Eye movements of stumptailed monkeys during discriminative performance: An overview

There are a number of statements that can be made about eye movements of monkeys during the learning of simple and complex discriminative problems that are probably applicable to a wide variety of visual tasks. There are systematic changes in eye movements as a function of practice. Some of these changes occur long after grosser measures of performance, such as frequency of correct choices, have reached an asymptote. Hence, short-term studies of visual information processing may be misleading. Duration of visual fixations and frequency of visual fixations are independent measures, reflecting different cognitive processes. Studies which measure only total looking time confound these two measures and, thus, may miss important information. Eye movements appear to be an important, if not essential, component of the chain of events constituting the cognitive processing underlying performance on visual tasks.     

Transfer of the Nonmatch-to-Goal rule in Monkeys across Cognitive Domains

To solve novel problems, it is advantageous to abstract relevant information from past experience to transfer on related problems. To study whether macaque monkeys were able to transfer an abstract rule across cognitive domains, we trained two monkeys on a nonmatch-to-goal (NMTG) task. In the object version of the task (O-NMTG), the monkeys were required to choose between two object-like stimuli, which differed either only in shape or in shape and color. For each choice, they were required to switch from their previously chosen object-goal to a different one. After they reached a performance level of over 90% correct on the O-NMTG task, the monkeys were tested for rule transfer on a spatial version of the task (S-NMTG). To receive a reward, the monkeys had to switch from their previously chosen location to a different one. In both the O-NMTG and S-NMTG tasks, there were four potential choices, presented in pairs from trial-to-trial. We found that both monkeys transferred successfully the NMTG rule within the first testing session, showing effective transfer of the learned rule between two cognitive domains.     

Follow the straggler: zebrafish use a simple heuristic for collective decision-making

Animal groups often make decisions sequentially, from the front to the back of the group. In such cases, individuals can use the choices made by earlier ranks, a form of social information, to inform their own choice. The optimal strategy for such decisions has been explored in models which differ on, for example, whether or not agents take into account the sequence of observed choices. The models demonstrate that choices made later in a sequence are more informative, but it is not clear if animals use this information or rely instead on simpler heuristics, such as quorum rules. We show that a simple rule ‘copy the last observed choice'', gives similar predictions to those of optimal models for most likely sequences. We trained groups of zebrafish to choose one arm of a Y-maze and used them to demonstrate various sequences to naive fish. We show that the naive fish appear to use a simple rule, most often copying the choice of the last demonstrator, which results in near-optimal choices at a fraction of the computational cost.     

Aging and Sensory Substitution in a Virtual Navigation Task

Virtual environments are becoming ubiquitous, and used in a variety of contexts–from entertainment to training and rehabilitation. Recently, technology for making them more accessible to blind or visually impaired users has been developed, by using sound to represent visual information. The ability of older individuals to interpret these cues has not yet been studied. In this experiment, we studied the effects of age and sensory modality (visual or auditory) on navigation through a virtual maze. We added a layer of complexity by conducting the experiment in a rotating room, in order to test the effect of the spatial bias induced by the rotation on performance. Results from 29 participants showed that with the auditory cues, it took participants a longer time to complete the mazes, they took a longer path length through the maze, they paused more, and had more collisions with the walls, compared to navigation with the visual cues. The older group took a longer time to complete the mazes, they paused more, and had more collisions with the walls, compared to the younger group. There was no effect of room rotation on the performance, nor were there any significant interactions among age, feedback modality and room rotation. We conclude that there is a decline in performance with age, and that while navigation with auditory cues is possible even at an old age, it presents more challenges than visual navigation.     

Neural correlates of knowledge: stable representation of stimulus associations across variations in behavioral performance

Behavioral responses to a sensory stimulus are often guided by associative memories. These associations remain intact even when other factors determine behavior. The substrates of associative memory should therefore be identifiable by neuronal responses that are independent of behavioral choices. We tested this hypothesis using a paired-associates task in which monkeys learned arbitrary associations between pairs of visual stimuli. We examined the activity of neurons in inferior temporal cortex as the animals prepared to choose a remembered stimulus from a visual display. The activity of some neurons (22%) depended on the monkey's behavioral choice; but for a novel class of neurons (54%), activity reflected the stimulus that the monkey was instructed to choose, regardless of the behavioral response. These neurons appear to represent memorized stimulus associations that are stable across variations in behavioral performance. In addition, many neurons (74%) were modulated by the spatial arrangement of the stimuli in the display.     

