THIS ARTICLE HAS BEEN RETRACTED: Enumeration of objects and substances in non‐human primates: experiments with brown lemurs (Eulemur fulvus)

Both human infants and adult non‐human primates share the capacity to track small numbers of objects across time and occlusion. The question now facing developmental and comparative psychologists is whether similar mechanisms give rise to this capacity across the two populations. Here, we explore whether non‐human primates’ object tracking abilities are subject to the same constraints as those of human infants. In particular, we examine whether one primate species, the brown lemur (Eulemur fulvus), also fails to represent and enumerate objects when they behave non‐rigidly or non‐cohesively. We presented lemurs with a series of expectancy violation studies involving simple 1 + 1 addition events in which we varied the entities to be enumerated. Like infants, lemurs successfully enumerated the two objects when those objects were rigid, cohesive individuals, but failed to enumerate similar‐looking non‐rigid piles of sand. In contrast to human infants, however, lemurs successfully enumerated non‐cohesive objects that broke into multiple pieces. These results are discussed in light of recent theories about object processing in human infants and adults.     

The best time to acquire new skills: age-related differences in implicit sequence learning across the human lifespan

Implicit skill learning underlies obtaining not only motor, but also cognitive and social skills through the life of an individual. Yet, the ontogenetic changes in humans' implicit learning abilities have not yet been characterized, and, thus, their role in acquiring new knowledge efficiently during development is unknown. We investigated such learning across the lifespan, between 4 and 85 years of age with an implicit probabilistic sequence learning task, and we found that the difference in implicitly learning high- vs. low-probability events--measured by raw reaction time (RT)--exhibited a rapid decrement around age of 12. Accuracy and z-transformed data showed partially different developmental curves, suggesting a re-evaluation of analysis methods in developmental research. The decrement in raw RT differences supports an extension of the traditional two-stage lifespan skill acquisition model: in addition to a decline above the age 60 reported in earlier studies, sensitivity to raw probabilities and, therefore, acquiring new skills is significantly more effective until early adolescence than later in life. These results suggest that due to developmental changes in early adolescence, implicit skill learning processes undergo a marked shift in weighting raw probabilities vs. more complex interpretations of events, which, with appropriate timing, prove to be an optimal strategy for human skill learning.     

Deviations in the emergence of representations: a neuroconstructivist framework for analysing developmental disorders

A common way of studying developmental disorders is to adopt a static neuropsychological deficit approach, in which the brain is characterized in terms of a normal brain with some parts or ‘modules’ impaired. In this paper we outline a neuroconstructivist approach in which developmental disorders are viewed as alternative developmental trajectories in the emergence of representations within neural networks. As a concrete instantiation of the assumptions underlying this general approach, we present a number of simulations in an artificial neural network model. The representations that emerge under different architectural, input and developmental timing conditions are then analysed within a multi‐dimensional state space. We explore alternative developmental trajectories in these simulations, demonstrating how initial differences in the same parameter can lead to very different outcomes, and conversely how different starting states can sometimes result in similar end states (phenotypes). We conclude that the assumptions of the neuroconstructivist approach are likely to be more appropriate for analysing developmental deviations in complex dynamic neural networks, such as the human brain.     

Primate vocal production and the riddle of language evolution

Trying to uncover the roots of human speech and language has been the premier motivation to study the signalling behaviour of nonhuman primates for several decades. Focussing on the question of whether we find evidence for linguistic reference in the production of nonhuman primate vocalizations, I will first discuss how the criteria used to diagnose referential signalling have changed over time, and will then turn to the paradigmatic case of semantic communication in animals, the alarm calls of vervet monkeys, Chlorocebus pygerythrus. A recent in-depth analysis of the original material revealed that, while the alarm calls could be well distinguished, calls of similar structure were also used in within- and between-group aggression. This finding is difficult to reconcile with the idea that calls denote objects in the environment. Furthermore, nonhuman primates show only minimal signs of vocal production learning, one key prerequisite for conventionalized and symbolic communication. In addition, the structure of calls in different populations or closely related species is highly conserved. In conclusion, any continuity between nonhuman primate and human communication appears to be found at the level of the processing of signals. Why and how the ancestors of our own species one day began to talk to each other continues to be an enigma. Future research should focus on changes in the neural structure supporting volitional control over vocalizations, the gene networks associated with vocal production, and the developmental processes involved in the integration of production and perception of vocalizations.     

