspects of emotional processing but has no effect on fine motor function or cognition in young or older male macaques. It is possible that the duration of T treatment was not long enough to affect cognition or fine motor function or that T levels were too high to improve these outcomes. An alternative explanation for the discrepancies of our findings with some of the cognitive and emotional effects of T reported in rodents and humans may be the use of a chemical castration, which reduced circulating gonadotropins in addition to T. Further studies will investigate whether the luteinizing hormone LH mediates the effects of T on brain function in male primates.