"Effects on executive function following damage to the prefrontal cortex in the rhesus monkey (Macaca mulatta)": Correction to Moore et al (2009).

Reports an error in "Effects on executive function following damage to the prefrontal cortex in the rhesus monkey (Macaca mulatta)" by Tara L. Moore, Stephen P. Schettler, Ronald J. Killiany, Douglas L. Rosene and Mark B. Moss (Behavioral Neuroscience, 2009[Apr], Vol 123[2], 231-241). There was an error in the first sentence of the third full paragraph in the text on p. 235. The sentence should read “Based on the lesion reconstructions it was determined, as intended, that all monkeys had complete damage to areas 46, 8a, 8b, 9 and slight damage to area 10.” (The following abstract of the original article appeared in record 2009-04037-001.) Executive function is a term used to describe the cognitive processes subserved by the prefrontal cortex (PFC). An extensive body of work has characterized the effects of damage to the PFC in nonhuman primates, but it has focused primarily on the capacity of recognition and working memory. One limitation in studies of the functional parcellation of the PFC has been the absence of tests that assess executive function or its functional components. The current study used an adaptation of the Wisconsin Card Sorting Test, a classic test of frontal lobe and executive function in humans, to assess the effects of bilateral lesions in the dorsolateral PFC on executive function in the rhesus monkey (Macaca mulatta). The authors used the category set-shifting task, which requires the monkey to establish a pattern of responding to a specific category (color or shape) based on reward contingency, maintain that pattern of responding, and then shift to responding to a different category when the reward contingency changes. Rhesus monkeys with lesions of the dorsolateral PFC were impaired in abstraction, establishing a response pattern to a specific category and maintaining and shifting that response pattern on the category set-shifting task. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Prefrontal cortex and rule abstraction: Where and whether? Theoretical comment on Moore et al. (2009).

The primate dorsolateral prefrontal cortex is implicated in diverse aspects of behavioral regulation, cognitive control, and memory. However, direct neuropsychological evidence supporting a requirement of this area in functions other than spatial working memory has been scarce. T. L. Moore, S. P. Schettler, R. J. Killiany, D. L. Rosene, and M. B. Moss (see record 2009-04037-001) have shown, for the first time, that lesions of dorsolateral prefrontal cortex in the rhesus monkey (including areas 9 and 46) substantially impair performance in a test of executive function modeled on the Wisconsin Card Sorting Task. The pattern of impairment is consistent with a role for dorsolateral prefrontal areas in rule abstraction but may relate to a role for this area in rule maintenance as well. Interestingly, monkeys with dorsolateral prefrontal lesions do not appear to perseverate in their use of particular rules in the task, different from the common impairment associated with frontal lobe damage in humans. These findings indicate that dorsolateral prefrontal cortex is necessary for some aspects of rule-guided behavior in the primate brain and help illuminate the involvement of different prefrontal areas in different aspects of executive function and rule-guided behavior. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The role of ventral and orbital prefrontal cortex in conditional visuomotor learning and strategy use in rhesus monkeys (Macaca mulatta).

[Correction Notice: An erratum for this article was reported in Vol 115(6) of Behavioral Neuroscience (see record 2007-17010-001). In Figure 1 (p. 974), the extent of the intended lesions in the sections 32 and 28 mm from the interaural plane was misprinted. The correctly printed figure is shown in the erratum.] Four rhesus monkeys (Macaca mulatta) were trained to learn novel sets of visuomotor associations in 50 trials or less, within single test sessions. After bilateral ablation of the orbital and ventral prefrontal cortex, the monkeys lost the ability to learn these associations within a session, although they could learn them when given several daily sessions. Thus, relatively slow, across-session visuomotor learning depends on neither the ventral nor orbital prefrontal cortex, but rapid, within-session learning does. The ablations also eliminated at least 2 response strategies, repeat-stay and lose-shift, which might account, in part, for the deficit in rapid learning. The deficit is unlikely to result from a failure of visual discriminative ability or working memory: The monkeys could discriminate similar stimulus material within a session, and reducing the working memory load did not improve within-session learning. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

How much does number matter to a monkey (Macaca mulatta)?

Although many animal species can represent numerical values, little is known about how salient number is relative to other object properties for nonhuman animals. In one hypothesis, researchers propose that animals represent number only as a last resort, when no other properties differentiate stimuli. An alternative hypothesis is that animals automatically, spontaneously, and routinely represent the numerical attributes of their environments. The authors compared the influence of number versus that of shape, color, and surface area on rhesus monkeys' (Macaca mulatta) decisions by testing them on a matching task with more than one correct answer: a numerical match and a nonnumerical (color, surface area, or shape) match. The authors also tested whether previous laboratory experience with numerical discrimination influenced a monkey's propensity to represent number. Contrary to the last-resort hypothesis, all monkeys based their decisions on numerical value when the numerical ratio was favorable. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Impairment of executive function induced by hypertension in the Rhesus monkey (Macaca mulatta).

