Weighted cue integration in the rodent head direction system

How the brain combines information from different sensory modalities and of differing reliability is an important and still-unanswered question. Using the head direction (HD) system as a model, we explored the resolution of conflicts between landmarks and background cues. Sensory cue integration models predict averaging of the two cues, whereas attractor models predict capture of the signal by the dominant cue. We found that a visual landmark mostly captured the HD signal at low conflicts: however, there was an increasing propensity for the cells to integrate the cues thereafter. A large conflict presented to naive rats resulted in greater visual cue capture (less integration) than in experienced rats, revealing an effect of experience. We propose that weighted cue integration in HD cells arises from dynamic plasticity of the feed-forward inputs to the network, causing within-trial spatial redistribution of the visual inputs onto the ring. This suggests that an attractor network can implement decision processes about cue reliability using simple architecture and learning rules, thus providing a potential neural substrate for weighted cue integration.     

Combination and competition between path integration and landmark navigation in the estimation of heading direction

Successful navigation requires the ability to compute one’s location and heading from incoming multisensory information. Previous work has shown that this multisensory input comes in two forms: body-based idiothetic cues, from one’s own rotations and translations, and visual allothetic cues, from the environment (usually visual landmarks). However, exactly how these two streams of information are integrated is unclear, with some models suggesting the body-based idiothetic and visual allothetic cues are combined, while others suggest they compete. In this paper we investigated the integration of body-based idiothetic and visual allothetic cues in the computation of heading using virtual reality. In our experiment, participants performed a series of body turns of up to 360 degrees in the dark with only a brief flash (300ms) of visual feedback en route. Because the environment was virtual, we had full control over the visual feedback and were able to vary the offset between this feedback and the true heading angle. By measuring the effect of the feedback offset on the angle participants turned, we were able to determine the extent to which they incorporated visual feedback as a function of the offset error. By further modeling this behavior we were able to quantify the computations people used. While there were considerable individual differences in performance on our task, with some participants mostly ignoring the visual feedback and others relying on it almost entirely, our modeling results suggest that almost all participants used the same strategy in which idiothetic and allothetic cues are combined when the mismatch between them is small, but compete when the mismatch is large. These findings suggest that participants update their estimate of heading using a hybrid strategy that mixes the combination and competition of cues.     

A model of head direction and landmark coding in complex environments

Environmental information is required to stabilize estimates of head direction (HD) based on angular path integration. However, it is unclear how this happens in real-world (visually complex) environments. We present a computational model of how visual feedback can stabilize HD information in environments that contain multiple cues of varying stability and directional specificity. We show how combinations of feature-specific visual inputs can generate a stable unimodal landmark bearing signal, even in the presence of multiple cues and ambiguous directional specificity. This signal is associated with the retrosplenial HD signal (inherited from thalamic HD cells) and conveys feedback to the subcortical HD circuitry. The model predicts neurons with a unimodal encoding of the egocentric orientation of the array of landmarks, rather than any one particular landmark. The relationship between these abstract landmark bearing neurons and head direction cells is reminiscent of the relationship between place cells and grid cells. Their unimodal encoding is formed from visual inputs via a modified version of Oja’s Subspace Algorithm. The rule allows the landmark bearing signal to disconnect from directionally unstable or ephemeral cues, incorporate newly added stable cues, support orientation across many different environments (high memory capacity), and is consistent with recent empirical findings on bidirectional HD firing reported in the retrosplenial cortex. Our account of visual feedback for HD stabilization provides a novel perspective on neural mechanisms of spatial navigation within richer sensory environments, and makes experimentally testable predictions.     

