Visual Paired Comparison Task Research Articles

Portable eyetracking-based assessment of memory decline

ABSTRACTIntroduction: Preferential viewing of novel stimuli in the Visual Paired Comparison task has provided a useful marker of memory and medial temporal lobe function. We created a portable version of the VPC (P-VPC) and contrasted P-VPC metrics against the Montreal Cognitive Assessment (MoCA) in healthy adults, to assess the validity and reliability of the P-VPC as an indicator of memory function across age. A supplementary case series was conducted with individuals diagnosed with Alzheimer’s disease (AD) and other dementias, to provide a preliminary illustration of the P-VPC’s use as a measure in clinical populations.Method: Participants (n = 207) were tested using the P-VPC. Individuals were familiarized with a set of objects, which were each presented alongside a novel object in the test phase. Novelty viewing scores were compared to MoCA scores to index concurrent validity. Item analyses were conducted as a test of internal reliability of the P-VPC. A complementary clinical case series was conducted with AD (n = 4) and dementia (n = 5) participants, who were tested using the P-VPC and further compared to healthy age-matched participants.Results: Preferential viewing decreased with age in healthy participants, and was positively correlated with MoCA scores. Compared to the MoCA, P-VPC scores did not differ based on education and/or whether English was spoken as the native language. Item analyses revealed acceptable internal consistency. P-VPC viewing percentiles of healthy participants were modeled as a function of age, and illustrated that individuals of the clinical case series diagnosed with AD scored in below-average percentiles, while those with dementia did not score below-average.Conclusion: Good concurrent validity and acceptable internal reliability were observed, and P-VPC scores were not confounded by education or language experience. Low performance was observed in individuals with clinically diagnosed AD, suggesting that the P-VPC may be a potential tool for screening memory decline.

Intact perceptual ability, but impaired familiarity judgment, after neonatal perirhinal lesions in rhesus macaques

The perirhinal cortex is known to support high-level perceptual abilities as well as familiarity judgments that may affect recognition memory. We tested whether poor perceptual abilities or a loss of familiarity judgment contributed to the recognition memory impairments reported earlier in monkeys with PRh lesions received in infancy (Neo-PRh) (Weiss and Bachevalier, 2016; Zeamer et al., 2015). Perceptual abilities were assessed using a version of the Visual Paired Comparison task with black&white (B&W) stimuli, and familiarity judgments were assessed using the Constant Negative task requiring repeated familiarization exposures. Adult monkeys with Neo-PRh lesions were able to recognize B&W stimuli after short delays, suggesting that their perceptual abilities were within the range of control animals. However, the same Neo-PRh monkeys were slower to acquire the Constant Negative task, requiring more exposures to objects before judging them as familiar compared to control animals. Taken together, the data help to account for the differential patterns of functional compensation on previously reported recognition tasks following neonatal versus adult-onset PRh lesions, and provide further support to the view that the PRh is involved in familiarity processes.

Visual recognition memory is impaired in rhesus monkeys repeatedly exposed to sevoflurane in infancy

BackgroundExperimental studies in animals have shown that exposure to general anaesthesia in infancy can cause loss of cells in the central nervous system and long-term impairments in neurocognitive function. Some human epidemiological studies have shown increased risk of learning disability after repeated anaesthesia exposure in early childhood. Thus, we investigated in a highly translational rhesus monkey model, whether repeated exposure in infancy to the inhalation anaesthetic sevoflurane is associated with impaired visual recognition memory during the first two yr of life. MethodsRhesus monkeys of both sexes were exposed to sevoflurane inhalation anaesthesia on approximately postnatal day 7 and then again 14 and 28 days later, for four h each time. Visual recognition memory was tested using the visual paired comparison task, which measures memory by assessing preference for looking at a new image over a previously-viewed image. Monkeys were tested at 6–10 months of age, again at 12–18 months of age, and again at 24–30 months of age. ResultsNo memory impairment was detected at 6–10 months old, but significant impairment (reduced time looking at the novel image) was observed at 12–18 and 24–30 months old. ConclusionsRepeated exposure of infant rhesus monkeys to sevoflurane results in visual recognition memory impairment that emerges after the first yr of life. This is consistent with epidemiological studies that show increased risk of learning disability after repeated exposure to anaesthesia in infancy/early childhood. Moreover, these deficits may emerge at later developmental stages, even when memory performance is unaffected earlier in development.