Systematic mapping of developmental milestones in wild chimpanzees

Postnatal development is protracted relative to lifespan in many primates, including modern humans (Homo sapiens), facilitating the acquisition of key motor, communication and social skills that can maximize fitness later in life. Nevertheless, it remains unclear what evolutionary drivers led to extended immature periods. While the developmental milestone literature is well established in humans, insight we can gain from one‐species models is limited. By comparing the timing of relatable developmental milestones in a closely related species, the chimpanzee (Pan troglodytes), we can gain further understanding of the evolution of such an extended developmental phase. To date, few studies have specifically attempted to estimate developmental milestones in a manner comparable to the human literature, and existing studies lack sufficient sample sizes to estimate which milestones are more plastic with higher inter‐individual variation in the timing of their emergence. Here, we describe the emergence of gross motor, fine motor, social interaction and communication traits from a longitudinal sample of 19 wild chimpanzee infants (8 females and 11 males), Taï National Park, Côte d’Ivoire. Gross motor traits emerged at a mean of 4 months, communication traits at 12 months, social interaction traits at 14 months and fine motor traits at 15 months, with later emerging milestones demonstrating greater inter‐individual variation in the timing of the emergence. This pattern of milestone emergence is broadly comparable to observations in humans, suggesting selection for a prolonged infantile phase and that sustained skills development has a deep evolutionary history, with implications for theories on primate brain development.     

Developmental neuroimaging of the human ventral visual cortex

Here, we review recent results that investigate the development of the human ventral stream from childhood, through adolescence and into adulthood. Converging evidence suggests a differential developmental trajectory across ventral stream regions, in which face-selective regions show a particularly long developmental time course, taking more than a decade to become adult-like. We discuss the implications of these recent findings, how they relate to age-dependent improvements in recognition memory performance and propose possible neural mechanisms that might underlie this development. These results have important implications regarding the role of experience in shaping the ventral stream and the nature of the underlying representations.     

Correlations between intelligence and components of serial timing variability

Psychometric intelligence correlates with reaction time in elementary cognitive tasks, as well as with performance in time discrimination and judgment tasks. It has remained unclear, however, to what extent these correlations are due to top–down mechanisms, such as attention, and bottom–up mechanisms, i.e. basic neural properties that influence both temporal accuracy and cognitive processes. Here, we assessed correlations between intelligence (Raven SPM Plus) and performance in isochronous serial interval production, a simple, automatic timing task where participants first make movements in synchrony with an isochronous sequence of sounds and then continue with self-paced production to produce a sequence of intervals with the same inter-onset interval (IOI). The target IOI varied across trials. A number of different measures of timing variability were considered, all negatively correlated with intelligence. Across all stimulus IOIs, local interval-to-interval variability correlated more strongly with intelligence than drift, i.e. gradual changes in response IOI. The strongest correlations with intelligence were found for IOIs between 400 and 900 ms, rather than above 1 s, which is typically considered a lower limit for cognitive timing. Furthermore, poor trials, i.e. trials arguably most affected by lapses in attention, did not predict intelligence better than the most accurate trials. We discuss these results in relation to the human timing literature, and argue that they support a bottom–up model of the relation between temporal variability of neural activity and intelligence.     

