Spatial inference without a cognitive map: the role of higher-order path integration

The cognitive map has been taken as the standard model for how agents infer the most efficient route to a goal location. Alternatively, path integration – maintaining a homing vector during navigation – constitutes a primitive and presumably less-flexible strategy than cognitive mapping because path integration relies primarily on vestibular stimuli and pace counting. The historical debate as to whether complex spatial navigation is ruled by associative learning or cognitive map mechanisms has been challenged by experimental difficulties in successfully neutralizing path integration. To our knowledge, there are only three studies that have succeeded in resolving this issue, all showing clear evidence of novel route taking, a behaviour outside the scope of traditional associative learning accounts. Nevertheless, there is no mechanistic explanation as to how animals perform novel route taking. We propose here a new model of spatial learning that combines path integration with higher-order associative learning, and demonstrate how it can account for novel route taking without a cognitive map, thus resolving this long-standing debate. We show how our higher-order path integration (HOPI) model can explain spatial inferences, such as novel detours and shortcuts. Our analysis suggests that a phylogenetically ancient, vector-based navigational strategy utilizing associative processes is powerful enough to support complex spatial inferences.     

A brain-inspired compact cognitive mapping system

In many simultaneous localization and mapping (SLAM) systems, the map of the environment grows over time as the robot explores the environment. The ever-growing map prevents long-term mapping, especially in large-scale environments. In this paper, we develop a compact cognitive mapping approach inspired by neurobiological experiments. Mimicking the firing activities of neighborhood cells, neighborhood fields determined by movement information, i.e. translation and rotation, are modeled to describe one of the distinct segments of the explored environment. The vertices with low neighborhood field activities are avoided to be added into the cognitive map. The optimization of the cognitive map is formulated as a robust non-linear least squares problem constrained by the transitions between vertices, and is numerically solved efficiently. According to the cognitive decision-making of place familiarity, loop closure edges are clustered depending on time intervals, and then batch global optimization of the cognitive map is performed to satisfy the combined constraint of the whole cluster. After the loop closure process, scene integration is performed, in which revisited vertices are removed subsequently to further reduce the size of the cognitive map. The compact cognitive mapping approach is tested on a monocular visual SLAM system in a naturalistic maze for a biomimetic animated robot. Our results demonstrate that the proposed method largely restricts the growth of the size of the cognitive map over time, and meanwhile, the compact cognitive map correctly represents the overall layout of the environment. The compact cognitive mapping method is well suitable for the representation of large-scale environments to achieve long-term robot navigation. Electronic supplementary materialThe online version of this article (10.1007/s11571-020-09621-6) contains supplementary material, which is available to authorized users.     

Attractylone attenuates sepsis-associated encephalopathy and cognitive dysfunction by inhibiting microglial activation and neuroinflammation

Multiple studies demonstrated that sepsis is a life-threatening state of organ dysfunction caused by infection and can induce neuroinflammation and cognitive impairment. The aim of this study was to evaluate the protective effects of attractylone (Atr) on sepsis-associated encephalopathy (SAE) and cognitive dysfunction. Moreover, we studied the underlying molecular mechanisms. We used an LPS-induced sepsis mouse model and evaluated the cognitive function with the Morris water maze and open field test. Neuronal damage in the hippocampus was assessed by immunohistochemical analysis. BV2 cells were used to identify the protective mechanism of Atr. The result showed that Atr attenuated LPS-induced cognitive impairment, neural apoptosis, inflammatory factors, and microglial activation. The in vitro experiment showed that Atr promoted silent information regulator 1 (SIRT1) expression and suppressed NFκB expression. Downregulation of SIRT1 reversed the protective effect of Atr in the LPS condition. Moreover, Atr-induced SIRT1 expression promoted BV2 from LPS-induced M1 to M2 phenotype. Taken together, these results indicated that Atr was a potential therapeutic agent for SAE and cognitive dysfunction.     