Evidence for face pareidolia in rhesus monkeys.

In everyday life we have a tendency to see faces in non-face objects; a famous example is the face of a nondescript man on the surface of mars. Although these misperceptions are often very compelling, it is not known whether "face pareidolia" is unique to humans or whether it is an experience shared with other animals. Like humans, rhesus monkeys have a functionally defined face-processing system, comprised of multiple interconnected areas distributed along the ventral visual pathway. In this study, we reasoned that the potential analogy between this system and our own made it likely that rhesus monkeys also experience face pareidolia. To test this hypothesis, we first collected 15 examples of face pareidolia from the public domain together with objects matched for object-content. An additional 15 photographs were taken of unfamiliar rhesus monkey faces. All possible pairs of these 45 images were shown to 5 male rhesus monkeys, one at a time for 4 seconds, in a visual paired comparison task. We collected two dependent variables (the total amount of time spent looking at each image; first fixation in each trial). In addition to replicating the common observation that rhesus monkeys look longer at face stimuli than other kinds of objects, we also found clear evidence that monkeys look for longer periods of time (and first) at examples of face pareidolia than at object-matched control images. We repeated this experiment with the images inverted and collected independent data from human participants (N = 10) who were asked to rate how face-like each image was on a 200-point scale. Overall, our results indicate that monkeys also see face configurations in non-face objects and, as such, provide the first compelling evidence of face pareidolia in any species other than our own. Meeting abstract presented at VSS 2017

Preference for Averageness in Faces Does Not Generalize to Non-Human Primates.

Facial attractiveness is a long-standing topic of active study in both neuroscience and social science, motivated by its positive social consequences. Over the past few decades, it has been established that averageness is a major factor influencing judgments of facial attractiveness in humans. Non-human primates share similar social behaviors as well as neural mechanisms related to face processing with humans. However, it is unknown whether monkeys, like humans, also find particular faces attractive and, if so, which kind of facial traits they prefer. To address these questions, we investigated the effect of averageness on preferences for faces in monkeys. We tested three adult male rhesus macaques using a visual paired comparison (VPC) task, in which they viewed pairs of faces (both individual faces, or one individual face and one average face); viewing time was used as a measure of preference. We did find that monkeys looked longer at certain individual faces than others. However, unlike humans, monkeys did not prefer the average face over individual faces. In fact, the more the individual face differed from the average face, the longer the monkeys looked at it, indicating that the average face likely plays a role in face recognition rather than in judgments of facial attractiveness: in models of face recognition, the average face operates as the norm against which individual faces are compared and recognized. Taken together, our study suggests that the preference for averageness in faces does not generalize to non-human primates.

Evolutionary Relevance and Experience Contribute to Face Discrimination in Infant Macaques (Macaca mulatta)

In human children and adults, familiar face types—typically own-age and own-species faces—are discriminated better than other face types; however, human infants do not appear to exhibit an own-age bias but instead better discriminate adult faces, which they see more often. There are two possible explanations for this pattern: Perceptual attunement predicts advantages in discrimination for the most experienced face types. Additionally or alternatively, there may be an experience-independent bias for infants to discriminate own-species faces, an adaptation for evolutionarily relevant faces. These possibilities have not been disentangled in studies thus far, and these studies did not control infants’ early experiences with faces. In the present study, we tested these predictions in infant macaques (Macaca mulatta) reared under controlled environments, not exposed to adult conspecifics. We measured newborns’ (15–25 days; n = 27) and 6- to 7-month-olds’ (n = 35) discrimination of human and macaque faces at 3 ages—young infants, old infants, and adults—in a visual paired comparison task. We found that 6- to 7-month-olds were the best at discriminating adult macaque faces; however, in the first few seconds of looking, tthey additionally discriminated familiar face types—same-aged peer and adult human faces—thereby highlighting the importance of experience with certain face categories. The present data suggest that macaque infants possess both experience-independent and experientially tuned face biases. In human infants, early face skills may likewise be driven by both experience and evolutionary relevance; future studies should consider both of these factors.

