Neuronal correlates of metacognition in primate frontal cortex

Humans are metacognitive: they monitor and control their cognition. Our hypothesis was that neuronal correlates of metacognition reside in the same brain areas responsible for cognition, including frontal cortex. Recent work demonstrated that nonhuman primates are capable of metacognition, so we recorded from single neurons in the frontal eye field, dorsolateral prefrontal cortex, and supplementary eye field of monkeys (Macaca mulatta) that performed a metacognitive visual-oculomotor task. The animals made a decision and reported it with a saccade, but received no immediate reward or feedback. Instead, they had to monitor their decision and bet whether it was correct. Activity was correlated with decisions and bets in all three brain areas, but putative metacognitive activity that linked decisions to appropriate bets occurred exclusively in the SEF. Our results offer a survey of neuronal correlates of metacognition and implicate the SEF in linking cognitive functions over short periods of time.     

Self-Knowledge Dim-Out: Stress Impairs Metacognitive Accuracy

Modulation of frontal lobes activity is believed to be an important pathway trough which the hypothalamic-pituitary-adrenal (HPA) axis stress response impacts cognitive and emotional functioning. Here, we investigate the effects of stress on metacognition, which is the ability to monitor and control one''s own cognition. As the frontal lobes have been shown to play a critical role in metacognition, we predicted that under activation of the HPA axis, participants should be less accurate in the assessment of their own performances in a perceptual decision task, irrespective of the effect of stress on the first order perceptual decision itself. To test this prediction, we constituted three groups of high, medium and low stress responders based on cortisol concentration in saliva in response to a standardized psycho-social stress challenge (the Trier Social Stress Test). We then assessed the accuracy of participants'' confidence judgments in a visual discrimination task. As predicted, we found that high biological reactivity to stress correlates with lower sensitivity in metacognition. In sum, participants under stress know less when they know and when they do not know.     

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.     

The highs and lows of theoretical interpretation in animal-metacognition research

Humans feel uncertain. They know when they do not know. These feelings and the responses to them ground the research literature on metacognition. It is a natural question whether animals share this cognitive capacity, and thus animal metacognition has become an influential research area within comparative psychology. Researchers have explored this question by testing many species using perception and memory paradigms. There is an emerging consensus that animals share functional parallels with humans' conscious metacognition. Of course, this research area poses difficult issues of scientific inference. How firmly should we hold the line in insisting that animals' performances are low-level and associative? How high should we set the bar for concluding that animals share metacognitive capacities with humans? This area offers a constructive case study for considering theoretical problems that often confront comparative psychologists. The authors present this case study and address diverse issues of scientific judgement and interpretation within comparative psychology.     

Intracerebroventricular injection of streptozotocin in rats produces both oxidative stress in the brain and cognitive impairment

Recent reports suggest the involvement of free radicals in the pathophysiology of Alzheimer's disease [AD]. Streptozotocin [STZ] injection in the brain is known to cause cognitive impairment in rats and is likened to sporadic AD in humans. Though STZ is known to cause impairment in glucose and energy metabolism, it is not known whether this is associated with free radical generation. The present study was designed to investigate if the changes in learning and memory by intracerebroventricular administration of STZ are associated with changes in the markers of oxidative stress. Adult male Wistar rats [330-340 g] were injected with intracerebroventricular STZ [3 mg/kg] bilaterally stereotaxically under ketamine anesthesia [70 mg/kg]. The rats were treated with STZ twice, on day 1 and on day 3. The learning and memory behavior was analyzed using passive avoidance paradigms, elevated plus maze and the closed field activity test while the parameters of oxidative stress assessed were malondialdehyde [MDA] and glutathione. The behavioral tests were performed on day 17, 18 and 19. The rats developed significant deficits in learning, memory and cognitive behavior, indicated by deficits in passive avoidance paradigm and elevated plus maze as compared to sham rats. On day 21, the rats were sacrificed under ether anesthesia and the brains were analyzed for biochemical studies. There was a development of oxidative stress in the brain as indicated by significant elevations in malondialdehyde [MDA] levels and decreased levels of glutathione. The study demonstrates that intracerebroventricular STZ may be appropriate model for investigations of antioxidants as potential treatment in Alzheimer's dementia.     