No need for a cognitive map: decentralized memory for insect navigation

In many animals the ability to navigate over long distances is an important prerequisite for foraging. For example, it is widely accepted that desert ants and honey bees, but also mammals, use path integration for finding the way back to their home site. It is however a matter of a long standing debate whether animals in addition are able to acquire and use so called cognitive maps. Such a 'map', a global spatial representation of the foraging area, is generally assumed to allow the animal to find shortcuts between two sites although the direct connection has never been travelled before. Using the artificial neural network approach, here we develop an artificial memory system which is based on path integration and various landmark guidance mechanisms (a bank of individual and independent landmark-defined memory elements). Activation of the individual memory elements depends on a separate motivation network and an, in part, asymmetrical lateral inhibition network. The information concerning the absolute position of the agent is present, but resides in a separate memory that can only be used by the path integration subsystem to control the behaviour, but cannot be used for computational purposes with other memory elements of the system. Thus, in this simulation there is no neural basis of a cognitive map. Nevertheless, an agent controlled by this network is able to accomplish various navigational tasks known from ants and bees and often discussed as being dependent on a cognitive map. For example, map-like behaviour as observed in honey bees arises as an emergent property from a decentralized system. This behaviour thus can be explained without referring to the assumption that a cognitive map, a coherent representation of foraging space, must exist. We hypothesize that the proposed network essentially resides in the mushroom bodies of the insect brain.     

Static magnetic field exposure affects behavior and learning in rats

The present work investigated the behavioral effects of a moderate exposure (1 h per day for 5 consecutive days) to a static magnetic field (SMF, 128 mT) in male rats. SMF effects were evaluated in two sets of control and SMF-exposed rats. One set of animals was used for evaluation of SMF potential effects on emotional behaviors in the elevated plus maze and in the open field. The other set of animals was tested for learning and memory abilities in different procedures of the Morris water maze task. We found no significant difference between control and SMF-exposed rats in anxiety tests. However, the ratio of open arms time in the plus maze was reduced by half in SMF-exposed rats. In the Morris water maze, SMF-exposed rats were partially impaired during the initial learning task as well as in the retention task at one week. We conclude that static magnetic field exposure altered emotional behaviors in the plus maze and led to cognitive impairments, or at least to substantial attention disorders, in the Morris water maze.     

Long term neurological and behavioral effects of graded perinatal asphyxia in the rat

Perinatal hypoxic-ischemic states can cause irreversible damage to the brain, ranging from minimal brain dysfunction to death. Only few studies have been reported describing neurological, cognitive and behavioral deficits following perinatal asphyxia. We therefore decided to study long term effects of perinatal asphyxia in a well-documented animal model resembling the clinical situation. Caeserean section in rats was performed and the pups, still in the uterus horns, were placed into a water bath at 37 degrees C for periods of 5-20 min; pups were then given to surrogate mothers and examined at three month of age. Examinations consisted of a battery of motor and reflex tests, Morris water maze, multiple T-maze, elevated plus maze and open field studies. No abnormalities were found in rats even with long periods of perinatal asphyxia by neurological examination, in the open field and in mazes. Interestingly, in the elevated plus maze rats with long lasting exposure to hypoxia (15 and 20 min of asphyxia) showed reduced anxiety-related behavior. This finding may be relevant for the explanation of anxiety related disorders in adulthood with a tentative history in the perinatal period.     

Ropren(?) is a polyprenol preparation from coniferous plants that ameliorates cognitive deficiency in a rat model of beta-amyloid peptide-(25-35)-induced amnesia

This study assesses the efficacy of a fixed dose of Ropren(?) (a plant preparation isolated from the neutral fraction of an extract of spruce needles) on cognitive impairment in rats with β-amyloid peptide-(25-35)-induced amnesia. Ropren(?) was administered at a dose of 8.6mg/kg for 28 days, per os, to rats with β-amyloid peptide-(25-35)-induced amnesia. Cognitive performance was assessed using the passive avoidance paradigm and the Morris water maze and behavior was assessed using the open field test. After four weeks, Ropren(?) treatment significantly improved non-spatial and spatial learning in rats with β-amyloid peptide-(25-35)-induced amnesia. The results of the present study suggest that Ropren(?), a novel plant preparation, ameliorates cognitive deficiencies in an animal model relevant to Alzheimer's disease.     