Memory for complex visual objects but not for allocentric locations during the first year of life

Although human infants demonstrate early competence to retain visual information, memory capacities during infancy remain largely undocumented. In three experiments, we used a Visual Paired Comparison (VPC) task to examine abilities to encode identity (Experiment 1) and spatial properties (Experiments 2a and 2b) of unfamiliar complex visual patterns during the first year of life. In the first experiment, 6- and 9-month-old infants were familiarized with visual arrays composed of four abstract patterns arranged in a square configuration. Recognition memory was evaluated by presenting infants with the familiarized array paired with a novel array composed of four new patterns. The second couple of experiments aimed to examine infant ability to encode the spatial relationships between each pattern of the array (e.g., where is A in the square configuration). The 6-, 9- and 12-month-old infants were tested on a spatial version of the VPC task, in which the novel array was composed of the same patterns than the familiarized array but arranged differently within the square configuration. Results indicated that infants retained the identity of the patterns but not their specific spatial relationships within the square configuration (i.e., allocentric location of the patterns), suggesting either an immaturity of the processes involved in object-to-location binding, or the inappropriateness of unfamiliar complex objects to reveal such early allocentric abilities.

Central complex and mushroom bodies mediate novelty choice behavior in Drosophila

Novelty choice, a visual paired-comparison task, for the fly Drosophila melanogaster is studied with severely restrained single animals in a flight simulator. The virtual environment simulates free flight for rotation in the horizontal plane. The behavior has three functional components: visual azimuth orientation, working memory, and pattern discrimination (perception). Here we study novelty choice in relation to its neural substrate in the brain and show that it requires the central complex and, in particular, the ring neurons of the ellipsoid body. Surprisingly, it also involves the mushroom bodies which are needed specifically in the comparison of patterns of different sizes.

The development of object recognition memory in rhesus macaques with neonatal lesions of the perirhinal cortex

To investigate the role of the perirhinal cortex on the development of recognition measured by the visual paired-comparison (VPC) task, infant monkeys with neonatal perirhinal lesions and sham-operated controls were tested at 1.5, 6, 18, and 48 months of age on the VPC task with color stimuli and intermixed delays of 10 s, 30 s, 60 s, and 120 s. Monkeys with neonatal perirhinal lesions showed an increase in novelty preference between 1.5 and 6 months of age similar to controls, although at these two ages, performance remained significantly poorer than that of control animals. With age, performance in animals with neonatal perirhinal lesions deteriorated as compared to that of controls. In contrast to the lack of novelty preference in monkeys with perirhinal lesions acquired in adulthood, novelty preference in the neonatally operated animals remained above chance at all delays and all ages. The data suggest that, although incidental recognition memory processes can be supported by the perirhinal cortex in early infancy, other temporal cortical areas may support these processes in the absence of a functional perirhinal cortex early in development. The neural substrates mediating incidental recognition memory processes appear to be more widespread in early infancy than in adulthood.