The effects of chronic, untreated hypertension on executive function were investigated in a nonhuman primate model of hypertensive cerebrovascular disease. Executive function was assessed with the Conceptual Set-Shifting Task (CSST), a task adapted from the human Wisconsin Card Sorting Test (WCST). Like the WCST, the CSST requires abstraction of a stimulus set, followed by a series of set shifts. Performance on the CSST by 7 young adult monkeys (Macaca mulatta) with surgically induced hypertension was compared with that of 6 normotensive monkeys. The hypertensive group was significantly impaired relative to the normotensive group in abstraction and set shifting. Although the neural basis of this impairment is unclear, evidence from studies with humans and monkeys suggests that the prefrontal cortex may be the locus for this effect of hypertension. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Implicit and explicit category learning by macaques (Macaca mulatta) and humans (Homo sapiens).

An influential theoretical perspective differentiates in humans an explicit, rule-based system of category learning from an implicit system that slowly associates different regions of perceptual space with different response outputs. This perspective was extended for the 1st time to the category learning of nonhuman primates. Humans (Homo sapiens) and macaques (Macaca mulatta) learned categories composed of sine-wave gratings that varied across trials in bar width and bar orientation. The categories had either a single-dimensional, rule-based solution or a two-dimensional, information-integration solution. Humans strongly dimensionalized the stimuli and learned the rule-based task far more quickly. Six macaques showed the same performance advantage in the rule-based task. In humans, rule-based category learning is linked to explicit cognition, consciousness, and declarative reports about the contents of cognition. These results demonstrate an empirical continuity between human and nonhuman primate cognition, suggesting that nonhuman primates may have some structural components of humans’ capacity for explicit cognition. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Stages of category learning in monkeys (Macaca mulatta) and humans (Homo sapiens).

Smith and Minda (1998) and Blair and Homa (2001) studied the time course of category learning in humans. They distinguished an early, abstraction-based stage of category learning from a later stage that incorporated a capacity for categorizing exceptional category members. The present authors asked whether similar processing stages characterize the category learning of nonhuman primates. Humans (Homo sapiens) and monkeys (Macaca mulatta) participated in category-learning tasks that extended Blair and Homa’s paradigm comparatively. Early in learning, both species improved on typical items more than on exception items, indicating an initial mastery of the categories’ general structure. Later in learning, both species selectively improved their exception-item performance, indicating exception-item resolution or exemplar memorization. An initial stage of abstraction-based category learning may characterize categorization across a substantial range of the order Primates. This default strategy may have an adaptive resonance with the family resemblance organization of many natural-kind categories. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Gaze following and joint attention in rhesus monkeys (Macaca mulatta).

Gaze and attention direction provide important sources of social information for primates. Behavioral studies show that chimpanzees spontaneously follow human gaze direction. By contrast, non-ape species such as macaques fail to follow gaze cues. The authors investigated the reactions of rhesus macaques (Macaca mulatta) to attention cues of conspecifics. Two subjects were presented with videotaped images of a stimulus monkey with its attention directed to 1 of 2 identical objects. Analysis of eye movements revealed that both subjects inspected the target (object or position attended by the stimulus monkey) more often than the distractor (nonattended object or position). These results provide evidence that rhesus monkeys follow gaze and use the attention cues of other monkeys to orient their own attention to objects. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The comparative psychology of same-different judgments by humans (Homo sapiens) and monkeys (Macaca mulatta).

The authors compared the performance of humans and monkeys in a Same-Different task. They evaluated the hypothesis that for humans the Same-Different concept is qualitative, categorical, and rule-based, so that humans distinguish 0-disparity pairs (i.e., same) from pairs with any discernible disparity (i.e., different); whereas for monkeys the Same-Different concept is quantitative, continuous, and similarity-based, so that monkeys distinguish small-disparity pairs (i.e., similar) from pairs with a large disparity (i.e., dissimilar). The results supported the hypothesis. Monkeys, more than humans, showed a gradual transition from same to different categories and an inclusive criterion for responding Same. The results have implications for comparing Same-Different performances across species--different species may not always construe or perform even identical tasks in the same way. In particular, humans may especially apply qualitative, rule-based frameworks to cognitive tasks like Same-Different. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Bilateral neurotoxic amygdala lesions in rhesus monkeys (Macaca mulatta): Consistent pattern of behavior across different social contexts.