Motor sequence learning in children with recovered and persistent developmental stuttering: preliminary findings

PurposePrevious studies have associated developmental stuttering with difficulty learning new motor skills. We investigated non-speech motor sequence learning in children with persistent developmental stuttering (CWS), children who have recovered from developmental stuttering (CRS) and typically developing controls (CON).MethodsOver the course of two days, participants completed the Multi-Finger Sequencing Task, consisting of repeated trials of a10-element sequence, interspersed with trials of random sequences of the same length. We evaluated motor sequence learning using accuracy and response synchrony, a timing measure for evaluation of sequencing timing. We examined error types as well as recognition and recall of the repeated sequences.ResultsCWS demonstrated lower performance accuracy than CON and CRS on the first day of the finger tapping experiment but improved to the performance level of CON and CRS on the second day. Response synchrony showed no overall difference among CWS, CRS and CON.Learning scores of repeated sequences did not differ from learning scores of random sequences in CWS, CRS and CON. CON and CRS demonstrated an adaptive strategy to response errors, whereas CWS maintained a high percentage of corrected errors for both days.ConclusionsOur study examined non-speech sequence learning across CWS, CRS and CON. Our preliminary findings support the idea that developmental stuttering is not associated with sequence learning per se but rather with general fine motor performance difficulties.     

Primate Numerical Competence: Contributions Toward Understanding Nonhuman Cognition

Nonhuman primates represent the most significant extant species for comparative studies of cognition, including such complex phenomena as numerical competence, among others. Studies of numerical skills in monkeys and apes have a long, though somewhat sparse history, although questions for current empirical studies remain of great interest to several fields, including comparative, developmental, and cognitive psychology; anthropology; ethology; and philosophy, to name a few. In addition to demonstrated similarities in complex information processing, empirical studies of a variety of potential cognitive limitations or constraints have provided insights into similarities and differences across the primate order, and continue to offer theoretical and pragmatic directions for future research. An historical overview of primate numerical studies is presented, as well as a summary of the 17‐year research history, including recent findings, of the Comparative Cognition Project at The Ohio State University Chimpanzee Center. Overall, the archival literature on number‐related skills and counting in nonhuman primates offers important implications for revising our thinking about comparative neuroanatomy, cross‐species (human/ape) cognitive similarities and differences, and the evolution of cognition represented by the primate continuum.     

The neuroethology of primate vocal communication: substrates for the evolution of speech

In this article, we review behavioral and neurobiological studies of the perception and use of species-specific vocalizations by non-human primates. At the behavioral level, primate vocal perception shares many features with speech perception by humans. These features include a left-hemisphere bias towards conspecific vocalizations, the use of temporal features for identifying different calls, and the use of calls to refer to objects and events in the environment. The putative neural bases for some of these behaviors have been revealed by recent studies of the primate auditory and prefrontal cortices. These studies also suggest homologies with the human language circuitry. Thus, a synthesis of cognitive, ethological and neurobiological approaches to primate vocal behavior is likely to yield the richest understanding of the neural bases of speech perception, and might also shed light on the evolutionary precursors to language.     

Evolution of the neural language network

The evolution of language correlates with distinct changes in the primate brain. The present article compares language-related brain regions and their white matter connectivity in the developing and mature human brain with the respective structures in the nonhuman primate brain. We will see that the functional specificity of the posterior portion of Broca’s area (Brodmann area [BA 44]) and its dorsal fiber connection to the temporal cortex, shown to support the processing of structural hierarchy in humans, makes a crucial neural difference between the species. This neural circuit may thus be fundamental for the human syntactic capacity as the core of language.     

The role of propulsive muscles of the shoulder during quadrupedalism in vervet monkeys (Cercopithecus aethiops): implications for neural control of locomotion in primates

In comparative anatomical studies of the shoulder, the humeral retractors are often grouped together as propulsive muscles, which are important in the propulsive stroke of the forelimb during quadrupedal locomotion. Electromyographic (EMG) analyses of these muscles in opossums, cats, and dogs in general have confirmed such conclusions. An EMG study of chimpanzee shoulder muscles during knuckle-walking found, however, that the humeral retractors are either inactive or perform a function unrelated to propulsion (Larson & Stern, 1987). This contrast in muscle recruitment patterns between chimpanzees and more "typical" mammalian quadrupeds was attributed to the derived morphology of the chimpanzee shoulder. The present study examines the activity patterns of the humeral retractors in the vervet monkey, a primate more closely resembling nonprimate mammals in its shoulder morphology. The results of this EMG analysis show that despite the significant differences in anatomy between chimpanzees and vervets, the two species display very similar muscle recruitment patterns during quadrupedalism, and there is evidence for this same pattern in other species of primates. These differences in muscle activity patterns between primates and nonprimate mammals may be related to changes in the neurological control of locomotion in primates due to the evolutionary development of manipulative abilities in the primate forelimb.     

