Rhesus monkeys see who they hear: spontaneous cross-modal memory for familiar conspecifics

Rhesus monkeys gather much of their knowledge of the social world through visual input and may preferentially represent this knowledge in the visual modality. Recognition of familiar faces is clearly advantageous, and the flexibility and utility of primate social memory would be greatly enhanced if visual memories could be accessed cross-modally either by visual or auditory stimulation. Such cross-modal access to visual memory would facilitate flexible retrieval of the knowledge necessary for adaptive social behavior. We tested whether rhesus monkeys have cross-modal access to visual memory for familiar conspecifics using a delayed matching-to-sample procedure. Monkeys learned visual matching of video clips of familiar individuals to photographs of those individuals, and generalized performance to novel videos. In crossmodal probe trials, coo-calls were played during the memory interval. The calls were either from the monkey just seen in the sample video clip or from a different familiar monkey. Even though the monkeys were trained exclusively in visual matching, the calls influenced choice by causing an increase in the proportion of errors to the picture of the monkey whose voice was heard on incongruent trials. This result demonstrates spontaneous cross-modal recognition. It also shows that viewing videos of familiar monkeys activates naturally formed memories of real monkeys, validating the use of video stimuli in studies of social cognition in monkeys.     

Late DNA replication in rhesus monkey (Macaca mulatta) chromosomes

A study of the pattern of late DNA replication in rhesus monkey chromosomes showed evident similarities with man. This must be a consequence of the evolutionary conservation of replication patterns in primate chromosomes, as it has been demonstrated in the great apes, in Cebus, and man. However, the pattern of late replication of the allocyclic X chromosome in lymphocytes of female rhesus monkey was identical with the fibroblast pattern in man, and with the pattern found in only 5 to 20% of human lymphocytes.     

Recognition of monkey faces by monkey experts

Human beings automatically discriminate human faces at the individual level. Infants aged 3 months implicitly recognise monkey faces, but this capacity disappears as recognition skills mature. Expertise is known to affect recognition capacities for different categories of stimuli that are not even face-like in their configuration. We have explored the capacity of adult experts and non-experts in primatology to recognise monkey faces in both explicit and implicit recognition tasks. In the explicit task, where subjects received the instruction to recognise a face seen previously, experts proved to be more accurate than non-experts. Experts were more affected by inversion than non-experts, suggesting that the processing of those faces is based on their configuration, as is generally observed for human faces. This replicates findings from Diamond and Carey (J Exp Psychol Gen 115:107–117, 1986) in dog experts. In the implicit recognition task, assessed by a visual paired comparison task where no instruction of recognition was given, automatic discrimination was observed for human faces but not for monkey faces. These results suggest that experience acquired by the time of adulthood did not lead the experts to develop recognition skills to the point of matching those exhibited for human faces.     

Visual artificial grammar learning: comparative research on humans, kea (Nestor notabilis) and pigeons (Columba livia)

Artificial grammar learning (AGL) provides a useful tool for exploring rule learning strategies linked to general purpose pattern perception. To be able to directly compare performance of humans with other species with different memory capacities, we developed an AGL task in the visual domain. Presenting entire visual patterns simultaneously instead of sequentially minimizes the amount of required working memory. This approach allowed us to evaluate performance levels of two bird species, kea (Nestor notabilis) and pigeons (Columba livia), in direct comparison to human participants. After being trained to discriminate between two types of visual patterns generated by rules at different levels of computational complexity and presented on a computer screen, birds and humans received further training with a series of novel stimuli that followed the same rules, but differed in various visual features from the training stimuli. Most avian and all human subjects continued to perform well above chance during this initial generalization phase, suggesting that they were able to generalize learned rules to novel stimuli. However, detailed testing with stimuli that violated the intended rules regarding the exact number of stimulus elements indicates that neither bird species was able to successfully acquire the intended pattern rule. Our data suggest that, in contrast to humans, these birds were unable to master a simple rule above the finite-state level, even with simultaneous item presentation and despite intensive training.     