The influence of habitat stability on landmark use during spatial learning in the three-spined stickleback

The capacity to learn enables animals to match their phenotypic response to a changing environment on the basis of experience but learning is likely to incur costs such as the cost of making mistakes or the energetic cost of processing information. Little is known about how animals optimize the use of learned behaviour within their natural environments such that potential costs are minimized. We investigated whether the use of local landmarks in learning orientation routes by the three-spined stickleback, Gasterosteus aculeatus, varied in response to the visual stability of their natural habitats. Sticklebacks collected from five fast-flowing rivers and five ponds were trained to locate a hidden reward in a T-maze. Locating the reward required the fish to learn a body-centred algorithmic behaviour (turn left or right) or to follow plant landmarks. Probe trials, in which these cues conflicted, revealed which spatial cue the fish was using. Pond fish appeared to rely more than river fish on visual landmarks, which is consistent with the suggestion that even within a species, learned behaviour is fine-tuned in response to local environmental conditions. Landmarks may be reliable indicators of location only in stable pond habitats. In rivers, turbulence and flow may continually disrupt the visual landscape such that river fish may benefit from learning orientation routes only if learning is constrained so that unreliable visual cues are ignored. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Spatial cognition and neuro-mimetic navigation: a model of hippocampal place cell activity

 A computational model of hippocampal activity during spatial cognition and navigation tasks is presented. The spatial representation in our model of the rat hippocampus is built on-line during exploration via two processing streams. An allothetic vision-based representation is built by unsupervised Hebbian learning extracting spatio-temporal properties of the environment from visual input. An idiothetic representation is learned based on internal movement-related information provided by path integration. On the level of the hippocampus, allothetic and idiothetic representations are integrated to yield a stable representation of the environment by a population of localized overlapping CA3-CA1 place fields. The hippocampal spatial representation is used as a basis for goal-oriented spatial behavior. We focus on the neural pathway connecting the hippocampus to the nucleus accumbens. Place cells drive a population of locomotor action neurons in the nucleus accumbens. Reward-based learning is applied to map place cell activity into action cell activity. The ensemble action cell activity provides navigational maps to support spatial behavior. We present experimental results obtained with a mobile Khepera robot. Received: 02 July 1999 / Accepted in revised form: 20 March 2000     

Subconscious Visual Cues during Movement Execution Allow Correct Online Choice Reactions

Part of the sensory information is processed by our central nervous system without conscious perception. Subconscious processing has been shown to be capable of triggering motor reactions. In the present study, we asked the question whether visual information, which is not consciously perceived, could influence decision-making in a choice reaction task. Ten healthy subjects (28±5 years) executed two different experimental protocols. In the Motor reaction protocol, a visual target cue was shown on a computer screen. Depending on the displayed cue, subjects had to either complete a reaching movement (go-condition) or had to abort the movement (stop-condition). The cue was presented with different display durations (20–160 ms). In the second Verbalization protocol, subjects verbalized what they experienced on the screen. Again, the cue was presented with different display durations. This second protocol tested for conscious perception of the visual cue. The results of this study show that subjects achieved significantly more correct responses in the Motor reaction protocol than in the Verbalization protocol. This difference was only observed at the very short display durations of the visual cue. Since correct responses in the Verbalization protocol required conscious perception of the visual information, our findings imply that the subjects performed correct motor responses to visual cues, which they were not conscious about. It is therefore concluded that humans may reach decisions based on subconscious visual information in a choice reaction task.     

Optimal cue integration in ants

In situations with redundant or competing sensory information, humans have been shown to perform cue integration, weighting different cues according to their certainty in a quantifiably optimal manner. Ants have been shown to merge the directional information available from their path integration (PI) and visual memory, but as yet it is not clear that they do so in a way that reflects the relative certainty of the cues. In this study, we manipulate the variance of the PI home vector by allowing ants (Cataglyphis velox) to run different distances and testing their directional choice when the PI vector direction is put in competition with visual memory. Ants show progressively stronger weighting of their PI direction as PI length increases. The weighting is quantitatively predicted by modelling the expected directional variance of home vectors of different lengths and assuming optimal cue integration. However, a subsequent experiment suggests ants may not actually compute an internal estimate of the PI certainty, but are using the PI home vector length as a proxy.     