Impact of path parameters on maze solution time

In order to compare spatial attention and visual processing capabilities of humans and rhesus macaques, we developed a visual maze task both could perform. Maze stimuli were constructed of orthogonal line segments displayed on a monitor. Each was octagonal in outline and contained a central square (the 'start box'). A single ('main') path, containing a random number of turns, extended outward from the start box, and either reached an exit in the maze's perimeter, or a blind ending within the maze. Subjects maintained ocular fixation within the start box, and indicated their judgment whether the path reached an exit or not by depressing one of two keys (humans) or foot pedals (monkeys). Successful maze solution by human subjects required a minimum viewing time. Replacing the maze with a masking stimulus after a variable interval revealed that the percent correct performance increased systematically with greater viewing time, reaching a plateau of approximately 85% correct if mazes were visible for 500 ms or more. A multiple linear regression analysis determined that the response time of both species depended upon several parameters of the main path, including the number of turns, total length, and exist status. Human and nonhuman primates required comparable time to process each turn in the path, whereas monkeys were faster than humans in processing each unit of path length. The data suggest that a covert analysis of the maze proceeds from the center outward along the main path in the absence of saccadic eye movements, and that both monkeys and humans undertake such an analysis during the solution of visual mazes.     

Navigation Using Sensory Substitution in Real and Virtual Mazes

Under certain specific conditions people who are blind have a perception of space that is equivalent to that of sighted individuals. However, in most cases their spatial perception is impaired. Is this simply due to their current lack of access to visual information or does the lack of visual information throughout development prevent the proper integration of the neural systems underlying spatial cognition? Sensory Substitution devices (SSDs) can transfer visual information via other senses and provide a unique tool to examine this question. We hypothesize that the use of our SSD (The EyeCane: a device that translates distance information into sounds and vibrations) can enable blind people to attain a similar performance level as the sighted in a spatial navigation task. We gave fifty-six participants training with the EyeCane. They navigated in real life-size mazes using the EyeCane SSD and in virtual renditions of the same mazes using a virtual-EyeCane. The participants were divided into four groups according to visual experience: congenitally blind, low vision & late blind, blindfolded sighted and sighted visual controls. We found that with the EyeCane participants made fewer errors in the maze, had fewer collisions, and completed the maze in less time on the last session compared to the first. By the third session, participants improved to the point where individual trials were no longer significantly different from the initial performance of the sighted visual group in terms of errors, time and collision.     

Assessment of meaning and the detection of unreliable signals by vervet monkeys

Free-ranging vervet monkeys, Cercopithecus aethiops, who had learned to ignore playbacks of one type of call by an unreliable signaller subsequently also ignored playback of an acoustically different call by the same individual if the calls had similar referents. Such transfer did not occur if either the identity of the signaller changed or if the two calls had different referents. After repeatedly being played an intergroup call in the absence of other groups, vervets also ignored an acoustically different intergroup call given by the same individual. The monkeys did not transfer habituation, however, if the new call was given by a different individual. In tests where the referents of two calls were different, the monkeys also failed to transfer habituation across call types. Vervet monkeys who had learned to ignore an unreliable leopard alarm call did not later ignore an eagle alarm call, even when the signaller remained the same. Results suggest that vervets, like humans, process information at a semantic, and not just an acoustic, level.     

Capacity of working memory in rats as determined by performance on a radial maze

Capacity of the working memory was tested in 12 rats highly overtrained in the 12- and 24-arm radial mazes. Asymptotic performance levels were characterized by 1.01 and 2.78 errors/trial in the 12- and 24-arm mazes, respectively. The incidence of errors increased from 31% on the last choice in the 12-arm maze to 51% on choices 23 and 24 in the 24-arm maze, but remained significantly below the expected error probability of about 85%. Linear extrapolation of the above trend to mazes with more arms suggests working memory capacity of 40 to 50 items. When two trials in a 12-arm maze were repeated in immediate succession, error incidence increased from 1.17 in the first trial to 2.13 in the second trial. The tendency to avoid choice repetition could be observed in any string of 12 continuous choices, but was weakest in segments divided by trial boundary (2.48 errors in choices 7 to 18). With a different trial separation (choices 1–6 and 19–24 in maze A, choices 7–18 in an adjacent maze B) errors dropped to 1.09 in B but increased to 2.30 in A. It is concluded that radial maze performance reflects avoidance of choice repetition which is improved by recognition of trial boundaries and is adversely influenced by forgetting and interference.     

