Effects of category learning on the stimulus selectivity of macaque inferior temporal neurons

Primates can learn to categorize complex shapes, but as yet it is unclear how this categorization learning affects the representation of shape in visual cortex. Previous studies that have examined the effect of categorization learning on shape representation in the macaque inferior temporal (IT) cortex have produced diverse and conflicting results that are difficult to interpret owing to inadequacies in design. The present study overcomes these issues by recording IT responses before and after categorization learning. We used parameterized shapes that varied along two shape dimensions. Monkeys were extensively trained to categorize the shapes along one of the two dimensions. Unlike previous studies, our paradigm counterbalanced the relevant categorization dimension across animals. We found that categorization learning increased selectivity specifically for the category-relevant stimulus dimension (i.e., an expanded representation of the trained dimension), and that the ratio of within-category response similarities to between-category response similarities increased for the relevant dimension (i.e., category tuning). These small effects were only evident when the learned category-related effects were disentangled from the prelearned stimulus selectivity. These results suggest that shape-categorization learning can induce minor category-related changes in the shape tuning of IT neurons in adults, suggesting that learned, category-related changes in neuronal response mainly occur downstream from IT.     

Even simple forms of social learning rely on intention attribution in marmoset monkeys (Callithrix jacchus)

Intention attribution guides the cognitively most demanding forms of social learning, such as imitation, thereby scaffolding cumulative cultural evolution. However, it is not thought to be necessary for more basic forms of social learning. Here we present evidence that in marmoset monkeys (Callithrix jacchus) even most basic forms of social learning such as enhancement depend on intention attribution. Marmosets perceived the behavior of a conspecific and a conspecific-like robot, but not that of a moving black box, as goal directed. Their subsequent choice behavior was shaped by social facilitation and stimulus enhancement, that is, by very simple forms of social learning, but only when exposed to the conspecific and robot, which they previously had perceived as intentional agents. We discuss the implications of this finding for contemporary debates about social learning, including emulation learning and ghost control studies, the necessity of goal-directed copying for cumulative cultural evolution, and the limits of current classification systems of social learning for the evolution of social and asocial learning.     

Behavioral test systems in marmoset monkeys

A number of neurobehavioral methods have been developed to test behavior in marmoset monkeys. These test systems are (1) the bungalow test, which quantifies spontaneous explorative behavior, (2) the hand-eye coordination test, which tests a learned task of coordinated motor behavior, and (3) the fear-potentiated startle response, which tests and quantifies pathological anxiety manifested by a response of fright. The test systems are extensively discussed, and the value of these test systems is exemplified by applying them to neurological disorders to register disease activity and drug efficacy.     

Developmental and cross-situational stability in infant pigtailed macaque temperament

We assessed developmental stability and context generalizability of temperament in pigtailed macaques (Macaca nemestrina) from the University of Washington Infant Primate Research Lab. A principal components analysis condensed 6 behavioral measures into 2 components, interpreted as reactivity and boldness. Changes in these measures over the 1st 10 months of development showed a trend toward calmer and bolder behavior with age, with significant individual variation in the pattern of change. Boldness showed a quadratic pattern of change, whereas reactivity decreased linearly. We also studied the relationship between temperament and response to a novelty probe. The magnitude of the response to the novelty probe decreased slightly over time, and boldness and reactivity in a familiar setting did not predict these changes in response to novelty. In a 2nd principal components analysis, reactivity to novelty represented a distinct aspect of temperament. Our results demonstrate developmental changes and context dependency in macaque behavior.     

Strategies in landmark use by children, adults, and marmoset monkeys

Common marmosets (Callithrix jacchus jacchus), human children, and human adults learned to find a goal that was located in the center of a square array of four identical landmarks. The location of the landmark array and corresponding goal varied across trials, so the task could not be solved without using the landmark array. In Experiment 1, a matrix of discrete goal locations was presented and the landmarks surrounded and were adjacent to the correct location during training. After training, an expansion test was given in which the distance between landmarks was increased. Marmosets, children (ages 5–9), and adults all readily learned to use the landmarks to search accurately during training. On the expansion test, adults uniformly searched in the center of the array. Monkeys and children concentrated their searching near the landmarks rather than in the center. The monkeys, but not the children, searched more often on the directionally appropriate side of the landmarks than on other sides of the landmarks. In Experiment 2, children (ages 3–5) were trained with a continuous search space and with the goal farther from the landmarks so that a beaconing strategy rule could not be used. Several of the children failed to acquire the training task. Of those who learned to find the goal, three searched in the middle on expansion tests but most searched nearer to the landmarks. The “middle rule” strategy that is uniformly used by adult humans does not appear to be a preferred strategy for children or non-human primates.     