Monkeys match the number of voices they hear to the number of faces they see

Convergent evidence demonstrates that adult humans possess numerical representations that are independent of language [1, 2, 3, 4, 5 and 6]. Human infants and nonhuman animals can also make purely numerical discriminations, implicating both developmental and evolutionary bases for adult humans' language-independent representations of number [7 and 8]. Recent evidence suggests that the nonverbal representations of number held by human adults are not constrained by the sensory modality in which they were perceived [9]. Previous studies, however, have yielded conflicting results concerning whether the number representations held by nonhuman animals and human infants are tied to the modality in which they were established [10, 11, 12, 13, 14 and 15]. Here, we report that untrained monkeys preferentially looked at a dynamic video display depicting the number of conspecifics that matched the number of vocalizations they heard. These findings suggest that number representations held by monkeys, like those held by adult humans, are unfettered by stimulus modality.     

Subjective socioeconomic status predicts human ventral striatal responses to social status information

The enormous influence of hierarchical rank on social interactions [1] suggests that neural mechanisms exist to process status-related information [2] and ascribe value to it. The ventral striatum is prominently implicated in processing value and salience, independent of hedonic properties [3, 4], and a functional magnetic resonance imaging (fMRI) study of social status perception in humans demonstrated that viewing higher-ranked compared to lower-ranked individuals evokes a ventral striatal response [5], indicative of a greater assignment of value/salience to higher status. Consistent with this interpretation, nonhuman primates value information associated with higher-ranked conspecifics more than lower-ranked, as illustrated using a choice paradigm in which monkeys preferentially take the opportunity to view high-status monkeys [6]. Interestingly, this status-related value assignment in nonhuman primates is influenced by one's own hierarchical rank: high-status monkeys preferentially attend to conspecifics of high status, whereas low-status monkeys will also attend to other low-status monkeys [7]. Complementary to these findings, using fMRI and a social status judgment task in humans, we suggest a neurobiological mechanism by which one's own relative hierarchical rank influences the value attributed to particular social status information by demonstrating that one's subjective socioeconomic status differentially influences ventral striatal activity during processing of status-related information.     

Western scrub-jays anticipate future needs independently of their current motivational state

Planning for the future has been considered to be a uniquely human trait [1-3]. However, recent studies challenge this hypothesis by showing that food-caching Western scrub-jays (Aphelocoma californica) can relate their previous experience as thieves to the possibility of future cache theft by another bird [4], are sensitive to the state of their caches at recovery ([5] and S. De Kort, S.P.C.C., D. Alexis, A.D., and N.S.C., unpublished data), and can plan for tomorrow's breakfast [6]. Although these results suggest that scrub-jays are capable of future planning, the degree to which these birds act independently of their current motivational state is a matter of contention. The Bischof-K?hler hypothesis [1] holds that nonhuman animals cannot anticipate and act toward the satisfaction of a future need not currently experienced or cued by their present motivational state. Using specific satiety to control for the jays' current and future motivational states, here we specifically test this hypothesis by dissociating current and future motivational states. We report that Western scrub-jays anticipate the recovery of their caches, as well as their own future needs, by acting independently of their current motivational state and immediate needs. The fact that the birds act in favor of a future need as opposed to the current one challenges the hypothesis that this ability is unique to humans.     

Wild chimpanzees inform ignorant group members of danger

The ability to recognize other individuals' mental states-their knowledge and beliefs, for example-is a fundamental part of human cognition and may be unique to our species. Tests of a "theory of mind" in animals have yielded conflicting results. Some nonhuman primates can read others' intentions and know what others see, but they may not understand that, in others, perception can lead to knowledge. Using an alarm-call-based field experiment, we show that chimpanzees were more likely to alarm call in response to a snake in the presence of unaware group members than in the presence of aware group members, suggesting that they recognize knowledge and ignorance in others. We monitored the behavior of 33 individuals to a model viper placed on their projected travel path. Alarm calls were significantly more common if the caller was with group members who had either not seen the snake or had not been present when alarm calls were emitted. Other factors, such as own arousal, perceived risk, or risk to receivers, did not significantly explain the likelihood of calling, although they did affect the call rates. Our results suggest that chimpanzees monitor the information available to other chimpanzees and control vocal production to selectively inform them.     

