Dissociation of visual localization and visual detection in rhesus monkeys (Macaca mulatta)

Conscious and unconscious cognitive processes contribute independently to human behavior and can be dissociated. For example, humans report failing to see objects clearly in the periphery while simultaneously being able to grasp those objects accurately (Milner in Proc R Soc B Biol Sci 279:2289–2298, 2012). Knowing whether similar dissociations are present in nonverbal species is critical to our understanding of comparative psychology and the evolution of brains. However, such dissociations are difficult to detect in nonhumans because verbal reports of experience are the main way we discriminate putative conscious from unconscious processing. We trained monkeys in a localization task in which they responded to the location where a target appeared, and a matched detection task in which they reported the presence or absence of the same target. We used masking to manipulate the visibility of targets. Accuracy was high in both tasks when stimuli were unmasked and was attenuated by visual masking. At the strongest level of masking, performance in the detection task was at chance, while localization remained significantly above chance. Critically, errors in the detection task were predominantly misses, indicating that the monkeys’ behavior remained under stimulus control, but that the monkeys did not detect the target despite above-chance localization. While these results cannot establish the existence of phenomenal vision in monkeys, the dissociation of visually guided action from detection parallels the dissociation of conscious and unconscious vision seen in humans.     

Discrimination of artificial polymorphous categories by rhesus monkeys (Macaca mulatta)

Monkeys (Macaca mulatta) were trained to discriminate between sets of artificial stimuli such as those used by Jitsumori (1993) for pigeons and humans. The stimuli were arrays of symbols differing along three two-valued (positive or negative) dimensions. The discrimination required was between polymorphous categories in which a positive stimulus was defined by possession of any 2 out of 3 positive features. Of the 5 monkeys, 3 learned the discrimination much faster than did pigeons, but transfer to novel stimuli was less impressive than had been shown in pigeons. The 3 monkeys showed high levels of transfer to the stimuli that contained either all 3 positive or all 3 negative features, but 2 of the 3 monkeys failed to show transfer to stimuli that had 1 of the 3 features replaced with a novel one. Analysis of the monkeys' performance raised doubts on the additive integration of features but supported learning of feature combinations as a basis for the discrimination of polymorphous categories by this species.     

Visual artificial grammar learning by rhesus macaques (<Emphasis Type="Italic">Macaca mulatta</Emphasis>): exploring the role of grammar complexity and sequence length

Humans and nonhuman primates can learn about the organization of stimuli in the environment using implicit sequential pattern learning capabilities. However, most previous artificial grammar learning studies with nonhuman primates have involved relatively simple grammars and short input sequences. The goal in the current experiments was to assess the learning capabilities of monkeys on an artificial grammar-learning task that was more complex than most others previously used with nonhumans. Three experiments were conducted using a joystick-based, symmetrical-response serial reaction time task in which two monkeys were exposed to grammar-generated sequences at sequence lengths of four in Experiment 1, six in Experiment 2, and eight in Experiment 3. Over time, the monkeys came to respond faster to the sequences generated from the artificial grammar compared to random versions. In a subsequent generalization phase, subjects generalized their knowledge to novel sequences, responding significantly faster to novel instances of sequences produced using the familiar grammar compared to those constructed using an unfamiliar grammar. These results reveal that rhesus monkeys can learn and generalize the statistical structure inherent in an artificial grammar that is as complex as some used with humans, for sequences up to eight items long. These findings are discussed in relation to whether or not rhesus macaques and other primate species possess implicit sequence learning abilities that are similar to those that humans draw upon to learn natural language grammar.     

The analysis of human behavior in context

Does the name of the special interest group, “The Experimental Analysis of Human Behavior,” imply that those who analyze the behavior of human animals must organize themselves apart from those who analyze the behavior of nonhuman animals? Is the use of nonhumans in experiments really not relevant to the analysis of the behavior of humans? If so, then something must have changed. Many differences exist, of course, between the behavior of humans and nonhumans—humans, for example, cannot fly under their own power—but have we really isolated differences in principle, differences that require separate organizations for the study of each? I will try to indicate why I believe this is a serious concern, where the concern comes from, and what, perhaps, might be done to maintain what was once a flourishing bidirectional relation between research with humans and nonhumans, in both basic and applied research.     