Involvement of D1 dopamine receptors in the cognitive effects of angiotensin IV and des-Phe6 angiotensin IV

An important role for angiotensin IV (Ang IV) in the processes of learning and memory has now been well established. We have previously found that intracerebroventricular (ICV) administration of Ang IV as well as des-Phe6-Ang IV enhances learning of conditioned avoidance responses (CARs), facilitates recall of a passive avoidance (PA) task, and improves object recognition (OR) in rats. Since the dopaminergic system is crucial for the cognitive processes, in this study our aim was to determine the dopaminergic D1 mediation of these effects using SCH 23390 as a selective D1 receptor antagonist. Male Wistar rats (180-200 g), pretreated with SCH 23390 (R-[+]-7-chloro-8-hydroxy-3-methyl-1-phenyl-2,3,4,5-tetrahydro-1H-3-benzazepine) 0.05 mg/kg intraperitoneally (IP), were given Ang IV or des-Phe6-Ang IV (1 nmol ICV) 1 h later and then tested in the above cognitive paradigms, as well as in the open field and an elevated 'plus' maze to control for the unspecific, respectively, motor and emotional, effects of our treatments. Both, Ang IV and des-Phe6-Ang IV effectively enhanced learning of CARs (P < 0.05), recall of PA (P < 0.001), and improved OR (P < 0.001). Pretreatment with SCH 23390 abolished the cognitive effects of both peptides. SCH 23390, Ang IV, and des-Phe6-Ang IV, given at the same doses and routes as in the cognitive tests, did not significantly influence crossings, rearings and bar approaches in the open field, nor the parameters measured in the elevated 'plus' maze, thus making a major contribution of the unspecific effects of our treatments to the results of the memory tests improbable. In conclusion, these results indicate that the functional dopaminergic D1 receptors are necessary for the Ang IV and des-Phe6-Ang IV cognitive effects to occur.     

Maintaining a cognitive map in darkness: the need to fuse boundary knowledge with path integration

Spatial navigation requires the processing of complex, disparate and often ambiguous sensory data. The neurocomputations underpinning this vital ability remain poorly understood. Controversy remains as to whether multimodal sensory information must be combined into a unified representation, consistent with Tolman's "cognitive map", or whether differential activation of independent navigation modules suffice to explain observed navigation behaviour. Here we demonstrate that key neural correlates of spatial navigation in darkness cannot be explained if the path integration system acted independently of boundary (landmark) information. In vivo recordings demonstrate that the rodent head direction (HD) system becomes unstable within three minutes without vision. In contrast, rodents maintain stable place fields and grid fields for over half an hour without vision. Using a simple HD error model, we show analytically that idiothetic path integration (iPI) alone cannot be used to maintain any stable place representation beyond two to three minutes. We then use a measure of place stability based on information theoretic principles to prove that featureless boundaries alone cannot be used to improve localization above chance level. Having shown that neither iPI nor boundaries alone are sufficient, we then address the question of whether their combination is sufficient and - we conjecture - necessary to maintain place stability for prolonged periods without vision. We addressed this question in simulations and robot experiments using a navigation model comprising of a particle filter and boundary map. The model replicates published experimental results on place field and grid field stability without vision, and makes testable predictions including place field splitting and grid field rescaling if the true arena geometry differs from the acquired boundary map. We discuss our findings in light of current theories of animal navigation and neuronal computation, and elaborate on their implications and significance for the design, analysis and interpretation of experiments.     

Cognitive ability is heritable and predicts the success of an alternative mating tactic

The ability to attract mates, acquire resources for reproduction, and successfully outcompete rivals for fertilizations may make demands on cognitive traits—the mechanisms by which an animal acquires, processes, stores and acts upon information from its environment. Consequently, cognitive traits potentially undergo sexual selection in some mating systems. We investigated the role of cognitive traits on the reproductive performance of male rose bitterling (Rhodeus ocellatus), a freshwater fish with a complex mating system and alternative mating tactics. We quantified the learning accuracy of males and females in a spatial learning task and scored them for learning accuracy. Males were subsequently allowed to play the roles of a guarder and a sneaker in competitive mating trials, with reproductive success measured using paternity analysis. We detected a significant interaction between male mating role and learning accuracy on reproductive success, with the best-performing males in maze trials showing greater reproductive success in a sneaker role than as a guarder. Using a cross-classified breeding design, learning accuracy was demonstrated to be heritable, with significant additive maternal and paternal effects. Our results imply that male cognitive traits may undergo intra-sexual selection.     