Ensembles of human MTL neurons "jump back in time" in response to a repeated stimulus

Episodic memory, which depends critically on the integrity of the medial temporal lobe (MTL), has been described as "mental time travel" in which the rememberer "jumps back in time." The neural mechanism underlying this ability remains elusive. Mathematical and computational models of performance in episodic memory tasks provide a specific hypothesis regarding the computation that supports such a jump back in time. The models suggest that a representation of temporal context, a representation that changes gradually over macroscopic periods of time, is the cue for episodic recall. According to these models, a jump back in time corresponds to a stimulus recovering a prior state of temporal context. In vivo single-neuron recordings were taken from the human MTL while epilepsy patients distinguished novel from repeated images in a continuous recognition memory task. The firing pattern of the ensemble of MTL neurons showed robust temporal autocorrelation over macroscopic periods of time during performance of the memory task. The gradually-changing part of the ensemble state was causally affected by the visual stimulus being presented. Critically, repetition of a stimulus caused the ensemble to elicit a pattern of activity that resembled the pattern of activity present before the initial presentation of the stimulus. These findings confirm a direct prediction of this class of temporal context models and may be a signature of the mechanism that underlies the experience of episodic memory as mental time travel. ? 2012 Wiley Periodicals, Inc.     

Event-related potentials to faces: the effects of priming and recognition

Short-term visual memory, as in both implicit priming and explicit recognition tasks, can be demonstrated by decreased reaction times, the ability to preferentially select previously presented objects from lists and the ability to more readily complete previously exposed words from fragmented letters. The visual processing of faces occurs separately from the visual processing of non-face stimuli, within discrete areas of bilateral posterior inferotemporal cortices. While visual recognition and memory of faces are independent of those for non-faces, their processing appears to be similar. We have demonstrated an electrophysiologic correlate of short-term visual memory in a face-matching paradigm. We have observed a series of evoked potential components consisting predominantly of a C140, C180 and C240 with a posterior, bitemporal distribution. The priming effect is reflected by a diminution of C240 amplitude in the response to repeated pictures of faces compared to novel pictures of faces. These data reflect a previously unreported set of neurophysiological observations on short-term visual memory for faces.     

Comparative reactivity of human IgE to cynomolgus monkey and human effector cells and effects on IgE effector cell potency

Background: Due to genetic similarities with humans, primates of the macaque genus such as the cynomolgus monkey are often chosen as models for toxicology studies of antibody therapies. IgE therapeutics in development depend upon engagement with the FcεRI and FcεRII receptors on immune effector cells for their function. Only limited knowledge of the primate IgE immune system is available to inform the choice of models for mechanistic and safety evaluations.   Methods: The recognition of human IgE by peripheral blood lymphocytes from cynomolgus monkey and man was compared. We used effector cells from each species in ex vivo affinity, dose-response, antibody-receptor dissociation and potency assays. Results: We report cross-reactivity of human IgE Fc with cynomolgus monkey cells, and comparable binding kinetics to peripheral blood lymphocytes from both species. In competition and dissociation assays, however, human IgE dissociated faster from cynomolgus monkey compared with human effector cells. Differences in association and dissociation kinetics were reflected in effector cell potency assays of IgE-mediated target cell killing, with higher concentrations of human IgE needed to elicit effector response in the cynomolgus monkey system. Additionally, human IgE binding on immune effector cells yielded significantly different cytokine release profiles in each species. Conclusion: These data suggest that human IgE binds with different characteristics to human and cynomolgus monkey IgE effector cells. This is likely to affect the potency of IgE effector functions in these two species, and so has relevance for the selection of biologically-relevant model systems when designing pre-clinical toxicology and functional studies.     

Comparative reactivity of human IgE to cynomolgus monkey and human effector cells and effects on IgE effector cell potency

Background: Due to genetic similarities with humans, primates of the macaque genus such as the cynomolgus monkey are often chosen as models for toxicology studies of antibody therapies. IgE therapeutics in development depend upon engagement with the FcεRI and FcεRII receptors on immune effector cells for their function. Only limited knowledge of the primate IgE immune system is available to inform the choice of models for mechanistic and safety evaluations.

Methods: The recognition of human IgE by peripheral blood lymphocytes from cynomolgus monkey and man was compared. We used effector cells from each species in ex vivo affinity, dose-response, antibody-receptor dissociation and potency assays.