Learning large-scale spatial relationships in a maze and effects of MK-801 on retrieval in the rhesus monkey

Monkeys have strong abilities to remember the visual properties of potential food sources for survival in the nature. The present study demonstrated the first observations of rhesus monkeys learning to solve complex spatial mazes in which routes were guided by visual cues. Three monkeys were trained in a maze (6 m x 6 m) included of four different mazes. We recorded the cue and cup errors, latencies, and pathway for each trial. The data showed that monkeys learned the target place after three days in the first maze and spent a shorter time in learning the following mazes. The maze was an efficient method to measure the ability and proceeding of spatial memory in monkeys. Moreover, working memory can also be tested by using the maze. MK-801 at 0.02 mg/kg but not at 0.005 mg/kg impaired monkeys' retrieval of spatial memory after they learned all four mazes. The present maze may provide an efficient method to help bridging the gap in cognition between nonhuman primates and humans, and in particular to gain insight into human cognitive function and dysfunction.     

A weighted constraint satisfaction approach to human goal-directed decision making

When we plan for long-range goals, proximal information cannot be exploited in a blindly myopic way, as relevant future information must also be considered. But when a subgoal must be resolved first, irrelevant future information should not interfere with the processing of more proximal, subgoal-relevant information. We explore the idea that decision making in both situations relies on the flexible modulation of the degree to which different pieces of information under consideration are weighted, rather than explicitly decomposing a problem into smaller parts and solving each part independently. We asked participants to find the shortest goal-reaching paths in mazes and modeled their initial path choices as a noisy, weighted information integration process. In a base task where choosing the optimal initial path required weighting starting-point and goal-proximal factors equally, participants did take both constraints into account, with participants who made more accurate choices tending to exhibit more balanced weighting. The base task was then embedded as an initial subtask in a larger maze, where the same two factors constrained the optimal path to a subgoal, and the final goal position was irrelevant to the initial path choice. In this more complex task, participants’ choices reflected predominant consideration of the subgoal-relevant constraints, but also some influence of the initially-irrelevant final goal. More accurate participants placed much less weight on the optimality-irrelevant goal and again tended to weight the two initially-relevant constraints more equally. These findings suggest that humans may rely on a graded, task-sensitive weighting of multiple constraints to generate approximately optimal decision outcomes in both hierarchical and non-hierarchical goal-directed tasks.     

Spider monkey sleeping sites: Use and availability

The behavior of spider monkeys (Ateles geoffroyi) at sleeping sites and the characteristics of these sites were studied in Santa Rosa National Park, Costa Rica. The spider monkeys tended to congregate just prior to dusk at a number of sleeping sites which were repeatedly used (81.6%), but occasionally they slept in trees which were only used once (18.4%). All of the regularly used sleeping trees were not used concurrently, but rather, there was a rotation between sites. In general, males were not encountered at regularly used sleeping sites as often as other age/sex classes, and when they were in all male subgroups, they did not sleep in repeatedly used sites. The trees used as regular sleeping sites tended to be large, but such trees were common in the group's home range. The size of the subgroups attending repeatedly used sleeping trees was large when food was abundant and small when food was scarce. It is suggested that this relationship reflects that the costs of travelling to the sleeping site would be more easily recovered when food was abundant than when food was scarce.     

Monkeys recall and reproduce simple shapes from memory

If you draw from memory a picture of the front of your childhood home, you will have demonstrated recall. You could also recognize this house upon seeing it. Unlike recognition, recall demonstrates memory for things that are not present. Recall is necessary for planning and imagining, and it can increase the flexibility of navigation, social behavior, and other cognitive skills. Without recall, memory is more limited to recognition of the immediate environment. Amnesic patients are impaired on recall tests [1, 2], and recall performance often declines with aging [3]. Despite its importance, we know relatively little about nonhuman animals' ability to recall information; we lack suitable recall tests for them and depend instead on recognition tests to measure nonhuman memory. Here we report that rhesus monkeys can recall simple shapes from memory and reproduce them on a touchscreen. As in humans [4, 5], monkeys remembered less in recall than recognition tests, and their recall performance deteriorated more slowly. Transfer tests showed that monkeys used a flexible memory mechanism rather than memorizing specific actions for each shape. Observation of recall in Old World monkeys suggests that it has been adaptive for over 30 million years [6] and does not depend on language.     