The Opioid System and Magnetic Field Perception

The impact of Opilong—a dermorphine analog and μ-receptor agonist—on male Wistar rats' sensitivity to a static magnetic field (MF) of 38 ± 2 μT was studied using an original behavioral model of spatial learning in a multiple alternative maze. The 90° maze rotation with respect to the geomagnetic force lines caused disorientation in 80% of well-trained rats preconditioned by the Opilong treatment (0.05 mg/kg), but not in the control rats. Analysis of the behavioral patterns of the opioid–induced rats implied that the rats' orientations in the maze were initially established by taking the geomagnetic force lines into account. The internal maze cues were dominant for control rats' orientations. We conclude that modulation of the opioid system caused increased MF sensitivity and allowed perception of MF parameters. This could serve as an information factor for orientation in the maze, while self-organizing complicated goal–directed behavior in opioid-induced rats.     

Strain differences in activity and emotionality do not account for differences in learning and memory performance between C57BL/6 and DBA/2 mice

This study examined emotionality, activity, learning and memory, as well as the influence of emotionality and activity on learning and memory performance in C57BL/6 and DBA/2 mice using a mouse-test battery. DBA/2 mice performed more poorly than C57BL/6 mice in complex learning tasks such as the water maze and object recognition tasks. In contrast, C57BL/6 mice showed attenuated habituation to novelty in the open field apparatus and poorer performance in the step-down passive avoidance task. The C57BL/6 mice were less exploratory and more anxious than the DBA/2 mice. The anxiety score (open arm entries in the elevated plus maze) was significantly correlated with all measures of learning and memory in the object recognition task, and some measures in the passive avoidance and water maze tasks. Analysis of covariance (with open arm entries as a covariate) revealed that some measures on trial 1 of the object recognition task, but not the memory scores on trial 2, were confounded by anxiety. No confounding factors of anxiety were found in the water maze or passive avoidance tasks. Similar results were obtained with the activity scores (line crossing and rearing in the open field). In conclusion, strain differences in activity and anxiety did not account for strain differences in learning and memory performance of C57BL/6 and DBA/2 mice. Nonetheless, the importance of using complete behavioural test batteries should be stressed to ensure that strain differences in learning and memory tasks are not confounded by non-cognitive factors.     

Deficits in acetylcholine homeostasis, receptors and behaviors in choline transporter heterozygous mice

Cholinergic neurons elaborate a hemicholinium-3 (HC-3) sensitive choline transporter (CHT) that mediates presynaptic, high-affinity choline uptake (HACU) in support of acetylcholine (ACh) synthesis and release. Homozygous deletion of CHT (-/-) is lethal shortly after birth (Ferguson et al. 2004), consistent with CHT as an essential component of cholinergic signaling, but precluding functional analyses of CHT contributions in adult animals. In contrast, CHT+/- mice are viable, fertile and display normal levels of synaptosomal HACU, yet demonstrate reduced CHT protein and increased sensitivity to HC-3, suggestive of underlying cholinergic hypofunction. We find that CHT+/- mice are equivalent to CHT+/+ siblings on measures of motor co-ordination (rotarod), general activity (open field), anxiety (elevated plus maze, light/dark paradigms) and spatial learning and memory (Morris water maze). However, CHT+/- mice display impaired performance as a result of physical challenge in the treadmill paradigm, as well as reduced sensitivity to challenge with the muscarinic receptor antagonist scopolamine in the open field paradigm. These behavioral alterations are accompanied by significantly reduced brain ACh levels, elevated choline levels and brain region-specific decreased expression of M1 and M2 muscarinic acetylcholine receptors. Our studies suggest that CHT hemizygosity results in adequate baseline ACh stores, sufficient to sustain many phenotypes, but normal sensitivities to physical and/or pharmacological challenge require full cholinergic signaling capacity.     