Attentional biases and memory for emotional stimuli in men and male rhesus monkeys

We examined attentional biases for social and non-social emotional stimuli in young adult men and compared the results to those of male rhesus monkeys (Macaca mulatta) previously tested in a similar dot-probe task (King et al. in Psychoneuroendocrinology 37(3):396–409, 2012). Recognition memory for these stimuli was also analyzed in each species, using a recognition memory task in humans and a delayed non-matching-to-sample task in monkeys. We found that both humans and monkeys displayed a similar pattern of attentional biases toward threatening facial expressions of conspecifics. The bias was significant in monkeys and of marginal significance in humans. In addition, humans, but not monkeys, exhibited an attentional bias away from negative non-social images. Attentional biases for social and non-social threat differed significantly, with both species showing a pattern of vigilance toward negative social images and avoidance of negative non-social images. Positive stimuli did not elicit significant attentional biases for either species. In humans, emotional content facilitated the recognition of non-social images, but no effect of emotion was found for the recognition of social images. Recognition accuracy was not affected by emotion in monkeys, but response times were faster for negative relative to positive images. Altogether, these results suggest shared mechanisms of social attention in humans and monkeys, with both species showing a pattern of selective attention toward threatening faces of conspecifics. These data are consistent with the view that selective vigilance to social threat is the result of evolutionary constraints. Yet, selective attention to threat was weaker in humans than in monkeys, suggesting that regulatory mechanisms enable non-anxious humans to reduce sensitivity to social threat in this paradigm, likely through enhanced prefrontal control and reduced amygdala activation. In addition, the findings emphasize important differences in attentional biases to social versus non-social threat in both species. Differences in the impact of emotional stimuli on recognition memory between monkeys and humans will require further study, as methodological differences in the recognition tasks may have affected the results.     

Human Sensitivity To Concurrent Schedules Of Reinforcement: Effects Of Observing Schedule-correlated Stimuli

The determinants of human sensitivity to concurrent variable-interval variable-interval schedules of reinforcement have been difficult to identify, in part because of procedural differences separating published experiments. This experiment investigated vigilance to stimuli correlated with concurrent schedules. Across phases, 3 college students were provided with either no schedule-correlated stimuli, an observing response that provided brief access to the stimuli, or a contingency that required the subject to identify the stimulus correlated with the source of each obtained reinforcer. Sensitivity, as quantified by the generalized matching equation, was low when no stimuli were available. When the stimuli were response contingent, 1 subject observed them, and her behavior became more sensitive to the distribution of reinforcers across the concurrent schedules. When the procedure required discrimination of the stimulus correlated with each reinforcer, the other 2 subjects also observed the stimuli, and their schedule sensitivity was increased as well. These results implicate procedural differences, rather than inherent behavioral differences, as the source of differences in sensitivity to schedules of reinforcement between humans and nonhumans.     

Duration perception in crossmodally-defined intervals

How humans perform duration judgments with multisensory stimuli is an ongoing debate. Here, we investigated how sub-second duration judgments are achieved by asking participants to compare the duration of a continuous sound to the duration of an empty interval in which onset and offset were marked by signals of different modalities using all combinations of visual, auditory and tactile stimuli. The pattern of perceived durations across five stimulus durations (ranging from 100 ms to 900 ms) follows the Vierordt Law. Furthermore, intervals with a sound as onset (audio-visual, audio-tactile) are perceived longer than intervals with a sound as offset. No modality ordering effect is found for visualtactile intervals. To infer whether a single modality-independent or multiple modality-dependent time-keeping mechanisms exist we tested whether perceived duration follows a summative or a multiplicative distortion pattern by fitting a model to all modality combinations and durations. The results confirm that perceived duration depends on sensory latency (summative distortion). Instead, we did not find evidence for multiplicative distortions. The results of the model and the behavioural data support the concept of a single time-keeping mechanism that allows for judgments of durations marked by multisensory stimuli.     