Operant conditioning of rat navigation using electrical stimulation for directional cues and rewards

Operant conditioning is often used to train a desired behavior in an animal. The contingency between a specific behavior and a reward is required for successful training. Here, we compared the effectiveness of two different mazes for training turning behaviors in response to directional cues in Sprague-Dawley rats. Forty-three rats were implanted with electrodes into the medial forebrain bundle and the left and right somatosensory cortices for reward and cues. Among them, thirteen rats discriminated between the left and right somatosensory stimulations to obtain rewards. They were trained to learn ipsilateral turning response to the stimulation of the left or right somatosensory cortex in either the T-maze (Group T) or the maze (Group W). Performance was measured by the navigation speed in the mazes. Performances of rats in Group T were enhanced faster than those in Group W. A significant correlation between performances during training and performance in final testing was observed in Group T starting with the fifth training session while such a correlation was not observed in Group W until the tenth training session. The training mazes did not however affect the performances in the final test. These results suggest that a simple maze is better than a complicated maze for training animals to learn directions and direct cortical stimulation can be used as a cue for direction training.     

Gonadal hormones and sex differences in nonreproductive behaviors in rodents: organizational and activational influences

Sex differences in many nonreproductive behaviors have been described in rodents. Among the behaviors that are sexually dimorphic in the rat are activity, aggression, pain, and taste sensitivity, food intake and body weight regulation, the learning and retention of certain kinds of mazes, avoidance responses, taste aversion, and performance on certain schedules of reinforcement. Gonadal hormones seem to be responsible, in part, for sex differences in these behaviors, but their contribution varies greatly with the behavior in question. Frequently, these sexually dimorphic behaviors are influenced both by organizational and activational actions of sex hormones. In other instances (e.g., maze learning and the acquisition of shuttle-box avoidance responses) organizational influences predominate. And while there is no sexually dimorphic behavior surveyed that can be shown to be influenced only by activational effects, wheel-running activity is clearly more strongly subject to activational than to organizational effects of the gonadal hormones. In general, only rudimentary information exists regarding the temporal limits of the period in development when organizational influences on nonsexual behaviors occur. The suggestion can be made that organizational influences often occur outside of the critical period for differentiation of the neuroendocrine system regulating cyclic release of gonadotrophins. Even for behaviors where organizational effects usually occur during a roughly delimited period of development, data for other behavioral systems suggest that the time limits during which organizational effects can occur are not rigidly fixed. Very little information exists regarding biochemical or neural mechanisms by which organizational or activational effects on sexually dimorphic nonreproductive behaviors are expressed. It is important to recognize for many of the sexually dimorphic behaviors in the rat that differences between the sexes are neither large nor absolute. This is especially true of several kinds of learning situations where groups of males and females typically differ in average levels of performance. Ostensibly minor variations in test procedure can abolish or accentuate the average difference in performance between the sexes. We are a long way from an adequate understanding of what factors are important, but such information could be quite helpful in estimating whether sex differences in certain laboratory learning tasks have any adaptive significance.Sex differences in nonreproductive behaviors may be influenced by many factors other than hormonal status. This greatly complicates a comparative analysis, but such an analysis will ultimately be necessary. What limited data exist on rodents suggest that: (1) Sexually dimorphic responses in the rat are often not similarly differentiated in the hamster, the gerbil, or the mouse; and (2) major differences exist among rodent species in hormonal effects on such responses.Over the last decade it has become clear that the behavioral effects of deliberate neurological insult are not necessarily the same in male and female rats (or in one case, in rhesus monkeys). Sex differences in the behavioral effects of ventromedial hypothalamic, lateral hypothalamic, septal, and striatal lesions in the rat and of orbital prefrontal cortex lesions in the monkey have been described. While information regarding hormonal modulation of these differences in response to brain damage is very limited, available data suggest both organizational and activational effects of sex hormones may be involved. It is too early to tell where this line of research may ultimately lead, but rather striking sex differences in the incidence of certain neurological disorders in humans suggest that further research may have both practical and theoretical significance.     

From Cognitive Maps to Cognitive Graphs

We investigate the structure of spatial knowledge that spontaneously develops during free exploration of a novel environment. We present evidence that this structure is similar to a labeled graph: a network of topological connections between places, labeled with local metric information. In contrast to route knowledge, we find that the most frequent routes and detours to target locations had not been traveled during learning. Contrary to purely topological knowledge, participants typically traveled the shortest metric distance to a target, rather than topologically equivalent but longer paths. The results are consistent with the proposal that people learn a labeled graph of their environment.     