Results: We report cross-reactivity of human IgE Fc with cynomolgus monkey cells, and comparable binding kinetics to peripheral blood lymphocytes from both species. In competition and dissociation assays, however, human IgE dissociated faster from cynomolgus monkey compared with human effector cells. Differences in association and dissociation kinetics were reflected in effector cell potency assays of IgE-mediated target cell killing, with higher concentrations of human IgE needed to elicit effector response in the cynomolgus monkey system. Additionally, human IgE binding on immune effector cells yielded significantly different cytokine release profiles in each species.

Conclusion: These data suggest that human IgE binds with different characteristics to human and cynomolgus monkey IgE effector cells. This is likely to affect the potency of IgE effector functions in these two species, and so has relevance for the selection of biologically-relevant model systems when designing pre-clinical toxicology and functional studies.     

Nonvisual motor training influences biological motion perception

Experimental evidence suggests a link between perception and the execution of actions . In particular, it has been proposed that motor programs might directly influence visual action perception . According to this hypothesis, the acquisition of novel motor behaviors should improve their visual recognition, even in the absence of visual learning. We tested this prediction by using a new experimental paradigm that dissociates visual and motor learning during the acquisition of novel motor patterns. The visual recognition of gait patterns from point-light stimuli was assessed before and after nonvisual motor training. During this training, subjects were blindfolded and learned a novel coordinated upper-body movement based only on verbal and haptic feedback. The learned movement matched one of the visual test patterns. Despite the absence of visual stimulation during training, we observed a selective improvement of the visual recognition performance for the learned movement. Furthermore, visual recognition performance after training correlated strongly with the accuracy of the execution of the learned motor pattern. These results prove, for the first time, that motor learning has a direct and highly selective influence on visual action recognition that is not mediated by visual learning.     

人手指柔性触觉感知的记忆特性

触觉再现技术是当前虚拟现实和远程操作机器人领域的前沿,而柔性触觉则是其重要的研究内容。触觉再现接口的设计需要充分研究人手的触觉感知特性。本文在柔性触觉装置上研究了人手指柔性触觉记忆特性。先通过回忆性实验确定人手指的柔性触觉记忆容量,在记忆容量范围内又进行了再认性实验,对人手指的柔性触觉记忆反应时间进行分析。本实验方法简单有效,得出的结论不仅可以用来改进触觉再现装置的设计,而且为触觉再现技术的研究提供了生理学依据。     

Maternal recognition of individual infant squirrel monkeys from isolation call playbacks

Responses of six squirrel monkey (Saimiri sciureus) mothers to playback of a single call type, the “isolation peep,” made by their own infants were tested after mothers and infants had been separated for more than a week. The playback tapes were edited from tapes containing mixed vocal material recorded when infants and mothers could see but not touch each other. Mothers showed recognition of their own infants compared to other familiar infants by increases in four measures of proximity to the speaker. These data provide evidence that maternal recognition of infants by means of acoustic cues is possible when the test stimuli consist of examples of a single call type with demonstrated individuality.     

The development of face expertise

Recent neuroimaging studies in adults indicate that visual areas selective for recognition of faces can be recruited through expertise for nonface objects. This reflects a new emphasis on experience in theories of visual specialization. In addition, novel work infers differences between categories of nonface objects, allowing a re-interpretation of differences seen between recognition of faces and objects. Whether there are experience-independent precursors of face expertise remains unclear; indeed, parallels between literature for infants and adults suggest that methodological issues need to be addressed before strong conclusions can be drawn regarding the origins of face recognition.     

When and how well can human‐socialized capuchins match actions demonstrated by a familiar human?

Capuchin monkeys have provided uneven evidence of matching actions they observe others perform. In accord with theories emphasizing the attentional salience of object movement and spatial relationships, we predicted that human-reared monkeys would better match events in which a human demonstrator moved an object into a new relation with another object or surface than other kinds of actions. Three human-reared capuchins were invited repeatedly by a familiar human to perform a fixed set of actions upon objects or upon their bodies, using the "Do as I do" procedure. Actions directed at the body were matched less reliably than actions involving objects, and actions were matched best when the monkey looked at the demonstration for at least 2 sec and performed its action within a few seconds after the demonstration. The most commonly matched actions were those that one monkey performed relatively often when the experiment began. One monkey partially reproduced three novel actions (out of 48 demonstrations), all three involving moving or placing objects, and two of which it also performed following other demonstrations. These findings contribute convergent evidence that capuchin monkeys display social facilitation of activity, enhanced interest in particular objects and emulation of spatial outcomes. This pattern can support the development of shared manipulative skills, as evident in traditions of foraging and tool use in natural settings. The findings do not suggest that human rearing substantively altered capuchins' ability or interest in matching the actions of a familiar human, although visual attention to the human demonstrator may have been greater in these monkeys than in normally reared monkeys.     