The influence of context on recognition memory in monkeys: Effects of hippocampal, parahippocampal and perirhinal lesions

This study further investigated the specific contributions of the medial temporal lobe structures to contextual recognition memory. Monkeys (Macaca mulatta) with either neurotoxic lesions of the hippocampus, aspiration lesions of the perirhinal cortex and parahippocampal areas TH/TF, or sham operations were tested on five conditions of a visual-paired comparison (VPC) task in which 3-dimensional objects were presented over multicolored backgrounds. In two conditions (Conditions 1 and 2: Context-changes), the sample object was presented on a new background during the retention tests, whereas in the three others (Conditions 3–5: No-context-changes) the sample object was presented over its familiar background. Novelty preference scores of control animals were weaker, but still significantly different from chance, in the Context-changes conditions than on the No-context-changes conditions. Animals in the three experimental groups showed strong preference for novelty on the No-context-change conditions, but weaker novelty preference on the Context-change conditions than controls. Thus, animals in all three lesion types had greater difficulty recognizing an object when its background was different from that used during encoding. The data are consistent with the view that the hippocampal formation, areas TH/TF, and perirhinal cortex contribute interactively to contextual memory processes.

Infant's visual preferences for facial traits associated with adult attractiveness judgements: Data from eye-tracking

Human preferences for facial attractiveness appear to emerge at an early stage during infant development. A number of studies have demonstrated that infants display a robust preference for facial attractiveness, preferring to look at physically attractive faces versus less attractive faces as judged by adults. However, to-date, relatively little is known about which traits of the face infants use to base these preferences upon. In contrast, a large number of studies conducted with human adults have identified that preference for attractive faces can be attributed to a number of specific facial traits. The purpose of the experiments here was to measure and assess infant's visual preference via eye-tracker technology for faces manipulated for one of three traits known to effect attractiveness judgments in adult preference tests: symmetry, averageness, and sexually dimorphic traits. Sixty-four infants (28 female and 36 male) aged between 12 and 24 months old each completed a visual paired comparison (VPC) task for one of the three facial dimensions investigated. Data indicated that infants displayed a significant visual preference for facial symmetry analogous to those preferences displayed by adults. Infants also displayed a significant visual preference for feminine versions of faces, in line with some studies of adult preferences. Visual preferences for facial non-averageness, or distinctiveness were also seen, a pattern opposite to that seen in adults. These findings demonstrate that infant's appreciation for facial attractiveness in adult images between the ages of 12 and 24 months of age is based on some, but not all, traits that adults find attractive.

Three-year-olds’ memory for a person met only once at the age of 12months: Very long-term memory revealed by a late-manifesting novelty preference

This study examined three-year-olds' verbal and non-verbal memory for a person met only once after a 28 month interval. Children in the Test group (N=50) had participated in an earlier experiment at our lab at the age of 12 months where they met one of two possible experimenters. At this past event half of the children were tested by one, the other half by the other experimenter. At the follow-up, run by a naïve experimenter, the children were shown two videos from the original experiment in a visual paired comparison task: One with the specific experimenter testing them at the original visit (the Target) and one of the other experimenter (the Foil), with whom they had no experience. When explicitly asked, the children's responses did not differ from chance. However, eye-tracking data revealed a late-manifesting novelty preference for the "Foil" person indicating memory for the "Target" person met once before.

Concurrent validity of Dubois' five-word-test compared with CERAD memory subtests

Background: We have recently demonstrated the use of an innovative and sensitive behavioral assay, the Visual Paired Comparison (VPC) task, to successfully predict the transition from healthy aging to mild cognitive impairment (MCI), and fromMCI to Alzheimer’s disease (AD) (Zola, et al., 2013). For a subset of subjects, however, predictability is less clear (gray zone). We report here that the application of Machine Learning algorithms and eye movement characteristics can significantly improve the predictive ability of the task for this subset of individuals. Methods: The VPC task measures how individuals view side-by-side novel and familiar images. Normal individuals typically look at the novel image about two-thirds of the viewing time. Previous work has relied on a single parameter, i.e., percent time viewing the novel image (novelty preference, NP). In the present study we used a Machine Learning-based approach that uses additional variables, namely, distribution of NP across multiple trials, and latent factor decompositionbased analysis of eye movement trajectories, to develop amore accurate prediction algorithm. Results: For subjects in the gray zone, NP alone is not sufficient to distinguish between the subjects who will convert to MCI/AD and those who will not, resulting in ROC AUC of 0.70. Our new approach achieves AUC of 0.87, which represents a 24% relative improvement in predictive ability for the subjects in the gray zone. Conclusions: The VPC task can offer early detection of impending cognitive decline as much as 3 years prior to clinical diagnosis. To our knowledge, this is the first behavioral task that can identify healthy subjects who will soon develop MCI and possibly progress to AD within the next few years. For individuals in the gray zone, Machine Learning approaches can enhance still further the predictive capabilities of the VPC task. Finally, when combinedwith biomarker assays, this approachmay provide a newway of interrogating the underlying dynamics of AD, as well as other illnesses in which impaired cognition is a leading symptom.

