Species discrimination and concept formation by rhesus monkeys (Macaca mulatta)

There are 19 species in genusMacaca and some of them are living in sympatry (Fooden, 1980). Although inter-specific hybrids are relatively easy to produce under artificial conditions, hybridization does not occur naturally. What is preventing that among the species of genusMacaca? Three rhesus monkeys acquired a discrimination between pictures with rhesus monkeys and without rhesus monkeys. All subjects showed positive transfer of this discrimination to new pictures with rhesus monkeys and without rhesus monkeys. A further test showed that these monkeys could discriminate between pictures of rhesus monkeys and pictures of Japanese monkeys. The results suggest that rhesus monkeys recognize rhesus monkeys as a class, independent of the actual stimuli such as a picture or an individual monkey. The ability to recognize members of their own species and the opportunities for such learning may be an important factor preventing hybridization among the species of genusMacaca.     

Picture – Object Recognition in Kea (Nestor notabilis)

Although pictures are widely used as stimuli in cognitive experiments with both humans and animals, the question of how subjects interpret pictures receives less attention. Gaining a better understanding of this is especially important when working with avian subjects, as their visual anatomy and processing is different from that of humans, and even differs from one avian species to another. Successful testing for picture recognition in birds has been carried out mainly with pigeons, but no such research has been explicitly performed with ‘brainy’ birds like parrots, despite the fact that these have been the subject of exciting cognitive research. This study tested kea (Nestor notabilis) mountain parrots for picture–object recognition using a procedure which required the transfer of a learned discrimination task between pictures and objects. Kea successfully showed both picture‐to‐object and object‐to‐picture transfer and performed at a comparable level when pictures were displayed on a touch screen or as printed photographs.     

From single cells to social perception

Research describing the cellular coding of faces in non-human primates often provides the underlying physiological framework for our understanding of face processing in humans. Models of face perception, explanations of perceptual after-effects from viewing particular types of faces, and interpretation of human neuroimaging data rely on monkey neurophysiological data and the assumption that neurophysiological responses of humans are comparable to those recorded in the non-human primate. Here, we review studies that describe cells that preferentially respond to faces, and assess the link between the physiological characteristics of single cells and social perception. Principally, we describe cells recorded from the non-human primate, although a limited number of cells have been recorded in humans, and are included in order to appraise the validity of non-human physiological data for our understanding of human face and social perception.     

An instance of viewpoint consistency in pigeon object recognition

Pigeons were trained on a visual discrimination, a task using a TV monitor. Two different types of stimuli appeared as pictures on the TV screen, one was a feeder used in their home cages and the other a coffee mug. One group of the pigeons was trained to peck the screen when the feeder appeared on it, while the other group was trained to peck the screen when the mug appeared. The feeder was considered to be a `familiar object' but the mug an `unfamiliar object' for the subjects. After training, to peck the familiar object, the subjects showed generalization to unusual view pictures of the object, but they did not show such generalization after training to peck the unfamiliar object. These results suggest that view point consistency is limited to familiar objects in pigeons.     

The role of the 'face-cell' area in the discrimination and recognition of faces by monkeys.

Cortical neurons that are selectively sensitive to faces, parts of faces and particular facial expressions are concentrated in the banks and floor of the superior temporal sulcus in macaque monkeys. Their existence has prompted suggestions that it is damage to such a region in the human brain that leads to prosopagnosia: the inability to recognize faces or to discriminate between faces. This was tested by removing the face-cell area in a group of monkeys. The animals learned to discriminate between pictures of faces or inanimate objects, to select the odd face from a group, to inspect a face then select the matching face from a pair of faces after a variable delay, to discriminate between novel and familiar faces, and to identify specific faces. Removing the face-cell area produced no or little impairment which in the latter case was not specific for faces. In contrast, several prosopagnosic patients were impaired at several of these tasks. The animals were less able than before to discern the angle of regard in pictures of faces, suggesting that this area of the brain may be concerned with the perception of facial expression and bearing, which are important social signals in primates.     

Better living by not completing: a wonderful peculiarity of pigeon vision?