Research progress on Drosophila visual cognition in China

Visual cognition,as one of the fundamental aspects of cognitive neuroscience,is generally associated with high-order brain functions in animals and human.Drosophila,as a model organism,shares certain features of visual cognition in common with mammals at the genetic,molecular,cellular,and even higher behavioral levels.From learning and memory to decision making,Drosophila covers a broad spectrum of higher cognitive behaviors beyond what we had expected.Armed with powerful tools of genetic manipulation in Drosophila,an increasing number of studies have been conducted in order to elucidate the neural circuit mechanisms underlying these cognitive behaviors from a genes-brain-behavior perspective.The goal of this review is to integrate the most important studies on visual cognition in Drosophila carried out in mainland China during the last decade into a body of knowledge encompassing both the basic neural operations and circuitry of higher brain function in Drosophila.Here,we consider a series of the higher cognitive behaviors beyond learning and memory,such as visual pattern recognition,feature and context generalization,different feature memory traces,salience-based decision,attention-like behavior,and cross-modal leaning and memory.We discuss the possible general gain-gating mechanism implementing by dopamine-mushroom body circuit in fly's visual cognition.We hope that our brief review on this aspect will inspire further study on visual cognition in flies,or even beyond.     

Serum insulin-like growth factor 1 concentrations in the developing rhesus monkey.

We studied the developmental pattern of serum IGF-1 concentrations in the rhesus monkey in cross-sectional and longitudinal manners. Values were lower in infants with a significant rise at the onset of puberty. Females values were lower than males except for pregnant females. There was a correlation of IGF-1 values with body weight in the males. Longitudinal study of six animals proved this age dependence of IGF-1 values. The rhesus monkey has a pattern of serum IGF-1 concentrations similar to that of the human being.     

Zur Informationsverarbeitung im visuellen System der Wirbeltiere. I

Summary In this paper it is tried to find a mathematical model for a number of mainly electrophysiological results concerning pattern recognition of mammals. The interpretations are essentially based on the experiments of Hubel and Wiesel in the visual system of the cat and the monkey.After a short introduction to the applied theory of linear nervous nets the investigations in the retina are interpreted. This part of the visual system can be considered as a bandpass-filter for space dependent oscillations. At the level of the geniculate body, a further filtering takes place which especially attenuates the low and the very high frequencies.The processes in the cortex regions 17, 18 and 19, where the further preprocessing of the pattern recognition takes place, can be interpreted by the theory of matched filters. In Area 17 the input pattern is reduced to the contour lines. In the two other areas the extraction of simple characteristic features such as line ends and corners takes place. By means of the present results it is not possible to draw complete conclusions on the structure of the recognition process.     

Visual recognition of age class and preference for infantile features: implications for species-specific vs universal cognitive traits in primates

Despite not knowing the exact age of individuals, humans can estimate their rough age using age-related physical features. Nonhuman primates show some age-related physical features; however, the cognitive traits underlying their recognition of age class have not been revealed. Here, we tested the ability of two species of Old World monkey, Japanese macaques (JM) and Campbell's monkeys (CM), to spontaneously discriminate age classes using visual paired comparison (VPC) tasks based on the two distinct categories of infant and adult images. First, VPCs were conducted in JM subjects using conspecific JM stimuli. When analyzing the side of the first look, JM subjects significantly looked more often at novel images. Based on analyses of total looking durations, JM subjects looked at a novel infant image longer than they looked at a familiar adult image, suggesting the ability to spontaneously discriminate between the two age classes and a preference for infant over adult images. Next, VPCs were tested in CM subjects using heterospecific JM stimuli. CM subjects showed no difference in the side of their first look, but looked at infant JM images longer than they looked at adult images; the fact that CMs were totally na?ve to JMs suggested that the attractiveness of infant images transcends species differences. This is the first report of visual age class recognition and a preference for infant over adult images in nonhuman primates. Our results suggest not only species-specific processing for age class recognition but also the evolutionary origins of the instinctive human perception of baby cuteness schema, proposed by the ethologist Konrad Lorenz.     