Sex-inducing effect of a hydrophilic fraction on reproductive switching in the planarian Dugesia ryukyuensis (Seriata, Tricladida)

Background

Insects are known to rely on terrestrial landmarks for navigation. Landmarks are used to chart a route or pinpoint a goal. The distant panorama, however, is often thought not to guide navigation directly during a familiar journey, but to act as a contextual cue that primes the correct memory of the landmarks.

Results

We provided Melophorus bagoti ants with a huge artificial landmark located right near the nest entrance to find out whether navigating ants focus on such a prominent visual landmark for homing guidance. When the landmark was displaced by small or large distances, ant routes were affected differently. Certain behaviours appeared inconsistent with the hypothesis that guidance was based on the landmark only. Instead, comparisons of panoramic images recorded on the field, encompassing both landmark and distal panorama, could explain most aspects of the ant behaviours.

Conclusion

Ants navigating along a familiar route do not focus on obvious landmarks or filter out distal panoramic cues, but appear to be guided by cues covering a large area of their panoramic visual field, including both landmarks and distal panorama. Using panoramic views seems an appropriate strategy to cope with the complexity of natural scenes and the poor resolution of insects' eyes. The ability to isolate landmarks from the rest of a scene may be beyond the capacity of animals that do not possess a dedicated object-perception visual stream like primates.     

Influence of habitat complexity on route learning among different populations of climbing perch (Anabas testudineus Bloch, 1792)

Animals use different behavioral strategies to maximize their fitness in the natural environment. Learning and memory are critical in this context, allowing organisms to flexibly and rapidly respond to environmental changes. We studied how the physical characteristics of the native habitat influence the spatial learning capacity of Anabas testudineus belonging to four different populations collected from two streams and two ponds, in a linear maze. Stream fish were able to learn the route faster than pond fish irrespective of the presence or absence of landmarks in the maze. However, climbing perch collected from ponds learned the route faster in the maze provided with landmarks than in Plain maze. The results indicate that fish inhabiting a lotic ecosystem use egocentric cues in route learning rather than visual cues like landmarks. A local landmark may be a more reliable cue in route learning in a relatively stable habitat like a pond. In flowing aquatic systems, water flow may continually disrupt the visual landscape and thus landmarks as visual cues become unreliable. Spatial learning is thus a fine-tuned response to the complexity of the habitat and early rearing conditions may influence the spatial learning ability in fish.     

Deciding to learn: modulation of learning flights in honeybees, <Emphasis Type="Italic">Apis mellifera</Emphasis>

Upon discovering new sources of food, honeybees and other insects perform learning flights to memorize visual landmarks that can guide their return. Learning flights are longest following initial visits to the food and subsequently decline in duration, which suggests that the investment in learning results from an active decision modulated by a bee's accumulating experience. We document various factors that influence this decision: (1). learning flights reappear when experienced bees encounter a delay in finding food at a familiar place and the durations of such "reorientation flights" increase with the length of the delay; (2). the decay in learning flight duration over visits following such reorientation flights is more rapid than following initial discovery of the food; (3). learning flight duration increases with the visual complexity of the scene surrounding the food, and when spatial relationships among landmarks are unstable; and (4). durations of learning flights at a new feeding place are influenced by the sucrose concentration in the food. Taken together, these experiments suggest that bees can adjust their learning efforts in response to changing needs for visual information and that both sources of spatial uncertainty and the quality of the food influence the value of such information.     

Use of water flow direction to provide spatial information in a small-scale orientation task

Experiments were designed to investigate whether three-spined sticklebacks Gasterosteus aculeatus can use direction of water flow as an orientation cue. The fish had to learn the location of a food patch in a channel where water flow direction was the only reliable indicator of the food patch position. Fish from two ponds and two rivers were trained and tested in the spatial task to determine whether river three-spined sticklebacks are more adept at using water flow as a spatial cue than fish from ponds. All fish were able to use water flow to locate the food patch but one of the two river groups was significantly faster at learning the patch location. When the task was reversed so that fish that had formerly been trained to swim downstream now had to learn to swim upstream and vice versa both river groups learned the reversed task faster than the two pond groups. In a second experiment, to investigate whether fish from ponds or rivers vary in the type of spatial cue that they prefer to use, fish from one pond and one river were given a choice between two different types of spatial cue: flow direction or visual landmarks. A test trial in which these two cues were put into conflict revealed that the river population showed a strong preference for flow direction whilst the pond population preferred to use visual landmarks.     