Monkey lipsmacking develops like the human speech rhythm

Across all languages studied to date, audiovisual speech exhibits a consistent rhythmic structure. This rhythm is critical to speech perception. Some have suggested that the speech rhythm evolved de novo in humans. An alternative account--the one we explored here--is that the rhythm of speech evolved through the modification of rhythmic facial expressions. We tested this idea by investigating the structure and development of macaque monkey lipsmacks and found that their developmental trajectory is strikingly similar to the one that leads from human infant babbling to adult speech. Specifically, we show that: (1) younger monkeys produce slower, more variable mouth movements and as they get older, these movements become faster and less variable; and (2) this developmental pattern does not occur for another cyclical mouth movement--chewing. These patterns parallel human developmental patterns for speech and chewing. They suggest that, in both species, the two types of rhythmic mouth movements use different underlying neural circuits that develop in different ways. Ultimately, both lipsmacking and speech converge on a ~5 Hz rhythm that represents the frequency that characterizes the speech rhythm of human adults. We conclude that monkey lipsmacking and human speech share a homologous developmental mechanism, lending strong empirical support to the idea that the human speech rhythm evolved from the rhythmic facial expressions of our primate ancestors.     

“Counting” serially presented stimuli by human and nonhuman primates and pigeons

Much of Stewart Hulse's career was spent analyzing how animals can extract patterned information from sequences of stimuli. Yet an additional form of information contained in a sequence may be the number of times different elements occurred. Experiments that required numerical discrimination between different stimulus items presented in sequence are analyzed for primates and pigeons. It is shown that a model based on magnitude discrimination can account well for data from human and nonhuman primate experiments. Similar experiments carried out with pigeons showed a strong recency effect not found with primates. The pigeon data are modeled successfully, however, by assuming that representations of events decay as other events are presented.     

The time of our lives: life span development of timing and event tracking

Life span developmental profiles were constructed for 305 participants (ages 4-95) for a battery of paced and unpaced perceptual-motor timing tasks that included synchronize-continue tapping at a wide range of target event rates. Two life span hypotheses, derived from an entrainment theory of timing and event tracking, were tested. A preferred period hypothesis predicted a monotonic slowing of a preferred rate (tempo) of event tracking across the life span. An entrainment region hypothesis predicted a quadratic profile in the range of event rates that produced effective timing across the life span; specifically, age-specific entrainment regions should be narrower in childhood and late adulthood than in midlife. Findings across tasks provide converging support for both hypotheses. Implications of these findings are discussed for understanding critical periods in development and age-related slowing of event timing.     

Modeling how, when, and what is learned in a simple fault-finding task

We have developed a process model that learns in multiple ways while finding faults in a simple control panel device. The model predicts human participants' learning through its own learning. The model's performance was systematically compared to human learning data, including the time course and specific sequence of learned behaviors. These comparisons show that the model accounts very well for measures such as problem-solving strategy, the relative difficulty of faults, and average fault-finding time. More important, because the model learns and transfers its learning across problems, it also accounts for the faster problem-solving times due to learning when examined across participants, across faults, and across the series of 20 trials on an individual participant basis. The model shows how learning while problem solving can lead to more recognition-based performance, and helps explain how the shape of the learning curve can arise through learning and be modified by differential transfer. Overall, the quality of the correspondence appears to have arisen from procedural, declarative, and episodic learning all taking place within individual problem-solving episodes.     