Remembering nutrient quality of sugar in Drosophila

Taste is an early stage in food and drink selection for most animals [1, 2]. Detecting sweetness indicates the presence of sugar and possible caloric content. However, sweet taste can be an unreliable predictor of nutrient value because some sugars cannot be metabolized. In addition, discrete sugars are detected by the same sensory neurons in the mammalian [3] and insect [4, 5] gustatory systems, making it difficult for animals to readily distinguish the identity of different sugars using taste alone [6-8]. Here we used an appetitive memory assay in Drosophila [9-11] to investigate the contribution of palatability and relative nutritional value of sugars to memory formation. We show that palatability and nutrient value both contribute to reinforcement of appetitive memory. Nonnutritious sugars formed less robust memory that could be augmented by supplementing with a tasteless but nutritious substance. Nutrient information is conveyed to the brain within minutes of training, when it can be used to guide expression of a sugar-preference memory. Therefore, flies can rapidly learn to discriminate between sugars using a postingestive reward evaluation system, and they preferentially remember nutritious sugars.     

Teaching with evaluation in ants

Tandem running in ants is a form of recruitment in which a single well-informed worker guides a naive nestmate to a goal [1-8]. The ant Temnothorax albipennis recently satisfied a strict set of predefined criteria for teaching in nonhuman animals [9, 10]. These criteria do not include evaluation as a prerequisite for teaching [10]. However, some authors claim that true teaching is always evaluative, i.e., sensitive to the competence or quality of the pupil [11-13]. They then assume, on the premise that only humans are capable of making such necessarily complex cognitive evaluations, that teaching must be unique to humans. We conducted experiments to test whether evaluation occurs during tandem running, in which a knowledgeable ant physically guides a naive follower to a goal. In each experiment, we interrupted the tandem run by removing the tandem follower. The response of the leader was to stand still at the point where the tandem run was interrupted. We then measured how long the leader waited for the missing follower before giving up. Our results demonstrate T. albipennis performs three different kinds of evaluation. First, the longer the tandem has proceeded the longer the leader will wait for the follower to re-establish contact. Second, ant teachers modulate their giving-up time depending on the value of the goal. Finally, leaders have shorter giving-up times after unusually slow tandem runs.     

The role of metacognition in human social interactions

Metacognition concerns the processes by which we monitor and control our own cognitive processes. It can also be applied to others, in which case it is known as mentalizing. Both kinds of metacognition have implicit and explicit forms, where implicit means automatic and without awareness. Implicit metacognition enables us to adopt a we-mode, through which we automatically take account of the knowledge and intentions of others. Adoption of this mode enhances joint action. Explicit metacognition enables us to reflect on and justify our behaviour to others. However, access to the underlying processes is very limited for both self and others and our reports on our own and others' intentions can be very inaccurate. On the other hand, recent experiments have shown that, through discussions of our perceptual experiences with others, we can detect sensory signals more accurately, even in the absence of objective feedback. Through our willingness to discuss with others the reasons for our actions and perceptions, we overcome our lack of direct access to the underlying cognitive processes. This creates the potential for us to build more accurate accounts of the world and of ourselves. I suggest, therefore, that explicit metacognition is a uniquely human ability that has evolved through its enhancement of collaborative decision-making.     

Neurodegenerative properties of chronic pain: cognitive decline in patients with chronic pancreatitis

Chronic pain has been associated with impaired cognitive function. We examined cognitive performance in patients with severe chronic pancreatitis pain. We explored the following factors for their contribution to observed cognitive deficits: pain duration, comorbidity (depression, sleep disturbance), use of opioids, and premorbid alcohol abuse. The cognitive profiles of 16 patients with severe pain due to chronic pancreatitis were determined using an extensive neuropsychological test battery. Data from three cognitive domains (psychomotor performance, memory, executive functions) were compared to data from healthy controls matched for age, gender and education. Multivariate multilevel analysis of the data showed decreased test scores in patients with chronic pancreatitis pain in different cognitive domains. Psychomotor performance and executive functions showed the most prominent decline. Interestingly, pain duration appeared to be the strongest predictor for observed cognitive decline. Depressive symptoms, sleep disturbance, opioid use and history of alcohol abuse provided additional explanations for the observed cognitive decline in some of the tests, but to a lesser extent than pain duration. The negative effect of pain duration on cognitive performance is compatible with the theory of neurodegenerative properties of chronic pain. Therefore, early and effective therapeutic interventions might reduce or prevent decline in cognitive performance, thereby improving outcomes and quality of life in these patients.     