Estimating Location without External Cues

The ability to determine one''s location is fundamental to spatial navigation. Here, it is shown that localization is theoretically possible without the use of external cues, and without knowledge of initial position or orientation. With only error-prone self-motion estimates as input, a fully disoriented agent can, in principle, determine its location in familiar spaces with 1-fold rotational symmetry. Surprisingly, localization does not require the sensing of any external cue, including the boundary. The combination of self-motion estimates and an internal map of the arena provide enough information for localization. This stands in conflict with the supposition that 2D arenas are analogous to open fields. Using a rodent error model, it is shown that the localization performance which can be achieved is enough to initiate and maintain stable firing patterns like those of grid cells, starting from full disorientation. Successful localization was achieved when the rotational asymmetry was due to the external boundary, an interior barrier or a void space within an arena. Optimal localization performance was found to depend on arena shape, arena size, local and global rotational asymmetry, and the structure of the path taken during localization. Since allothetic cues including visual and boundary contact cues were not present, localization necessarily relied on the fusion of idiothetic self-motion cues and memory of the boundary. Implications for spatial navigation mechanisms are discussed, including possible relationships with place field overdispersion and hippocampal reverse replay. Based on these results, experiments are suggested to identify if and where information fusion occurs in the mammalian spatial memory system.     

Model analyses of visual biofeedback training for EEG-based brain-computer interface

The primary goal of this study was to construct a simulation model of a biofeedback brain-computer interface (BCI) system to analyze the effect of biofeedback training on BCI users. A mathematical model of a man-machine visual-biofeedback BCI system was constructed to simulate a subject using a BCI system to control cursor movements. The model consisted of a visual tracking system, a thalamo-cortical model for EEG generation, and a BCI system. The BCI system in the model was realized for real experiments of visual biofeedback training. Ten sessions of visual biofeedback training were performed in eight normal subjects during a 3-week period. The task was to move a cursor horizontally across a screen, or to hold it at the screen’s center. Experimental conditions and EEG data obtained from real experiments were then simulated with the model. Three model parameters, representing the adaptation rate of gain in the visual tracking system and the relative synaptic strength between the thalamic reticular and thalamo-cortical cells in the Rolandic areas, were estimated by optimization techniques so that the performance of the model best fitted the experimental results. The serial changes of these parameters over the ten sessions, reflecting the effects of biofeedback training, were analyzed. The model simulation could reproduce results similar to the experimental data. The group mean success rate and information transfer rate improved significantly after training (56.6 to 81.1% and 0.19 to 0.76 bits/trial, respectively). All three model parameters displayed similar and statistically significant increasing trends with time. Extensive simulation with systematic changes of these parameters also demonstrated that assigning larger values to the parameters improved the BCI performance. We constructed a model of a biofeedback BCI system that could simulate experimental data and the effect of training. The simulation results implied that the improvement was achieved through a quicker adaptation rate in visual tracking gain and a larger synaptic gain from the visual tracking system to the thalamic reticular cells. In addition to the purpose of this study, the constructed biofeedback BCI model can also be used both to investigate the effects of different biofeedback paradigms and to test, estimate, or predict the performances of other newly developed BCI signal processing algorithms.     