‘Unwilling’ versus ‘unable’: capuchin monkeys’ (Cebus apella) understanding of human intentional action

A sensitivity to the intentions behind human action is a crucial developmental achievement in infants. Is this intention reading ability a unique and relatively recent product of human evolution and culture, or does this capacity instead have roots in our non‐human primate ancestors? Recent work by Call and colleagues (2004) lends credence to the latter hypothesis, providing evidence that chimpanzees are also sensitive to human intentions. Specifically, chimpanzees remained in a testing area longer and exhibited fewer frustration behaviors when an experimenter behaved as if he intended to give food but was unable to do so, than when the experimenter behaved as if he had no intention of giving food. The present research builds on and extends this paradigm, providing some of the first evidence of intention reading in a more distant primate relative, the capuchin monkey (Cebus apella). Like chimpanzees, capuchin monkeys distinguish between different goal‐directed acts, vacating an enclosure sooner when an experimenter acts unwilling to give food than when she acts unable to give food. Additionally, we found that this pattern is specific to animate action, and does not obtain when the same actions are performed by inanimate rods instead of human hands (for a similar logic, see Woodward, 1998 ). Taken together with the previous evidence, the present research suggests that our own intention reading is not a wholly unique aspect of the human species, but rather is shared broadly across the primate order.     

The Role of Propulsive Muscles of the Shoulder During Quadrupedalism in Vervet Monkeys (Cercopithecus aethiops)

In comparative anatomical studies of the shoulder, the humeral retractors are often grouped together as propulsive muscles, which are important in the propulsive stroke of the forelimb during quadrupedal locomotion. Electromyographic (EMG) analyses of these muscles in opossums, cats, and dogs in general have confirmed such conclusions. An EMG study of chimpanzee shoulder muscles during knuckle-walking found, however, that the humeral retractors are either inactive or perform a function unrelated to propulsion (Larson & Stern, 1987). This contrast in muscle recruitment patterns between chimpanzees and more “typical” mammalian quadrupeds was attributed to the derived morphology of the chimpanzee shoulder. The present study examines the activity patterns of the humeral retractors in the vervet monkey, a primate more closely resembling nonprimate mammals in its shoulder morphology. The results of this EMG analysis show that despite the significant differences in anatomy between chimpanzees and vervets, the two species display very similar muscle recruitment patterns during quadrupedalism, and there is evidence for this same pattern in other species of primates. These differences in muscle activity patterns between primates and nonprimate mammals may be related to changes in the neurological control of locomotion in primates due to the evolutionary development of manipulative abilities in the primate forelimb.     

Un modèle neurobiologique de la perception et de l'estimation du temps

Frontal-striatal circuits provide an important neurobiological substrate for timing and time perception as well as for working memory. In this review, we outline recent theoretical and empirical work to suggest that interval timing and working memory rely not only on the same anatomic structures, but also on the same neural representation of a specific stimulus. In the striatal beat-frequency model, cortical neurons fire in an oscillatory fashion to form representations of stimuli, and striatal medium spiny neurons detect those patterns of cortical firing that occur co-incident to important temporal events. Information about stimulus identity can be extracted from the specific cortical networks that are involved in the representation, and information about duration can be extracted from the relative phase of neural firing. The properties derived from these neurobiological models fit well with the psychophysics of timing and time perception as well as with information-processing models that emphasize the importance of temporal coding in a variety of working-memory phenomena.     

Neurobehavioral Changes in Adolescence

Adolescents across a variety of species exhibit age-specific behavioral characteristics that may have evolved to help them attain the necessary skills for independence. These adolescent-related characteristics, such as an increase in risk taking, may be promoted less by the hormonal changes of puberty than by developmental events occurring in brain. Among the prominent brain transformations of adolescence are alterations in the prefrontal cortex, limbic brain areas, and their dopamine input, systems that are sensitive to stressors and form part of the neural circuitry modulating the motivational value of drugs and other reinforcing stimuli. Such developmental transformations of the adolescent brain may predispose adolescents to behave in particular ways and make them particularly likely to initiate use of alcohol and other drugs.