Whereas many non-human species have been demonstrated to visually complete partly occluded figures, pigeons have been repeatedly failed to do so. We asked whether this failure reflected the pigeons' lack of perceptual process for completion or their decision among completed and non-completed figures. Four pigeons searched for a red lozenge target having one of its four contours punched in a rectangular edge out among three intact lozenges. All of these four stimuli had a white square next to them. After obtaining consistent search performances, the pigeons were tested with the punched target in a variety of locations relative to the white square, including right at the edges. Humans tested in the same task needed longer times before detecting the target when the square was placed right at the punched edge, suggesting automatic completion in humans. In contrast, the pigeons showed no similar difficulty. This result has two important suggestions: first, pigeons fail to complete partially occluded objects at the perceptual level, and second, this lack of completion is sometimes advantageous for them.     

Superior abstract-concept learning by Clark's nutcrackers (Nucifraga columbiana)

The ability to learn abstract relational concepts is fundamental to higher level cognition. In contrast to item-specific concepts (e.g. pictures containing trees versus pictures containing cars), abstract relational concepts are not bound to particular stimulus features, but instead involve the relationship between stimuli and therefore may be extrapolated to novel stimuli. Previous research investigating the same/different abstract concept has suggested that primates might be specially adapted to extract relations among items and would require fewer exemplars of a rule to learn an abstract concept than non-primate species. We assessed abstract-concept learning in an avian species, Clark''s nutcracker (Nucifraga columbiana), using a small number of exemplars (eight pairs of the same rule, and 56 pairs of the different rule) identical to that previously used to compare rhesus monkeys, capuchin monkeys and pigeons. Nutcrackers as a group (N = 9) showed more novel stimulus transfer than any previous species tested with this small number of exemplars. Two nutcrackers showed full concept learning and four more showed transfer considerably above chance performance, indicating partial concept learning. These results show that the Clark''s nutcracker, a corvid species well known for its amazing feats of spatial memory, learns the same/different abstract concept better than any non-human species (including non-human primates) yet tested on this same task.     

Pigeons identify individual humans but show no sign of recognizing them in photographs

Photographs, especially of humans, are widely used as stimuli in behavioural research with pigeons. Despite their abundant use, it is not clear to what extent pigeons perceive photographs as representing three-dimensional objects. To address this question, we trained 16 pigeons to identify individual, real-life humans. This discrimination depended primarily on visual cues from the heads of the persons. Subsequently, the pigeons were shown photographs of these individuals to test for transfer to a two-dimensional representation. Successful identification of a three-dimensional person did not facilitate learning of the corresponding photographs. These results demonstrate limitations of cross-recognition of complex objects and their photographs in pigeons.     

Picture processing in tufted capuchin monkeys (Cebus apella)

Although pictures are frequently used in place of real objects to investigate various aspects of cognition in different non-human species, there is little evidence that animals treat pictorial stimuli as representations of the real objects. In the present study, we carried out four experiments designed to assess picture processing in tufted capuchin monkeys (Cebus apella), using a simultaneous Matching-to-Sample (MTS) task. The results of the first three experiments indicate that capuchins are able to match objects with their colour photographs and vice versa, and that object-picture matching in this New World monkey species is not due to picture-object confusion. The results of the fourth experiment show that capuchins are able to recognize objects in their pictures with a high level of accuracy even when less realistic images, such as black-and-white photographs, silhouettes and line drawings, are employed as bi-dimensional stimuli. Overall, these findings indicate that capuchin monkeys are able to establish a correspondence between the real objects and their pictorial representations.     

Mind perception: real but not artificial faces sustain neural activity beyond the N170/VPP

Faces are visual objects that hold special significance as the icons of other minds. Previous researchers using event-related potentials (ERPs) have found that faces are uniquely associated with an increased N170/vertex positive potential (VPP) and a more sustained frontal positivity. Here, we examined the processing of faces as objects vs. faces as cues to minds by contrasting images of faces possessing minds (human faces), faces lacking minds (doll faces), and non-face objects (i.e., clocks). Although both doll and human faces were associated with an increased N170/VPP from 175-200 ms following stimulus onset, only human faces were associated with a sustained positivity beyond 400 ms. Our data suggest that the N170/VPP reflects the object-based processing of faces, whether of dolls or humans; on the other hand, the later positivity appears to uniquely index the processing of human faces--which are more salient and convey information about identity and the presence of other minds.     

Heterochrony and Cross-Species Intersensory Matching by Infant Vervet Monkeys

Background

Understanding the evolutionary origins of a phenotype requires understanding the relationship between ontogenetic and phylogenetic processes. Human infants have been shown to undergo a process of perceptual narrowing during their first year of life, whereby their intersensory ability to match the faces and voices of another species declines as they get older. We investigated the evolutionary origins of this behavioral phenotype by examining whether or not this developmental process occurs in non-human primates as well.