Strain-dependent effects of cognitive enhancers in the mouse

A series of cognitive enhancers (CEs) have been reported to increase spatial memory in rodents, information on behavioral effects, however, is limited. The aim of the study was therefore to examine the behavioral effects of three CEs in two well-documented inbred mouse strains. C57BL/6J and DBA/2 mice were administered intraperitonial. D-cycloserine (DCS; NMDA receptor agonist), 1-(4-Amino-5-chloro-2-methoxyphenyl)-3-[1-butyl-4-piperidinyl]-1-propanone hydrochloride (RS67333; 5HT4-receptor agonist), and (R)-4-{[2-(1-methyl-2-pyrrolidinyl)ethyl]thio}phenol hydrochloride (SIB-1553A; beta-4-nicotinic receptor agonist) and tested in the open field (OF), elevated plus maze (EPM), neurological observational battery and rota-rod. Cognitive performance was tested in the Morris water maze. All compounds modified behavioral performance in the OF, DCS showed an anxiolytic effect in the EPM, and differences in the observational battery were observed i.e. vestibular drop was decreased by SIB-1553A and RS67333 treatment in C57BL/6J and increased with DCS treatment in DBA/2 mice. In the rota rod SIB-1553A improved motor performance. DCS effects on learning and memory was comparable to controls whereas the other compounds impaired performance in the Morris water maze. In conclusion, behavioral testing of CEs in the mouse revealed significant changes that may have to be taken into account for evaluation of CEs, interpretation of cognitive studies and warrant further neurotoxicological studies. Moreover, strain-dependent differences were observed that in turn may confound results obtained from behavioral and cognitive testing.     

Behavioral interferences modify the acceleration in memory decay caused by diazepam

A staircase maze has been used to test the modification induced by a chronic administration of different doses of diazepam in the decay of the rat performance caused by an interruption of 20 days in the daily training. The possibility that behavioral interferences modify the diazepam effect has been examined by testing the rat in an open field or in a Y maze during the interruption of the training in the staircase maze. The diazepam effect on the rat behavior in the staircase maze increased linearly with the doses; an intercalated training in the open field increased the diazepam effect, while an intercalated training in a Y maze completely abolished the increase of forgetting caused by diazepam.     

Fast and robust image segmentation by small-world neural oscillator networks

Inspired by the temporal correlation theory of brain functions, researchers have presented a number of neural oscillator networks to implement visual scene segmentation problems. Recently, it is shown that many biological neural networks are typical small-world networks. In this paper, we propose and investigate two small-world models derived from the well-known LEGION (locally excitatory and globally inhibitory oscillator network) model. To form a small-world network, we add a proper proportion of unidirectional shortcuts (random long-range connections) to the original LEGION model. With local connections and shortcuts, the neural oscillators can not only communicate with neighbors but also exchange phase information with remote partners. Model 1 introduces excitatory shortcuts to enhance the synchronization within an oscillator group representing the same object. Model 2 goes further to replace the global inhibitor with a sparse set of inhibitory shortcuts. Simulation results indicate that the proposed small-world models could achieve synchronization faster than the original LEGION model and are more likely to bind disconnected image regions belonging together. In addition, we argue that these two models are more biologically plausible.     

Purposive behavior and cognitive mapping: a neural network model

This study presents a real-time, biologically plausible neural network approach to purposive behavior and cognitive mapping. The system is composed of (a) an action system, consisting of a goal-seeking neural mechanism controlled by a motivational system; and (b) a cognitive system, involving a neural cognitive map. The goal-seeking mechanism displays exploratory behavior until either (a) the goal is found or (b) an adequate prediction of the goal is generated. The cognitive map built by the network is a top logical map, i.e., it represents only the adjacency, but not distances or directions, between places. The network has recurrent and non-recurrent properties that allow the reading of the cognitive map without modifying it. Two types of predictions are introduced: fast-time and real-time predictions. Fast-time predictions are produced in advance of what occurs in real time, when the information stored in the cognitive map is used to predict the remote future. Real-time predictions are generated simultaneously with the occurrence of environmental events, when the information stored in the cognitive map is being updated. Computer simulations show that the network successfully describes latent learning and detour behavior in rats. In addition, simulations demonstrate that the network can be applied to problem-solving paradigms such as the Tower of Hanoi puzzle.     