[Correction Notice: An erratum for this article was reported in Vol 122(4) of Behavioral Neuroscience (see record 2008-09788-025). In the aforementioned article, Table 1 on page 256 was incorrect. The correct table is printed in the erratum.] Although the amygdala has been repeatedly implicated in normal primate social behavior, great variability exists in the specific social and nonsocial behavioral changes observed in nonhuman primates with bilateral amygdala lesions. One plausible explanation pertains to differences in social context. This study measured the social behavior of amygdala-lesioned and unoperated rhesus monkeys (Macaca mulatta) in 2 contexts. Monkeys interacted in 4-member social groups over 32 test days. They were previously assessed in pairs (N. J. Emery et al., 2001) and were therefore familiar with each other at the beginning of this study. Across the 2 contexts, amygdala lesions produced a highly consistent pattern of social behavior. Operated monkeys engaged in more affiliative social interactions with control partners than did controls. In the course of their interactions, amygdala-lesioned monkeys also displayed an earlier decrease in nervous and fearful personality qualities than did controls. The increased exploration and sexual behavior recorded for amygdala-lesioned monkeys in pairs was not found in the 4-member groups. The authors concluded that the amygdala contributes to social inhibition and that this function transcends various social contexts. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Trajectory-selective neuronal activity in the motor cortex of rhesus monkeys (Macaca mulatta).

Neuronal activity recorded in the primate motor cortex reflected movement parameters in addition to the distance and direction of a target. These neurons may reflect the selection, from memory, of a detailed movement trajectory to be executed in response to visuospatial instructions. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

"The role of ventral and orbital prefrontal cortex in conditional visuomotor learning and strategy use in rhesus monkeys (Macaca mulatto)": Correction to Bussey et al (2001).

Reports an error in "The role of ventral and orbital prefrontal cortex in conditional visuomotor learning and strategy use in rhesus monkeys (Macaca mulatta)." by Timothy J. Bussey, Steven P. Wise and Elisabeth A. Murray (Behavioral Neuroscience, 2001[Oct], Vol 115[5], 971-982). In Figure 1 (p. 974), the extent of the intended lesions in the sections 32 and 28 mm from the interaural plane was misprinted. The correctly printed figure is shown in the erratum. (The following abstract of the original article appeared in record 2001-18882-001.) Four rhesus monkeys (Macaca mulatta) were trained to learn novel sets of visuomotor associations in 50 trials or less, within single test sessions. After bilateral ablation of the orbital and ventral prefrontal cortex, the monkeys lost the ability to learn these associations within a session, although they could learn them when given several daily sessions. Thus, relatively slow, across-session visuomotor learning depends on neither the ventral nor orbital prefrontal cortex, but rapid, within-session learning does. The ablations also eliminated at least 2 response strategies, repeat-stay and lose-shift, which might account, in part, for the deficit in rapid learning. The deficit is unlikely to result from a failure of visual discriminative ability or working memory: The monkeys could discriminate similar stimulus material within a session, and reducing the working memory load did not improve within-session learning. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Rhinal cortex ablations fail to disrupt reinforcer devaluation effects in rhesus monkeys (Macaca mulatta).

Studies have shown that excitotoxic lesions of the amygdala attenuate reinforcer devaluation effects in monkeys and rats. Because the rhinal (i.e., entorhinal and perirhinal) cortex has prominent reciprocal connections with the amygdala and has been suggested to store knowledge about objects, it is possible that it too composes part of the critical circuitry subserving learning about objects and their associated reinforcement value. To test this possibility, rhesus monkeys with rhinal cortex removals as well as unoperated controls were tested using a reinforcer devaluation procedure. Monkeys with rhinal cortex removals and controls, unlike those with amygdala lesions, tended to avoid displacing objects overlying a devalued food. These results indicate that the rhinal cortex is not a critical part of the neural circuitry mediating the effects of reinforcer devaluation. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Detection of directed gaze in rhesus monkeys (Macaca mulatta).

To examine the ability of monkeys to detect the direction of attention of other individuals, the authors quantitatively investigated the visual scanning pattern of rhesus monkeys (Macaca mulatta) in response to visually presented images of a human frontal face. The present results demonstrated not only that monkeys predominantly gaze at the eyes as compared with other facial areas in terms of duration and number of fixations, but also that they gaze at the eyes for a longer time period and more frequently when a human face, presented as a stimulus, gazed at them than when the gaze was shifted. These results indicate that rhesus monkeys are sensitive to the directed gaze of humans, suggesting that monkeys pay more attention to the human whose attention is directed to them. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

"Bilateral neurotoxic amygdala lesions in rhesus monkeys (Macaca mulatta): Consistent pattern of behavior across different social contexts": Correction.