Methodology/Principal Findings

We tested the ability of infant vervet monkeys (Cercopithecus aethiops), ranging in age from 23 to 65 weeks, to match the faces and voices of another non-human primate species (the rhesus monkey, Macaca mulatta). Even though the vervets had no prior exposure to rhesus monkey faces and vocalizations, our findings show that infant vervets can, in fact, recognize the correspondence between rhesus monkey faces and voices (but indicate that they do so by looking at the non-matching face for a greater proportion of overall looking time), and can do so well beyond the age of perceptual narrowing in human infants. Our results further suggest that the pattern of matching by vervet monkeys is influenced by the emotional saliency of the Face+Voice combination. That is, although they looked at the non-matching screen for Face+Voice combinations, they switched to looking at the matching screen when the Voice was replaced with a complex tone of equal duration. Furthermore, an analysis of pupillary responses revealed that their pupils showed greater dilation when looking at the matching natural face/voice combination versus the face/tone combination.

Conclusions/Significance

Because the infant vervets in the current study exhibited cross-species intersensory matching far later in development than do human infants, our findings suggest either that intersensory perceptual narrowing does not occur in Old World monkeys or that it occurs later in development. We argue that these findings reflect the faster rate of neural development in monkeys relative to humans and the resulting differential interaction of this factor with the effects of early experience.     

Recognition of facial expressions in a Japanese monkey (Macaca fuscata) and humans (Homo sapiens)

Recognition of facial expressions by a Japanese monkey and two humans was studied. The monkey subject matched 20 photographs of monkey facial expressions and 20 photographs of human facial expressions. Humans sorted the same pictures. Matching accuracy by the monkey was about 80% correct for both human and monkey facial expressions. The confusion matrices of those facial expressions were analyzed by a multi-dimensional scaling procedure (MDSCAL). The resulting MDS plots suggested that the important cues in recognizing facial expressions of monkeys were “thrusting the mouth” and ‘raising the eyebrows.” Comparison of the MDS plots by the monkey subject with those by human subjects suggested that the monkey categorized the human “happiness” faces. This may suggest that the monkey has an ability to recognize human smile face even though it is learned. However, the monkey did not differentiate the human “anger/disgust” faces from the human “sad” faces, while human subjects clearly did. This may correlate with the lack of eyebrow movement in monkeys.     

The evolution of face processing in primates

The ability to recognize faces is an important socio-cognitive skill that is associated with a number of cognitive specializations in humans. While numerous studies have examined the presence of these specializations in non-human primates, species where face recognition would confer distinct advantages in social situations, results have been mixed. The majority of studies in chimpanzees support homologous face-processing mechanisms with humans, but results from monkey studies appear largely dependent on the type of testing methods used. Studies that employ passive viewing paradigms, like the visual paired comparison task, report evidence of similarities between monkeys and humans, but tasks that use more stringent, operant response tasks, like the matching-to-sample task, often report species differences. Moreover, the data suggest that monkeys may be less sensitive than chimpanzees and humans to the precise spacing of facial features, in addition to the surface-based cues reflected in those features, information that is critical for the representation of individual identity. The aim of this paper is to provide a comprehensive review of the available data from face-processing tasks in non-human primates with the goal of understanding the evolution of this complex cognitive skill.     

Successive two-item same-different discrimination and concept learning by pigeons

Four pigeons were trained in a successive same/different procedure involving the alternation of two stimuli per trial. Using a go/no-go procedure, two different or two identical color photographs were alternated, with a brief, dark, inter-stimulus interval, on a computer screen for 20s. Pigeons learned to discriminate between same (S+) and different (D-) sequences with moderate to large contrasts between successive pictures. Analyses of pecking behavior within single trials revealed this discrimination emerged at the earliest possible point in the sequence (i.e. by the presentation of the second item). Pigeons transferred to novel color and gray-scale pictures, and showed savings in tests with novel video stimuli. These results suggest that same/different discrimination and concept formation can be acquired with successively presented pairs of stimuli by pigeons. When combined with results using simultaneous same/different presentations, these findings further support a qualitative similarity among birds and primates in their capacity to judge certain types of stimulus relations.     