Long-term effects of neonatal hippocampal lesions on novelty preference in monkeys.

In a recent longitudinal study to assess the development of incidental recognition memory processes in monkeys, we showed that the effects of neonatal hippocampal lesions did alter incidental recognition memory only when the animals reached the juvenile period (Zeamer et al., ). The current follow-up study tested whether this incidental memory loss was long-lasting, i.e., present in adulthood, or only transitory, due to functional compensation with further brain maturation. The same animals with neonatal hippocampal lesions and their sham-operated controls were re-tested in the visual paired-comparison task when they reached adulthood (48 months). The results demonstrated that, at least for easily discriminable color pictures of objects, the involvement of the hippocampus was only transitory, given that when re-tested as adults, animals with neonatal hippocampal lesions performed as well as sham-operated controls at all delays. Yet, significant recognition memory impairment was re-instated when the discriminability of the stimuli was made more difficult (black/white pictures of similar objects). The data demonstrate profound functional remodeling within the hippocampus and its interactions with different medial temporal lobe structures from the juvenile period to adulthood, which is substantiated by a parallel morphological maturation of hippocampal intrinsic circuits (Lavenex et al., ; Jabès et al., ).

A behavioral task predicts conversion to mild cognitive impairment and Alzheimer's disease.

Currently, we cannot reliably differentiate individuals at risk of cognitive decline, for example, mild cognitive impairment (MCI), Alzheimer's disease (AD), from those individuals who are not at risk. A total of 32 participants with MCI and 60 control (CON) participants were tested on an innovative, sensitive behavioral assay, the visual paired comparison (VPC) task using infrared eye tracking. The participants were followed for 3 years after testing. Scores on the VPC task predicted, up to 3 years prior to a change in clinical diagnosis, those patients with MCI who would and who would not progress to AD and CON participants who would and would not progress to MCI. The present findings show that the VPC task can predict impending cognitive decline. To our knowledge, this is the first behavioral task that can identify CON participants who will develop MCI or patients with MCI who will develop AD within the next few years.

Detecting cognitive impairment by eye movement analysis using automatic classification algorithms

The Visual Paired Comparison (VPC) task is a recognition memory test that has shown promise for the detection of memory impairments associated with mild cognitive impairment (MCI). Because patients with MCI often progress to Alzheimer's Disease (AD), the VPC may be useful in predicting the onset of AD. VPC uses noninvasive eye tracking to identify how subjects view novel and repeated visual stimuli. Healthy control subjects demonstrate memory for the repeated stimuli by spending more time looking at the novel images, i.e., novelty preference. Here, we report an application of machine learning methods from computer science to improve the accuracy of detecting MCI by modeling eye movement characteristics such as fixations, saccades, and re-fixations during the VPC task. These characteristics are represented as features provided to automatic classification algorithms such as Support Vector Machines (SVMs). Using the SVM classification algorithm, in tandem with modeling the patterns of fixations, saccade orientation, and regression patterns, our algorithm was able to automatically distinguish age-matched normal control subjects from MCI subjects with 87% accuracy, 97% sensitivity and 77% specificity, compared to the best available classification performance of 67% accuracy, 60% sensitivity, and 73% specificity when using only the novelty preference information. These results demonstrate the effectiveness of applying machine-learning techniques to the detection of MCI, and suggest a promising approach for detection of cognitive impairments associated with other disorders.