A continuous smooth map of space in the primary visual cortex of the common marmoset

We examined the fine-scale mapping of the visual world within the primary visual cortex of the marmoset monkey (Callithrix jacchus) using differential optical imaging. We stimulated two sets of complementary stripe-like locations in turn, subtracting them to generate the cortical representations of continuous bands of visual space. Rotating this stimulus configuration makes it possible to map different spatial axes within the primary visual cortex. In a similar manner, shifting the stimulated locations between trials makes it possible to map retinotopy at an even finer scale. Using these methods we found no evidence of any local anisotropies or distortions in the cortical representation of visual space. This is despite the fact that orientation preference is mapped in a discontinuous manner across the surface of marmoset V1. Overall, our results indicate that space is mapped in a continuous and smooth manner in the primary visual cortex of the common marmoset.     

Spatial relational memory in 9-month-old macaque monkeys

This experiment assesses spatial and nonspatial relational memory in freely moving 9-mo-old and adult (11-13-yr-old) macaque monkeys (Macaca mulatta). We tested the use of proximal landmarks, two different objects placed at the center of an open-field arena, as conditional cues allowing monkeys to predict the location of food rewards hidden in one of two sets of three distinct locations. Monkeys were tested in two different conditions: (1) when local visual cues marked the two sets of potentially baited locations, so that monkeys could use both local and spatial information to discriminate these locations from never-baited locations; and (2) when no local visual cues marked the two sets of potentially baited locations, so that monkeys had to rely on a spatial relational representation of the environment to discriminate these locations. No 9-mo-old or adult monkey associated the presence of the proximal landmarks, at the center of the arena, with the presence of food in one set of three distinct locations. All monkeys, however, discriminated the potentially baited locations in the presence of local visual cues, thus providing evidence of visual discrimination learning. More importantly, all 9-mo-old monkeys tested discriminated the potentially baited locations in absence of the local visual cues, thus exhibiting evidence of spatial relational learning. These findings indicate that spatial memory processes characterized by a relational representation of the environment are present as early as 9 mo of age in macaque monkeys.     

Tolerant macaque species are less impulsive and reactive

Animal Cognition - Inhibitory control, the inhibition of impulsive behaviours, is believed to be key in navigating a complex social environment. Species characterised by higher social tolerance,...     

Schedule-induced drinking as functions of interpellet interval and draught size in the Java macaque

Three Java monkeys received food pellets that were assigned by both ascending and descending series of fixed-time schedules whose values varied between 8 and 256 seconds. The draught size dispensed by a concurrently available water-delivery tube was systematically varied between 1.0 and 0.3 milliliter per lick at various fixed-time values during the second and third series determinations. Session water intake was bitonically related to the interpellet interval and was determined by the interaction of (1) the probability of initiating a drinking bout, which fell off at the highest interpellet intervals and, (2) the size of the bout, which increased directly with increases in interpellet interval. Variations in draught size had little effect on total session intakes, but reduced bout size at draught sizes of 0.5 milliliter and below. Thus, a volume-regulation process of schedule-induced drinking operated generally at the session-intake level, but was limited to higher draught sizes at the bout level.     

Category learning in the color-word contingency learning paradigm

In the typical color-word contingency learning paradigm, participants respond to the print color of words where each word is presented most often in one color. Learning is indicated by faster and more accurate responses when a word is presented in its usual color, relative to another color. To eliminate the possibility that this effect is driven exclusively by the familiarity of item-specific word-color pairings, we examine whether contingency learning effects can be observed also when colors are related to categories of words rather than to individual words. To this end, the reported experiments used three categories of words (animals, verbs, and professions) that were each predictive of one color. Importantly, each individual word was presented only once, thus eliminating individual color-word contingencies. Nevertheless, for the first time, a category-based contingency effect was observed, with faster and more accurate responses when a category item was presented in the color in which most of the other items of that category were presented. This finding helps to constrain episodic learning models and sets the stage for new research on category-based contingency learning.     