An update on the search for symmetry in nonhumans

Sidman et al.'s (1982) failure to find evidence for symmetry (bidirectional associations between stimuli) in monkeys and baboons set the stage for decades of work on emergent relations in nonhumans. They attributed the failure to the use of procedures that did not (1) promote stimulus control based on the relation between the sample and correct comparison and (2) reduce control by irrelevant stimulus features. Previous reviews of symmetry in nonhumans indicated that multiple exemplar training and successive matching might encourage appropriate stimulus control. This review examined 16 studies that investigated symmetry in 94 subjects, including pigeons, rats, capuchin monkeys, and baboons. Several studies used alternative training procedures to minimize sources of irrelevant stimulus control, and many combined multiple exemplar training with other procedural modifications. Symmetry was observed in approximately 30% of subjects. Studies that reported the strongest evidence for symmetry used successive matching-to-sample procedures that included training on both symbolic and identity relations, and studies finding mixed evidence employed alternative methods. These studies highlight the challenge in creating training procedures that promote symmetry and the need to assess the underlying sources of control on positive demonstrations.     

Discrimination of faces and houses by rhesus monkeys: the role of stimulus expertise and rotation angle

The face inversion effect, or impaired recognition of upside down compared to upright faces, is used as a marker for the configural processing of faces in primates. The inversion effect in humans and chimpanzees is strongest for categories of stimuli for which subjects have considerable expertise, primarily conspecifics’ faces. Moreover, discrimination performance decreases linearly as faces are incrementally rotated from upright to inverted. This suggests that rotated faces must be transformed, or normalized back into their most typical viewpoint before configural processing can ensue, and the greater the required normalization, the greater the likelihood of errors resulting. Previous studies in our lab have demonstrated a general face inversion effect in rhesus monkeys that was not influenced by expertise. Therefore, the present study examined the influence of rotation angle on the visual perception of face and nonface stimuli that varied in their level of expertise to further delineate the processes underlying the inversion effect in rhesus monkeys. Five subjects discriminated images in five orientation angles. Results showed significant linear impairments for all stimulus categories, including houses. However, compared to the upright images, only rhesus faces resulted in worse performance at rotation angles greater than 45°, suggesting stronger configural processing for stimuli for which subjects had the greatest expertise.     

Theoretical implications of the neurotic paradox as a problem in behavior theory: An experimental resolution

Why do human phobias last for months or years when such behavior should undergo extinction? This failure of extinction or persistence of self-defeating behavior of human disorders was labeled by Mowrer as the neurotic paradox. The paradox is cited by an ever-increasing number of critics who challenge any laboratory-based learning model of human psychopathology. Laboratory research, of course, omits essential requirements in the analysis of behavior, and the principles derived from such analyses must be combined in order to explain complex human behavaior. Validation for a behavioral model can thus be achieved if (a) basic principles inferred from observation of humans treated with a laboratory-derived extinction procedure (e.g., implosive therapy) are combined with (b) principles examined in laboratory research that are combined to generate unique predictions that correspond to known features of human phobic behavior. The latter evidence is briefly reviewed in research demonstrating sustained responding over one thousand consecutive active avoidance responses with complete avoidance of the “phobic” CS for an initial single shock trial. Differential reinforcement for responses to early sequential stimuli depends on minimal work requirement, and reinforcement by timeout from avoidance. This combination of factors effectively precludes extinction to main conditioned aversive stimuli for nonhumans, as it does for human phobias. Support for a laboratory model of human phobia is thereby attained.     

Are monkeys aesthetists? Rensch (1957) revisited

Three experiments assessed whether capuchin monkeys (Cebus apella) and squirrel monkeys (Saimiri sciureus) prefer regular and symmetrical visual patterns. Pictorial representations of faces were included in 1 stimulus set. When the monkeys could pick up and manipulate small cards bearing the stimuli, all preferences expressed by capuchins and most of those expressed by squirrel monkeys were for regular stimuli. Symmetry of the patterns was influential but not essential. Some preferences were also found for faces. When images of the patterns were presented on a touch screen, capuchins continued to express preferences especially for regular and symmetrical stimuli, but they showed some avoidance of faces. Squirrel monkeys responded less discriminatingly to the touch screen stimuli. The findings provide support for B. Rensch's (1957) claim that monkeys prefer visual stimuli that humans find aesthetically pleasing.     