Influence of visual targets and landmarks on honey bee foraging and waggle dancing

Animals use diverse sensory stimuli to navigate their environment and to recognize rewarding food sources.Honey bees use visual atributes of the targeted food source,such as its color,shape,size,direction and distance from the hive,and the landmarks around it to navigate during foraging.They transmit the location information of the food source to other bees if it is highly rewarding.To investigate the relative importance of these attributes,we trained bees to feeders in two different experiments.In the first experiment,we asked whether bees prefer to land on(a)a similar feeder at a different distance on the same heading or on(b)a visually distinct feeder located at the exact same location.We found that,within a short foraging range,bees relied heavily on the color and the shape of the food source and to a lesser extent on its distance from the hive.In the second experiment,we asked if moving the main landmark or the feeder(visual target)influenced recruitment dancing for the feeder.We found that foragers took longer to land and danced fewer circuits when the location of the food source,or a major landmark associated with it,changed.These results demonstrate that prominent visual atributes of food sources and landmarks are evidently more reliable than distance information and that foraging bees heavily utilize these visual cues at the later stages of their journey.     

Establishment of lal-/- Myeloid Lineage Cell Line That Resembles Myeloid-Derived Suppressive Cells

Myeloid-derived suppressor cells (MDSCs) in mouse are inflammatory cells that play critical roles in promoting cancer growth and metastasis by directly stimulating cancer cell proliferation and suppressing immune surveillance. In order to facilitate characterization of biochemical and cellular mechanisms of MDSCs, it is urgent to establish an “MDSC-like” cell line. By cross breeding of immortomouse (simian virus 40 large T antigen transgenic mice) with wild type and lysosomal acid lipase (LAL) knock-out (lal-/-) mice, we have established a wild type (HD1A) and a lal-/- (HD1B) myeloid cell lines. Compared with HD1A cells, HD1B cells demonstrated many characteristics similar to lal-/- MDSCs. HD1B cells exhibited increased lysosomes around perinuclear areas, dysfunction of mitochondria skewing toward fission structure, damaged membrane potential, and increased ROS production. HD1B cells showed increased glycolytic metabolism during blockage of fatty acid metabolism to fuel the energy need. Similar to lal-/- MDSCs, the mTOR signal pathway in HD1B cells is overly activated. Rapamycin treatment of HD1B cells reduced ROS production and restored the mitochondrial membrane potential. HD1B cells showed much stronger immunosuppression on CD4⁺ T cell proliferation and function in vitro, and enhanced cancer cells proliferation. Knockdown of mTOR with siRNA reduced the HD1B cell ability to immunosuppress T cells and stimulate cancer cell proliferation. Therefore, the HD1B myeloid cell line is an “MDSC-like” cell line that can be used as an alternative in vitro system to study how LAL controls various myeloid cell functions.     

Development of cue integration in human navigation

Mammalian navigation depends both on visual landmarks and on self-generated (e.g., vestibular and proprioceptive) cues that signal the organism's own movement [1-5]. When these conflict, landmarks can either reset estimates of self-motion or be integrated with them [6-9]. We asked how humans combine these information sources and whether children, who use both from a young age [10-12], combine them as adults do. Participants attempted to return an object to its original place in an arena when given either visual landmarks only, nonvisual self-motion information only, or both. Adults, but not 4- to 5-year-olds or 7- to 8-year-olds, reduced their response variance when both information sources were available. In an additional "conflict" condition that measured relative reliance on landmarks and self-motion, we predicted behavior under two models: integration (weighted averaging) of the cues and alternation between them. Adults' behavior was predicted by integration, in which the cues were weighted nearly optimally to reduce variance, whereas children's behavior was predicted by alternation. These results suggest that development of individual spatial-representational systems precedes development of the capacity to combine these within a common reference frame. Humans can integrate spatial cues nearly optimally to navigate, but this ability depends on an extended developmental process.     