Magnetic Navigation

Recent evidence suggests that some amphibians, reptiles and birds may be capable of homing using information about geographic position (“map” information) derived from subtle geographic gradients in the earth's magnetic field. The “magnetic map” hypothesis faces numerous theoretical difficulties, however, due to the extremely high level of sensitivity that would be necessary to detect natural magnetic gradients, and to the presence of spatial irregularities and temporal variation in the geomagnetic field that might make map coordinates derived from magnetic gradients unreliable. To date, the majority of studies carried out to test the magnetic map hypothesis have involved field observations of the effects on homing orientation of naturally occurring spatial or temporal variation in the geomagnetic field. While providing an important first step, these studies are subject to the criticism that the observed changes in homing orientation could result from effects on a magnetic compass, or some other unidentified component of the navigational system, rather than from effects on a magnetic map. The recent development of experimental systems in which navigational ability can be studied under controlled or semi-controlled laboratory conditions has opened up the possibility of using new experimental approaches to more rigorously test the magnetic map hypothesis. After briefly reviewing the available evidence of the geomagnetic field's involvement in the map component of homing, a simple graphical model is presented which describes how the home direction derived from a bicoordinate map varies as a function of the value of one of the map coordinates when the value of the second map coordinate is held constant. In studies of homing orientation in which the value of a specific magnetic field parameter (e.g., total intensity, inclination, etc.) can be varied independently of other putative map parameters, the graphical model can be used to generate qualitative predictions about the changes in the direction of homing orientation that should be observed if the magnetic field parameter being manipulated serves as one coordinate of a bicoordinate map. The relationship between the direction of homing orientation and the value of a putative magnetic map parameter can also be used to generate quantitative predictions about characteristics of the local gradient of that magnetic field parameter in the vicinity of the home site (i.e., the alignment and “home value” of the local gradient) which can then be compared with actual measured values. Together, the qualitative and quantitative predictions of the graphical model permit rigorous tests of whether one or both coordinates of a bicoordinate navigational map are derived from the geomagnetic field.     

Spatial memory and orientation strategies in the elasmobranch<Emphasis Type="Italic"> Potamotrygon motoro</Emphasis>

We investigated whether juvenile freshwater stingrays (Potamotrygon motoro) can solve spatial tasks by constructing a cognitive map of their environment. Two experimental conditions were run: allocentric and ego-allocentric. Rays were trained to locate food within a four-arm maze placed in a room with visual spatial cues. The feeding location (goal) within the maze (room) remained constant while the starting position varied for the allocentrically but not for the ego-allocentrically trained group. After training, all rays solved the experimental tasks; however, different orientation strategies were used within and between groups. Allocentrically trained rays reached the goal via novel routes starting from unfamiliar locations, while ego-allocentrically trained rays primarily solved the task on the basis of an egocentric turn response. Our data suggest that P. motoro orients by constructing a visual cognitive map of its environment, but also uses egocentric and/or other orientation strategies alone or in combination for spatial orientation, a choice which may be governed by the complexity of the problem. We conclude that spatial memory functions are a general feature of the vertebrate brain.     

Omega-3 fatty acids and rodent behavior

This paper reviews the role of the n-3 fatty acids in the regulation of cognitive functions, locomotor and exploratory activity and emotional status in rodents. There are disparate data on the performance of n-3 fatty acid deficient animals in the open field test and elevated plus maze. Results obtained in our laboratory indicated slower habituation to the open field in deficient mice, which affects total locomotor and exploratory parameters. We also observed no change in plus maze performance of deficient mice under low-stress but elevated anxiety under high-stress conditions. There is some evidence of elevated aggression and increased immobility time in the forced swimming test caused by n-3 fatty acid deficiency in rodents. Effects of n-3 fatty acid deficiency and supplementation on learning in several tests such as the Morris water maze, two odor olfactory discriminations, radial arm maze performance and avoidance tasks are reviewed in detail. There is some evidence of an enhanced vulnerability to stress of n-3 fatty acid deficient animals and this factor can influence performance in a variety of tests. Thus, behavioral tasks that involve a higher level of stress may better differentiate behavioral effects related to brain docosahexaenoic acid (DHA) status. It is suggested that a fruitful area for future investigations of functional alterations related to brain DHA status will be the delineation of the factors underlying changes in performance in behavioral tasks. The possible role of non-cognitive factors like emotionality and attention in the impaired performance of n-3 fatty acid deficient animals also requires further investigation.