The Role of Anterior Nuclei of the Thalamus: A Subcortical Gate in Memory Processing: An Intracerebral Recording Study

Objective

To study the involvement of the anterior nuclei of the thalamus (ANT) as compared to the involvement of the hippocampus in the processes of encoding and recognition during visual and verbal memory tasks.

Methods

We studied intracerebral recordings in patients with pharmacoresistent epilepsy who underwent deep brain stimulation (DBS) of the ANT with depth electrodes implanted bilaterally in the ANT and compared the results with epilepsy surgery candidates with depth electrodes implanted bilaterally in the hippocampus. We recorded the event-related potentials (ERPs) elicited by the visual and verbal memory encoding and recognition tasks.

Results

P300-like potentials were recorded in the hippocampus by visual and verbal memory encoding and recognition tasks and in the ANT by the visual encoding and visual and verbal recognition tasks. No significant ERPs were recorded during the verbal encoding task in the ANT. In the visual and verbal recognition tasks, the P300-like potentials in the ANT preceded the P300-like potentials in the hippocampus.

Conclusions

The ANT is a structure in the memory pathway that processes memory information before the hippocampus. We suggest that the ANT has a specific role in memory processes, especially memory recognition, and that memory disturbance should be considered in patients with ANT-DBS and in patients with ANT lesions.ANT is well positioned to serve as a subcortical gate for memory processing in cortical structures.     

Neuronal mechanisms for visual stability: progress and problems

How our vision remains stable in spite of the interruptions produced by saccadic eye movements has been a repeatedly revisited perceptual puzzle. The major hypothesis is that a corollary discharge (CD) or efference copy signal provides information that the eye has moved, and this information is used to compensate for the motion. There has been progress in the search for neuronal correlates of such a CD in the monkey brain, the best animal model of the human visual system. In this article, we briefly summarize the evidence for a CD pathway to frontal cortex, and then consider four questions on the relation of neuronal mechanisms in the monkey brain to stable visual perception. First, how can we determine whether the neuronal activity is related to stable visual perception? Second, is the activity a possible neuronal correlate of the proposed transsaccadic memory hypothesis of visual stability? Third, are the neuronal mechanisms modified by visual attention and does our perceived visual stability actually result from neuronal mechanisms related primarily to the central visual field? Fourth, does the pathway from superior colliculus through the pulvinar nucleus to visual cortex contribute to visual stability through suppression of the visual blur produced by saccades?     

In search for significant cognitive features in Klinefelter syndrome through cross-species comparison of a supernumerary X chromosome

The behavioral characterization of animals that carry genetic disorder abnormalities in a controlled genetic and environmental background may be used to identify human deficits that are significant to understand underlying neurobiological mechanisms. Here, we studied whether previously reported object recognition impairments in mice with a supernumerary X chromosome relate to specific cognitive deficits in Klinefelter syndrome (47,XXY). We aimed to optimize face validity by studying temporal object recognition in human cognitive assays. Thirty-four boys with Klinefelter syndrome (mean age 12.01) were compared with 90 age-matched normal controls, on a broad range of visual object memory tasks, including tests for pattern and temporal order discrimination. The results indicate that subjects with Klinefelter syndrome have difficulty in the processing of visual object and pattern information. Visual object patterns seem difficult to discriminate especially when temporal information needs to be processed and reproduced. On the basis of cross-species comparison, we propose that impaired temporal processing of object pattern information is an important deficit in Klinefelter syndrome. The current study shows how cross-species behavioral characterization may be used as a starting point to understand the neurobiology of syndromal phenotypic expression. The features of this study may serve as markers for interventions in Klinefelter syndrome. Similar cross-species evaluations of standard mouse behavioral paradigms in different genetic contexts may be powerful tools to optimize genotype-phenotype relationships.