Cortical mechanisms and cues for action

Monkeys have more highly developed brains and are more intelligent than rats; yet rats learn some tasks as efficiently as monkeys. For example, rats are as quick at discovering which of two doors hides food or how to open the doors. Presumably tasks of this sort do not greatly tax cortical associative mechanisms since the animals have only to cumulate facts about objects. It is argued that cortical mechanisms are crucial for the ability to relate together information that is presented at different times or in different places. After removal of parts of frontal cortex monkeys can still associate cues that are presented together but they are poor at relating cues that are presented apart.     

Infants' knowledge of their own species

Recognition of individuals at first sight is important for social species and can be achieved by attending to facial or body information. Previous research suggests that infants possess a perceptual template for evolutionarily relevant stimuli, which may include humans, dangerous animals (e.g. snakes), but not non-dangerous animals. To be effective, such a mechanism should result in a systematic preference for attending to humans over non-dangerous animals. Using a preferential looking paradigm, the present studies investigated the nature of infants' early representation of humans. We show that 3.5- and six-month-old infants attend more to human beings than non-human primates (a gorilla or monkey) which are examplars of non-dangerous animals. This occurred when infants were presented with head or body information in isolation, as well as when both are presented simultaneously. This early preference for humans by 3.5 months of age suggests that there is a basic representation for humans, which includes both head and/or body information. However, neonates demonstrated a preference only for human faces over non-human primate faces, not for humans over non-human primates when the stimuli were presented with both head and body simultaneously. The results show that although neonates display a preference for human faces over others, preference for the human body only develops later, in the first few months of life. This suggests that infants have acquired some knowledge about the human body at 3.5 months of age that may have developed from their privileged experience with other humans in the first few months of life, rather than an innate ability to detect humans in their entirety.     

Natural conceptual behavior in squirrel monkeys (saimiri sciureus): An experimental investigation

Natural conceptual discriminations have been tested in many different species, including pigeons and a variety of non-human primates. The ability of four male squirrel monkeys (Saimiri sciureus) to learn and use the natural concept ‘squirrel monkey’ was investigated in this study. After a training phase, subjects were presented with novel stimuli in transfer and test trials. All subjects performed at a rate significantly above chance on the first test trial (p<.001), indicating that squirrel monkeys can utilize natural concepts in the laboratory.     

Behavioral research in pigeons with ARENA: An Automated Remote Environmental Navigation Apparatus

Three experiments established the effectiveness of an Automated Remote Environmental Navigation Apparatus (ARENA) developed in our lab to study behavioral processes in pigeons. The technology utilizes one or more wireless modules, each capable of presenting colored lights as visual stimuli to signal reward and of detecting subject peck responses. In Experiment 1, subjects were instrumentally shaped to peck at a single ARENA module following an unsuccessful autoshaping procedure. In Experiment 2, pigeons were trained with a simultaneous discrimination procedure during which two modules were illuminated different colors; pecks to one color (S+) were reinforced while pecks to the other color (S−) were not. Pigeons learned to preferentially peck the module displaying the S+. In Experiment 3, two modules were lit the same color concurrently from a set of six colors in a conditional discrimination task. For three of the colors pecks to the module in one location (e.g., upper quadrant) were reinforced while for the remaining colors pecks at the other module (e.g., lower quadrant) were reinforced. After learning this discrimination, the color-reinforced location assignments were reversed. Pigeons successfully acquired the reversal. ARENA is an automated system for open-field studies and a more ecologically valid alternative to the touchscreen.     

Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: comparison of cortical eye fields with humans

The frontal and parietal eye fields serve as functional landmarks of the primate brain, although their correspondences between humans and macaque monkeys remain unclear. We conducted fMRI at 4.7 T in monkeys performing visually-guided saccade tasks and compared brain activations with those in humans using identical paradigms. Among multiple parietal activations, the dorsal lateral intraparietal area in monkeys and an area in the posterior superior parietal lobule in humans exhibited the highest selectivity to saccade directions. In the frontal cortex, the selectivity was highest at the junction of the precentral and superior frontal sulci in humans and in the frontal eye field (FEF) in monkeys. BOLD activation peaks were also found in premotor areas (BA6) in monkeys, which suggests that the apparent discrepancy in location between putative human FEF (BA6, suggested by imaging studies) and monkey FEF (BA8, identified by microstimulation studies) partly arose from methodological differences.