Can puzzle feeders be used as cognitive screening instruments? Differential performance of young and aged female monkeys on a puzzle feeder task

Conventional cognitive testing of monkeys is time‐consuming and involves single‐caging and food or water deprivation. Here we report a novel test of global cognitive performance that can be completed in a short time period without food/water or social restrictions. Nine mazes of increasing difficulty were developed using a standard puzzle feeder, and the maze‐solving performance of ten young and five aged female cynomolgus monkeys (Macaca fascicularis) was tested. The young monkeys solved maze configurations at higher levels of difficulty and solved the first level of difficulty more quickly than aged monkeys. This task discriminated performance by age in nonhuman primates as do more conventional forms of cognitive testing and indicates that this task may be a quick and easy assessment of global cognitive function. Am. J. Primatol. 49:195–202, 1999. © 1999 Wiley‐Liss, Inc.     

Cheek pouch use in relation to interspecific competition and predator risk for three guenon monkeys (Cercopithecus spp.)

Forest guenons (Cercopithecus spp.) are often found in polyspecific associations that may decrease predator risk while increasing interspecific competition for food. Cheek pouch use may mitigate interspecific competition and predator risk by reducing the time spent in areas of high competition/predator risk. I investigated these ideas in three forest guenons: Campbell’s monkey (Cercopithecus campbelli), spot-nosed monkey (C. petaurista), and Diana monkey (C. diana). I present 13 months of scan sample data from Taï Forest, Côte d’Ivoire, including 3,675, 3,330, and 5,689 records of cheek pouch distention, to quantify cheek pouch use, for Campbell’s, spot-nosed, and Diana monkeys, respectively. Cheek pouches are often used to hold fruit, so I first predicted that the most frugivorous species, Diana monkeys, would have the most cheek pouch distension. Spot-nosed monkeys ate the least amount of fruit over the study period and had the least distended cheek pouches, suggesting the importance of frugivory in relation to cheek pouch distension for this species. This was not a sufficient explanation for Campbell’s monkeys; Campbell’s ate fruit less than Diana monkeys, but had more distended cheek pouches, suggesting that cheek pouch use was not simply a reflection of high frugivory. From the interspecific competition hypothesis, I predicted that Campbell’s monkeys would have more distended cheek pouches than Diana and spot-nosed monkeys, and more distended cheek pouches when associated with Diana because Campbell’s monkeys have the highest potential for interspecific competition with dominant Diana monkeys. From the predator risk hypothesis, I predicted that Campbell’s would have more distended cheek pouches when not associated with highly vigilant Diana monkeys. Campbell’s monkeys had the most distended cheek pouches overall, but had more distended cheek pouches when not in association with Diana, suggesting the greater importance of predator risk rather than interspecific competition in Campbell’s cheek pouch use.     

Choosing hunting sites with little information: patch-choice responses of crab spiders to distant cues

Adult female crab spiders (Misumena valid) released in a meadowmoved to milkweed stems more often than to other sites and alsomoved to flowering milkweed stems more often than to equallyavailable nonflowering ones. Preferences of the spiders as apopulation were similar during initial and second trials, butgiven individuals did not repeat their initial choices moreoften than predicted by chance. Thus, spiders probably respondeddirectly to cues present, rather than to information retainedfrom earlier experience. Spiders placed at the base of floweringmilkweed stems did not choose these sites more often than predictedby chance or more often than did spiders released in the grass,suggesting that this increase in localization provided no additionalinformation for choosing a hunting site. However, spiders placedat the bases of nonflowering stems selected them less oftenthan predicted. Second trials with these spiders also resembledinitial trials, but, as with the spiders released in the grass,given individuals did not repeat their initial performance moreoften than predicted. Thus, spiders released in the grass probablyresponded directly to cues present, as did spiders releasedat the base of stems. The choices of these spiders, combinedwith flexible giving-up times, caused the spiders to be concentratedon flowering stems. Although this strategy results in a better-than-randompattern of selecting hunting sites, the spiders lose considerableforaging time in the process.     

Latent learning,shortcuts and detours: a computational model

Voicu and Schmajuk (Rob. Auto. Syst. 35 (2001a) 23) described a model of spatial navigation and exploration that includes an action system capable of guiding, with the help of a cognitive system, the search for specific goals as determined by a motivation system. Whereas in the original model the cognitive map stores information about the connectivity between places in the environment, in the present version the cognitive map also stores information about the paths traversed by the agent. Computer simulations show that the network correctly describes experimental results including latent learning in a maze, detours in a maze, and shortcuts in an open field. In addition, the model generates novel predictions about detours and shortcuts in an open field.