Natural concepts in a juvenile gorilla (gorilla gorilla gorilla) at three levels of abstraction

The extent to which nonhumans are able to form conceptual versus perceptual discriminations remains a matter of debate. Among the great apes, only chimpanzees have been tested for conceptual understanding, defined as the ability to form discriminations not based solely on simple perceptual features of stimuli, and to transfer this learning to novel stimuli. In the present investigation, a young captive female gorilla was trained at three levels of abstraction (concrete, intermediate, and abstract) involving sets of photographs representing natural categories (e.g., orangutans vs. humans, primates vs. nonprimate animals, animals vs. foods). Within each level of abstraction, when the gorilla had learned to discriminate positive from negative exemplars in one set of photographs, a novel set was introduced. Transfer was defined in terms of high accuracy during the first two sessions with the new stimuli. The gorilla acquired discriminations at all three levels of abstraction but showed unambiguous transfer only with the concrete and abstract stimulus sets. Detailed analyses of response patterns revealed little evidence of control by simple stimulus features. Acquisition and transfer involving abstract stimulus sets suggest a conceptual basis for gorilla categorization. The gorilla's relatively poor performance with intermediate-level discriminations parallels findings with pigeons, and suggests a need to reconsider the role of perceptual information in discriminations thought to indicate conceptual behavior in nonhumans.     

The sunk cost effect across species: A review of persistence in a course of action due to prior investment

The sunk cost effect is the bias or tendency to persist in a course of action due to prior investments of effort, money or time. At the time of the only review on the sunk cost effect across species (Arkes & Ayton, 1999), research with nonhuman animals had been ecological in its nature, and the findings about the effect of past investments on current choice were inconclusive. However, in the last decade a new line of experimental laboratory‐based research has emerged with the promise of revolutionizing the way we approach the study of the sunk cost effect in nonhumans. In the present review we challenge Arkes and Ayton's conclusion that the sunk cost effect is exclusive to humans, and describe evidence for the sunk cost effect in nonhuman animals. By doing so, we also challenge the current explanations for the sunk cost effect in humans, as they are not applicable to nonhumans. We argue that a unified theory is called for, because different independent variables, in particular, investment amount, have the same influence on the sunk cost effect across species. Finally, we suggest possible psychological mechanisms shared across different species, contrast and depreciation, that could explain the sunk cost effect.     

Social competence is reduced in socially deprived rhesus monkeys (Macaca mulatta)

Rhesus monkeys deprived for some period from their mother have often served as a model for the effect of adverse rearing conditions on social competence in humans. Social competence is the capacity to react in a species-specific way to social interactions. The current study assesses whether early deprivation from peers also affects the rates of behavior and social competence in rhesus monkeys. This was studied in groups of rhesus monkeys with different rearing conditions: subadult females that were mother-only reared during their first year of life and subsequently housed with peers were compared with subadult females from five naturalistic social groups. Socially deprived monkeys showed higher rates of submission and stereotypic behaviors than socially reared individuals. In addition, they show socially incompetent behavior, since they react with agonistic behavior to nonthreatening social situations. The results suggest that this socially incompetent behavior is rooted in a general feeling of anxiety toward group companions. The authors hypothesize that anxiety negatively affects social information processing, which results in socially incompetent behavior.     

The reversed work‐ethic effect: Monkeys avoid stimuli associated with high‐effort1

We investigated how different numbers of responses prior to the presentation of a stimulus influenced preferences for the stimulus in three Japanese monkeys (Macaca fuscata). Monkeys were trained for two kinds of simultaneous discriminations that followed a high‐effort or a low‐effort response. In probe test trials, the stimulus that followed the high‐effort and the stimulus that followed the low‐effort response during discriminations were presented simultaneously. All monkeys chose stimuli that in training followed a low‐effort response. This result suggested that monkeys avoided stimuli that followed high‐effort responses because of the association between those stimuli and the preceding greater effort. The present result is consistent with our previous study conducted with humans, but contradicts analogous studies carried out with pigeons that reported either opposite results (i.e. pigeons preferred the stimuli after high‐effort) or non‐biased preferences. The differences between mammals and birds are discussed in terms of the lack of a successive negative contrast effect in birds.     