Bottlenecks of Motion Processing during a Visual Glance: The Leaky Flask Model

Where do the bottlenecks for information and attention lie when our visual system processes incoming stimuli? The human visual system encodes the incoming stimulus and transfers its contents into three major memory systems with increasing time scales, viz., sensory (or iconic) memory, visual short-term memory (VSTM), and long-term memory (LTM). It is commonly believed that the major bottleneck of information processing resides in VSTM. In contrast to this view, we show major bottlenecks for motion processing prior to VSTM. In the first experiment, we examined bottlenecks at the stimulus encoding stage through a partial-report technique by delivering the cue immediately at the end of the stimulus presentation. In the second experiment, we varied the cue delay to investigate sensory memory and VSTM. Performance decayed exponentially as a function of cue delay and we used the time-constant of the exponential-decay to demarcate sensory memory from VSTM. We then decomposed performance in terms of quality and quantity measures to analyze bottlenecks along these dimensions. In terms of the quality of information, two thirds to three quarters of the motion-processing bottleneck occurs in stimulus encoding rather than memory stages. In terms of the quantity of information, the motion-processing bottleneck is distributed, with the stimulus-encoding stage accounting for one third of the bottleneck. The bottleneck for the stimulus-encoding stage is dominated by the selection compared to the filtering function of attention. We also found that the filtering function of attention is operating mainly at the sensory memory stage in a specific manner, i.e., influencing only quantity and sparing quality. These results provide a novel and more complete understanding of information processing and storage bottlenecks for motion processing.     

Learning and time‐dependent cue choice in the desert ant,Melophorus bagoti

Foraging ants are known to use multiple sources of information to return to the nest. These cue sets are employed by independent navigational systems including path integration in the case of celestial cues and vision‐based learning in the case of terrestrial landmarks and the panorama. When cue sets are presented in conflict, the Australian desert ant species, Melophorus bagoti, will choose a compromise heading between the directions dictated by the cues or, when navigating on well‐known routes, foragers choose the direction indicated by the terrestrial cues of the panorama against the dictates of celestial cues. Here, we explore the roles of learning terrestrial cues and delays since cue exposure in these navigational decisions by testing restricted foragers with differing levels of terrestrial cue experience with the maximum (180°) cue conflict. Restricted foragers appear unable to extrapolate landmark information from the nest to a displacement site 8 m away. Given only one homeward experience, foragers can successfully orient using terrestrial cues, but this experience is not sufficient to override a conflicting vector. Terrestrial cue strength increases with multiple experiences and eventually overrides the celestial cues. This appears to be a dynamic choice as foragers discount the reliability of the terrestrial cues over time, reverting back to preferring the celestial vector when the forager has an immediate vector, but the forager's last exposure to the terrestrial cues was 24 hr in the past. Foragers may be employing navigational decision making that can be predicted by the temporal weighting rule.     

A fine-structure gynandromorph fate map of the Drosophila head

A gynandromorph fate map of the head of D. melanogaster was produced using 28 landmarks derived from one imaginal disc. An examination of the meaning of fine-structure mapping discloses that the sturt value observed between one pair of landmarks within a disc may approximate the relative physical distance of their progenitor cells at blastoderm, but for another pair of landmarks (assuming no directed cell movements), the sturt value may simply reflect their close geographic location at the time the cells are specified for their particular differentiation, a time much later in development when most cell division within the disc has come to an end. The formation of early developmental compartments has little effect on fate-map distances. Our analysis of the data suggests there are approximately ten cells present at the blastoderm stage that are head progenitors. Each blastoderm cell is likely to be the progenitor of a particular array of landmarks, but there is overlap between arrays from different blastoderm cells.     

Orientation and Communication in the Neotropical Ant Odontomachus bauri Emery (Hymenoptera,Formicidae, Ponerinae)

The Neotropical species Odontomachus bauri employs canopy orientation during foraging and homing. An artificial canopy pattern above the ants is much more effective as an orientation cue than horizontal landmarks or chemical marks. However, both horizontal visual cues and chemical marks on the ground can serve in localizing the nest entrance. Successful O. bauri foragers recruit nestmates to leave the nest and search for food. However, the recruitment signals do not contain directional information. Antennation bouts and pheromones from the pygidial gland most likely serve as stimulating recruitment signals. Secretions from the mandibular and poison gland elicit alarm and attack behavior.