The Genetic Algorithm Applied as a Modelling Tool to Predict the Fold of Small Proteins with Different Topologies

The genetic algorithm exploits the principles of natural evolution. Solution trials are evolved by mutation, recombination and selection until they achieve near optimal solutions [1].Our own approach has now been developed [2] after a general overview on the application potential for protein structure analysis [3] to a tool to delineate the three-dimensional topology for the mainchain of small proteins [4], no matter whether they are largely helical, are mixed or -strand rich [5].Results on several protein examples for these different modelling tasks are presented and compared with the experimentally observed structures (RMSDs are around 4.5-5.5 Å). To start a modelling trial only the protein sequence and knowledge of its secondary structure is required. The fittest folds obtained after the evolution at the end of the simulations yield the three dimensional models of the fold. Current limitations are protein size (generally less than 100 aminoacids), number of secondary structure elements [7-8] and irregular topologies (e.g. ferridoxins).Further, preliminary results from current simulations are illustrated. We now want to apply simple experimental or other information, which is available long before the three-dimensional structure of the protein becomes known, to refine the modelling of the protein fold and tackle also more difficult modelling examples by our tool.Supplementary material to this paper is available in electronic form at http://dx.doi.org/10.1007/s0089460020304     

Anomalous rise in algal production linked to lakewater calcium decline through food web interactions

Increased algal blooms are a threat to aquatic ecosystems worldwide, although the combined effects of multiple stressors make it difficult to determine the underlying causes. We explore whether changes in trophic interactions in response to declining calcium (Ca) concentrations, a water quality issue only recently recognized in Europe and North America, can be linked with unexplained bloom production. Using a palaeolimnological approach analysing the remains of Cladocera (herbivorous grazers) and visual reflectance spectroscopically inferred chlorophyll a from the sediments of a Nova Scotia (Canada) lake, we show that a keystone grazer, Daphnia, declined in the early 1990s and was replaced by a less effective grazer, Bosmina, while inferred chlorophyll a levels tripled at constant total phosphorus (TP) concentrations. The decline in Daphnia cannot be attributed to changes in pH, thermal stratification or predation, but instead is linked to declining lakewater [Ca]. The consistency in the timing of changes in Daphnia and inferred chlorophyll a suggests top-down control on algal production, providing, to our knowledge, the first evidence of a link between lakewater [Ca] decline and elevated algal production mediated through the effects of [Ca] decline on Daphnia. [Ca] decline has severe implications for whole-lake food webs, and presents yet another mechanism for potential increases in algal blooms.     

Cage size preference in rats in the laboratory

The size of an enclosure is an integral part of how well it accommodates a nonhuman animal's welfare; however, most enrichment studies concentrate on modifying the area inside the enclosure rather than enlarging it. It has been suggested that rats have little need for more cage space, but there is no empirical evidence about rats' need for space. This experiment provides preliminary evidence for the preferences of 5 male and 5 female albino rats using T-maze choices followed by 5 min dwelling times. The rats showed a moderate but significant preference for the larger of 2 cages [540 cm2 vs. 1,620 cm2; binomial z, p <.05]. When the rats shared the chosen cage with 4 familiar cage mates, their preference for the larger cage did not become any stronger [paired t[9] = -.820, p >.05]. The results suggest that rats should be given a somewhat larger space allowance but could share it with up to 4 other rats.     

Agitated honeybees exhibit pessimistic cognitive biases

Whether animals experience human-like emotions is controversial and of immense societal concern [1-3]. Because animals cannot provide subjective reports of how they feel, emotional state can only be inferred using physiological, cognitive, and behavioral measures [4-8]. In humans, negative feelings are reliably correlated with pessimistic cognitive biases, defined as the increased expectation of bad outcomes [9-11]. Recently, mammals [12-16] and birds [17-20] with poor welfare have also been found to display pessimistic-like decision making, but cognitive biases have not thus far been explored in invertebrates. Here, we ask whether honeybees display a pessimistic cognitive bias when they are subjected to an anxiety-like state induced by vigorous shaking designed to simulate a predatory attack. We show for the first time that agitated bees are more likely to classify ambiguous stimuli as predicting punishment. Shaken bees also have lower levels of hemolymph dopamine, octopamine, and serotonin. In demonstrating state-dependent modulation of categorization in bees, and thereby a cognitive component of emotion, we show that the bees' response to a negatively valenced event has more in common with that of vertebrates than previously thought. This finding reinforces the use of cognitive bias as a measure of negative emotional states across species and suggests that honeybees could be regarded as exhibiting emotions.     