The evolution of face processing in primates.

The ability to recognize faces is an important socio-cognitive skill that is associated with a number of cognitive specializations in humans. While numerous studies have examined the presence of these specializations in non-human primates, species where face recognition would confer distinct advantages in social situations, results have been mixed. The majority of studies in chimpanzees support homologous face-processing mechanisms with humans, but results from monkey studies appear largely dependent on the type of testing methods used. Studies that employ passive viewing paradigms, like the visual paired comparison task, report evidence of similarities between monkeys and humans, but tasks that use more stringent, operant response tasks, like the matching-to-sample task, often report species differences. Moreover, the data suggest that monkeys may be less sensitive than chimpanzees and humans to the precise spacing of facial features, in addition to the surface-based cues reflected in those features, information that is critical for the representation of individual identity. The aim of this paper is to provide a comprehensive review of the available data from face-processing tasks in non-human primates with the goal of understanding the evolution of this complex cognitive skill.

Developmental trajectory of object recognition memory in infant rhesus macaques with and without neonatal hippocampal lesions.

To examine the developmental trajectory of object recognition memory and its neural substrate, 10-12-d-old monkeys (Macaca mulatta) received sham operations or neurotoxic hippocampal lesions and were tested at the ages of 1.5, 6, and 18 months on the visual paired-comparison task using delays of 10, 30, 60, and 120 s. In sham-operated controls, incidental recognition memory was present at 1.5 months, became more robust at 6 months, and was delay-dependent by 18 months of age, suggesting that the brain structures mediating these early developing recognition abilities may undergo significant modifications after 6 months of age in monkeys. A similar developmental progression was also observed in animals with neonatal hippocampal lesions, although the delay-dependent effect at 18 months was significantly more pronounced after the neonatal hippocampal lesions, suggesting that with maturation animals with neonatal hippocampal lesions grow into a recognition-memory deficit. These findings suggest not only that the medial temporal cortical areas, known to mediate incidental recognition memory processes in adulthood, could support these processes in early infancy even when long delays are used, but also that later in development, after reaching functional maturity, the hippocampus begins to interact with the medial temporal cortical areas to mediate this function.

Visual recognition memory across contexts

In two experiments, we investigated the development of representational flexibility in visual recognition memory during infancy using the Visual Paired Comparison (VPC) task. In Experiment 1, 6- and 9-month-old infants exhibited recognition when familiarization and test occurred in the same room, but showed no evidence of recognition when familiarization and test occurred in different rooms. In contrast, 12- and 18-month-old infants exhibited recognition irrespective of testing room. Thus, flexibility across a change of room was observed at a younger age than flexibility across a change of background that has previously been seen with the VPC procedure (Robinson & Pascalis, 2004). To determine if limitations in representational flexibility across a change of background could be overcome by experiences during encoding, in Experiment 2, 6-, 9-, 12- and 18-month-old infants were familiarized with a picture on multiple backgrounds. At all ages, infants showed recognition across a change in background at test. These findings indicate that dissociating an item from its context during encoding may be an important factor in understanding the representational flexibility of visual recognition memory in infancy. Developmental changes in representational flexibility are likely driven by changes in the functional maturity of the hippocampal formation, and experience.

When You Turn the other Cheek: A Preference for Novel Viewpoints of Familiar Faces

Inferences about the psychobiological processes that underlie face perception have been drawn from the spontaneous behaviour of eyes. Using a visual paired-comparison task, we recorded the eye movements of twenty adults as they viewed pairs of faces that differed in their relative familiarity. The results indicate an advantage for novel viewpoints of familiar faces over familiar viewpoints of familiar faces and novel faces. We conclude that this preference serves the face recognition system by collecting the variation necessary to build robust representations of identity.