Reports an error in "Bilateral neurotoxic amygdala lesions in rhesus monkeys (Macaca mulatta): Consistent pattern of behavior across different social contexts" by Christopher J. Machado, Nathan J. Emery, John P. Capitanio, William A. Mason, Sally P. Mendoza and David G. Amaral (Behavioral Neuroscience, 2008[Apr], Vol 122[2], 251-266). In the aforementioned article, Table 1 on page 256 was incorrect. The correct table is printed in the erratum. (The following abstract of the original article appeared in record 2008-03769-001.) Although the amygdala has been repeatedly implicated in normal primate social behavior, great variability exists in the specific social and nonsocial behavioral changes observed in nonhuman primates with bilateral amygdala lesions. One plausible explanation pertains to differences in social context. This study measured the social behavior of amygdala-lesioned and unoperated rhesus monkeys (Macaca mulatta) in 2 contexts. Monkeys interacted in 4-member social groups over 32 test days. They were previously assessed in pairs (N. J. Emery et al., 2001) and were therefore familiar with each other at the beginning of this study. Across the 2 contexts, amygdala lesions produced a highly consistent pattern of social behavior. Operated monkeys engaged in more affiliative social interactions with control partners than did controls. In the course of their interactions, amygdala-lesioned monkeys also displayed an earlier decrease in nervous and fearful personality qualities than did controls. The increased exploration and sexual behavior recorded for amygdala-lesioned monkeys in pairs was not found in the 4-member groups. The authors concluded that the amygdala contributes to social inhibition and that this function transcends various social contexts. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Visual discrimination and reversal learning in the aged monkey (Macaca mulatta).

Visual discrimination and reversal learning were assessed in young adult (10–12 yrs old, n?=?4) and aged (23–27 yrs old, n?=?5) female rhesus monkeys. Performance was comparable across age groups in many tasks, suggesting that the acquisition of stimulus–reward associations remains largely intact in the aged monkey. Most older Ss, however, required more training than any young animal to learn an initial pattern discrimination. In combination with previous findings (P. R. Rapp and D. G. Amaral; 1989) from the same groups of monkeys, these data suggest that deficits in attending to the relevant stimulus features in novel testing procedures may contribute to poor performance in aged Ss across a variety of learning and memory tasks. In addition, preliminary findings from a discrimination probe procedure raise the possibility that aged Ss may adopt alternate testing strategies that compensate for some aspects of age-dependent cognitive dysfunction. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Prospective memory in the formation of learning sets by rhesus monkeys (Macaca mulatta).

In conventional discrimination learning-set formation, it is possible that rhesus monkeys (Macaca mulatta) learn to lay down prospective memories by anticipating the next trial and deciding in advance what choice will be made. To test this hypothesis, the authors administered discrimination problems with 24-hr intertrial intervals, predicting that these long intervals would disrupt or prevent the putative anticipation of the next trial. Confirming their expectation, the authors found no indication of learning-set formation under these conditions. (PsycINFO Database Record (c) 2011 APA, all rights reserved)     

Effects of selective neonatal temporal lobe lesions on socioemotional behavior in infant rhesus monkeys (Macaca mulatta).

Normal infant monkeys and infant monkeys with neonatal damage to either the medial temporal lobe or the inferior temporal visual area were assessed in dyadic social interactions at 2 and 6 months of age. Unlike the normal infant monkeys, which developed strong affiliative bonds and little or no behavioral disturbances, the lesioned monkeys (each of which was observed with an unoperated control) exhibited socioemotional abnormalities and aberrant behaviors. The socioemotional changes predominated at 6 months of age and were particularly severe in monkeys with medial temporal lesions. In both the pattern and time course, the socioemotional deficits produced by the neonatal medial temporal lesions bear a striking resemblance to the behavioral syndrome in children with autism. Further analysis of these lesion-induced abnormalities in nonhuman primates may therefore provide insight into this debilitating human developmental disorder. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The impact of selective amygdala, orbital frontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta).

Social dominance, personality ratings, and frequency, duration, and timing of social behaviors were measured pre- and postsurgically in 6 groups of rhesus monkeys (Macaca mulatta), each consisting of 1 sham-operated control and 1 monkey each with a selective amygdala, hippocampal, or orbital frontal cortex lesion. Unlike previous reports, none of the operated groups showed changes in social dominance postsurgery, although changes in other measures varied by lesion site. Although sham-operated monkeys displayed heightened avoidant, anxious, and aggressive behaviors, those with hippocampal lesions also showed increased exploration and excitability, along with reduced responses to affiliative signals. Amygdala lesions yielded several personality changes that precluded positive social interactions (increased exploration and excitability, decreased affiliation and popularity) and altered responses to threatening social signals. By contrast, monkeys with orbital frontal lesions were involved in more aggressive interactions and responded differently to both affiliative and threatening signals. Although several findings differ from earlier nonhuman primate studies, they are largely in agreement with human data and emphasize the context-specific nature of social behavior studies. Interpretation of results in relation to cognitive processes mediated by each structure is discussed. (PsycINFO Database Record (c) 2010 APA, all rights reserved)