Speech perception by rhesus monkeys: The voicing distinction in synthesized labial and velar stop consonants

Monkeys were presented with synthetic speech stimuli in a shock-avoidance situation. On the basis of their behavior, perceptual boundaries were determined along the physical continua between /ba/ and /pa/, and /ga/ and /ka/, that were close to the human boundaries between voiced and voiceless consonants. As is the case with humans, discrimination across a boundary was better than discrimination between stimuli that were both on one side of the boundary, and there was generalization of the voiced-voiceless distinction from labial to velar syllables. Unlike humans, the monkeys showed large shifts in boundary when the range of stimuli was varied.     

Spatial representation of magnitude in humans (<Emphasis Type="Italic">Homo sapiens</Emphasis>), Western lowland gorillas (<Emphasis Type="Italic">Gorilla gorilla gorilla</Emphasis>), and American black bears (<Emphasis Type="Italic">Ursus americanus</Emphasis>)

The spatial-numerical association of response codes (SNARC) effect is the tendency for humans to respond faster to relatively larger numbers on the left or right (or with the left or right hand) and faster to relatively smaller numbers on the other side. This effect seems to occur due to a spatial representation of magnitude either in occurrence with a number line (wherein participants respond to relatively larger numbers faster on the right), other representations such as clock faces (responses are reversed from number lines), or culturally specific reading directions, begging the question as to whether the effect may be limited to humans. Given that a SNARC effect has emerged via a quantity judgement task in Western lowland gorillas and orangutans (Gazes et al., Cog 168:312–319, 2017), we examined patterns of response on a quantity discrimination task in American black bears, Western lowland gorillas, and humans for evidence of a SNARC effect. We found limited evidence for SNARC effect in American black bears and Western lowland gorillas. Furthermore, humans were inconsistent in direction and strength of effects, emphasizing the importance of standardizing methodology and analyses when comparing SNARC effects between species. These data reveal the importance of collecting data with humans in analogous procedures when testing nonhumans for effects assumed to bepresent in humans.     

Is the inversion effect in rhesus monkeys face-specific?

This study investigated the face inversion effect in rhesus monkeys (Macaca mulatta). Face stimuli consisted of ten black-and-white examples of unfamiliar rhesus monkey faces, brown capuchin faces, and human faces. Two non-face categories included ten examples of automobiles and abstract shapes. All stimuli were presented in a sequential matching-to-sample format using an automated joystick-testing paradigm. Subjects performed significantly better on upright than on inverted presentations of automobiles, rhesus monkey and capuchin faces, but not human faces or abstract shapes. These results are inconsistent with data from humans and chimpanzees that show the inversion effect only for categories of stimuli for which subjects have developed expertise. The inversion effect in rhesus monkeys does not appear to be face-specific, and should therefore not be used as a marker of specialized face processing in this species. Received: 18 November 1998 / Accepted after revision: 9 May 1999     

The Continuity Strategy,Human Behavior,and Behavior Analysis

The Psychological Record - In behavior analysis, continuity refers to the assumption of a similarity of behavioral principles or processes between nonhumans and humans, which is often considered to...     

Grey parrot numerical competence: a review

The extent to which humans and nonhumans share numerical competency is a matter of debate. Some researchers argue that nonhumans, lacking human language, possess only a simple understanding of small quantities, generally less than four. Animals that have, however, received some training in human communication systems might demonstrate abilities intermediate between those of untrained nonhumans and humans. Here I review data for a Grey parrot (Psittacus erithacus) that has been shown to quantify sets of up to and including six items (including heterogeneous subsets) using vocal English labels, to comprehend these labels fully, and to have a zero-like concept. Recent research demonstrates that he can also sum small quantities. His success shows that he understands number symbols as abstract representations of real-world collections, and that his sense of number compares favorably to that of chimpanzees and young human children.