A test of imitative learning in starlings using a two-action method with an enhanced ghost control

Imitative learning, in which an individual learns to reproduce the behaviour pattern of another, has attracted considerable attention as a potentially powerful form of social learning. Despite extensive research, however, it has proved difficult to demonstrate in nonhuman animals. We investigated the ability of European starlings, Sturnus vulgaris, to imitate the behaviour of a conspecific. Subjects watched a trained conspecific manipulating a plug for access to a food reward, using either a pushing or a pulling action. When later tested with the same apparatus these birds completed the task using the same action they had previously observed. In a second experiment, a separate group of starlings saw the plug move upwards or downwards automatically and a nearby conspecific obtain a food reward. When given access to the task these starlings failed to move the plug in the direction they had seen. Our experiment is an improvement on previous bidirectional control designs and provides strong evidence that starlings are capable of imitation. We advocate further use of this experimental design in attempts to demonstrate imitative learning. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Domestic hens succeed at serial reversal learning and perceptual concept generalisation using a new automated touchscreen device

Improving the welfare of farm animals depends on our knowledge on how they perceive and interpret their environment; the latter depends on their cognitive abilities. Hence, limited knowledge of the range of cognitive abilities of farm animals is a major concern. An effective approach to explore the cognitive range of a species is to apply automated testing devices, which are still underdeveloped in farm animals. In screen-like studies, the uses of automated devices are few in domestic hens. We developed an original fully automated touchscreen device using digital computer-drawn colour pictures and independent sensible cells adapted for cognitive testing in domestic hens, enabling a wide range of test types from low to high complexity. This study aimed to test the efficiency of our device using two cognitive tests. We focused on tasks related to adaptive capacities to environmental variability, such as flexibility and generalisation capacities as this is a good start to approach more complex cognitive capacities. We implemented a serial reversal learning task, categorised as a simple cognitive test, and a delayed matching-to-sample (dMTS) task on an identity concept, followed by a generalisation test, categorised as more complex. In the serial reversal learning task, the hens performed equally for the two changing reward contingencies in only three reversal stages. In the dMTS task, the hens increased their performance rapidly throughout the training sessions. Moreover, to the best of our knowledge, we present the first positive result of identity concept generalisation in a dMTS task in domestic hens. Our results provide additional information on the behavioural flexibility and concept understanding of domestic hens. They also support the idea that fully automated devices would improve knowledge of farm animals’ cognition.     

Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism

Wolbachia is a genus of alpha-proteobacteria found in obligate intracellular association with a wide variety of arthropods, including an estimated 10-20% of all insect species [1]. Wolbachia represents one of a number of recently identified 'reproductive parasites' [2] which manipulate the reproduction of their hosts in ways that enhance their own transmission [3] [4] [5] [6] [7] [8] [9]. The influence of Wolbachia infection on the dynamics of host populations has focused considerable interest on its possible role in speciation through reproductive isolation [3] [10] [11] and as an agent of biological control [2] [12] [13]. Although Wolbachia normally undergoes vertical transmission through the maternal line of its host population [14], there is compelling evidence from molecular phylogenies that extensive horizontal (intertaxon) transmission must have occurred [1] [9] [15] [16] [17]. Some of the best candidate vectors for the horizontal transmission of Wolbachia are insect parasitoids [15], which comprise around 25% of all insect species and attack arthropods from an enormous range of taxa [18]. In this study, we used both fluorescence microscopy and PCR amplification with Wolbachia-specific primers to show that Wolbachia can be transmitted to a parasitic wasp (Leptopilina boulardi) from its infected host (Drosophila simulans) and subsequently undergo diminishing vertical transmission in this novel host species. These results are, to our knowledge, the first to reveal a natural horizontal transfer route for Wolbachia between phylogenetically distant insect species.