Implicit visual learning and the expression of learning

Although the existence of implicit motor learning is now widely accepted, the findings concerning perceptual implicit learning are ambiguous. Some researchers have observed perceptual learning whereas other authors have not. The review of the literature provides different reasons to explain this ambiguous picture, such as differences in the underlying learning processes, selective attention, or differences in the difficulty to express this knowledge. In three experiments, we investigated implicit visual learning within the original serial reaction time task. We used different response devices (keyboard vs. mouse) in order to manipulate selective attention towards response dimensions. Results showed that visual and motor sequence learning differed in terms of RT-benefits, but not in terms of the amount of knowledge assessed after training. Furthermore, visual sequence learning was modulated by selective attention. However, the findings of all three experiments suggest that selective attention did not alter implicit but rather explicit learning processes.     

Role or dominance in macaque response to novel objects

Forty-four juvenile rhesus, 30 stumptailed, and 6 pigtailed monkeys were tested individually and in stable quadrads for time to contact slightly and highly novel objects. When peer-group tested, dominant monkeys were the first to contact the slightly novel but not the highly novel objects, unlike preferences found when they were tested individually. A role analysis revealed better contact-order prediction, most groups having their habitual first contactor. When this contactor was overtly punished or covertly trained to avoid the object, group response was altered. The use of the termrole is discussed in detail, concluding that a role involves a particular individual who is expected to interact with others while in certain groups to complete some beneficial function.     

Matching and oddity learning in the pigeon: Transfer effects and the absence of relational learning

Three experiments examined the extent to which pigeons trained on a matching or oddity discrimination with one pair of colours showed transfer when tested on a new matching or oddity discrimination with a new pair of colours. Experiment 1 examined the effects of key spacing and a delay procedure and replicated previous reports that in the transfer stage subjects given the same kind of problem (Non-shift condition) in general learn more rapidly than those given the opposite problem (Shift condition). However, this difference appeared only when pigeons given matching in both training and transfer stages were compared to those shifted from oddity to matching; it did not appear in birds transferred to oddity. Transfer was not significantly affected by key spacing or by the delay.

Experiments 2 and 3 examined transfer from a non-relational conditional discrimination based on one set of colours to a subsequent matching or oddity task based on two new colours. Both a comparison between the results of Experiment 1 and 2 and the corresponding within-experiment comparison from Experiment 3 showed that transfer from conditional training to matching was as great as from prior training on matching, while prior training on oddity produced negative transfer on shift to matching. It was suggested that this negative transfer occurs because pigeons trained on oddity have not learned to override an initial bias towards the odd stimulus in an array. Whatever the correct explanation; the present results provide no support for the claim that pigeons solve matching or oddity discriminations relationally.     

Diagnosticity and prototypicality in category learning: a comparison of inference learning and classification learning

Category knowledge allows for both the determination of category membership and an understanding of what the members of a category are like. Diagnostic information is used to determine category membership; prototypical information reflects the most likely features given category membership. Two experiments examined 2 means of category learning, classification and inference learning, in terms of sensitivity to diagnostic and prototypical information. Classification learners were highly sensitive to diagnostic features but not sensitive to nondiagnostic, but prototypical, features. Inference learners were less sensitive to the diagnostic features than were classification learners and were also sensitive to the nondiagnostic, prototypical, features. Discussion focuses on aspects of the 2 learning tasks that might lead to this differential sensitivity and the implications for learning real-world categories.     

An analysis of immediate serial recall performance in a macaque

There has been considerable research into the ability of nonhuman primates to process sequential information, a topic that is of interest in part because of the extensive involvement of sequence processing in human language use. Surprisingly, no previous study has unambiguously tested the ability of nonhuman primates to encode and immediately reproduce a novel temporal sequence of perceptual events, the ability tapped in the immediate serial recall (ISR) task extensively studied in humans. We report here the performance of a rhesus macaque on a spatial ISR task, closely resembling tasks widely used in human memory research. Detailed analysis of the monkey’s recall performance indicates a number of important parallels with human ISR, consistent with the idea that a single mechanism for short-term serial order memory may be shared across species.