Investigating visual navigation using spiking neural network models of the insect mushroom bodies.

Ants are capable of learning long visually guided foraging routes with limited neural resources. The visual scene memory needed for this behaviour is mediated by the mushroom bodies; an insect brain region important for learning and memory. In a visual navigation context, the mushroom bodies are theorised to act as familiarity detectors, guiding ants to views that are similar to those previously learned when first travelling along a foraging route. Evidence from behavioural experiments, computational studies and brain lesions all support this idea. Here we further investigate the role of mushroom bodies in visual navigation with a spiking neural network model learning complex natural scenes. By implementing these networks in GeNN-a library for building GPU accelerated spiking neural networks-we were able to test these models offline on an image database representing navigation through a complex outdoor natural environment, and also online embodied on a robot. The mushroom body model successfully learnt a large series of visual scenes (400 scenes corresponding to a 27 m route) and used these memories to choose accurate heading directions during route recapitulation in both complex environments. Through analysing our model's Kenyon cell (KC) activity, we were able to demonstrate that KC activity is directly related to the respective novelty of input images. Through conducting a parameter search we found that there is a non-linear dependence between optimal KC to visual projection neuron (VPN) connection sparsity and the length of time the model is presented with an image stimulus. The parameter search also showed training the model on lower proportions of a route generally produced better accuracy when testing on the entire route. We embodied the mushroom body model and comparator visual navigation algorithms on a Quanser Q-car robot with all processing running on an Nvidia Jetson TX2. On a 6.5 m route, the mushroom body model had a mean distance to training route (error) of 0.144 ± 0.088 m over 5 trials, which was performance comparable to standard visual-only navigation algorithms. Thus, we have demonstrated that a biologically plausible model of the ant mushroom body can navigate complex environments both in simulation and the real world. Understanding the neural basis of this behaviour will provide insight into how neural circuits are tuned to rapidly learn behaviourally relevant information from complex environments and provide inspiration for creating bio-mimetic computer/robotic systems that can learn rapidly with low energy requirements.

Trail using ants follow idiosyncratic routes in complex landscapes.

A large volume of research on individually navigating ants has shown how path integration and visually guided navigation form a major part of the ant navigation toolkit for many species and are sufficient mechanisms for successful navigation. One of the behavioural markers of the interaction of these mechanisms is that experienced foragers develop idiosyncratic routes that require that individual ants have personal and unique visual memories that they use to guide habitual routes between the nest and feeding sites. The majority of ants, however, inhabit complex cluttered environments and social pheromone trails are often part of the collective recruitment, organisation and navigation of these foragers. We do not know how individual navigation interacts with collective behaviour along shared trails in complex natural environments. We thus asked here if wood ants that forage through densely cluttered woodlands where they travel along shared trails repeatedly follow the same routes or if they choose a spread of paths within the shared trail. We recorded three long homing trajectories of 20 individual wood ants in their natural woodland habitat. We found that wood ants follow idiosyncratic routes when navigating along shared trails through highly complex visual landscapes. This shows that ants rely on individual memories for habitual route guidance even in cluttered environments when chemical trail information is available. We argue that visual cues are likely to be the dominant sensory modality for the idiosyncratic routes. These experiments shed new light on how ants, or insects in general, navigate through complex multimodal environments.

Descending neurons of the hoverfly respond to pursuits of artificial targets.

Many animals use motion vision information to control dynamic behaviors. Predatory animals, for example, show an exquisite ability to detect rapidly moving prey, followed by pursuit and capture. Such target detection is not only used by predators but is also important in conspecific interactions, such as for male hoverflies defending their territories against conspecific intruders. Visual target detection is believed to be subserved by specialized target-tuned neurons found in a range of species, including vertebrates and arthropods. However, how these target-tuned neurons respond to actual pursuit trajectories is currently not well understood. To redress this, we recorded extracellularly from target-selective descending neurons (TSDNs) in male Eristalis tenax hoverflies. We show that they have dorso-frontal receptive fields with a preferred direction up and away from the visual midline. We reconstructed visual flow fields as experienced during pursuits of artificial targets (black beads). We recorded TSDN responses to six reconstructed pursuits and found that each neuron responded consistently at remarkably specific time points but that these time points differed between neurons. We found that the observed spike probability was correlated with the spike probability predicted from each neuron's receptive field and size tuning. Interestingly, however, the overall response rate was low, with individual neurons responding to only a small part of each reconstructed pursuit. In contrast, the TSDN population responded to substantially larger proportions of the pursuits but with lower probability. This large variation between neurons could be useful if different neurons control different parts of the behavioral output.

Geosmin suppresses defensive behaviour and elicits unusual neural responses in honey bees.

Geosmin is an odorant produced by bacteria in moist soil. It has been found to be extraordinarily relevant to some insects, but the reasons for this are not yet fully understood. Here we report the first tests of the effect of geosmin on honey bees. A stinging assay showed that the defensive behaviour elicited by the bee's alarm pheromone component isoamyl acetate (IAA) is strongly suppressed by geosmin. Surprisingly, the suppression is, however, only present at very low geosmin concentrations, and disappears at higher concentrations. We investigated the underlying mechanisms at the level of the olfactory receptor neurons by means of electroantennography, finding the responses to mixtures of geosmin and IAA to be lower than to pure IAA, suggesting an interaction of both compounds at the olfactory receptor level. Calcium imaging of the antennal lobe (AL) revealed that neuronal responses to geosmin decreased with increasing concentration, correlating well with the observed behaviour. Computational modelling of odour transduction and coding in the AL suggests that a broader activation of olfactory receptor types by geosmin in combination with lateral inhibition could lead to the observed non-monotonic increasing-decreasing responses to geosmin and thus underlie the specificity of the behavioural response to low geosmin concentrations.

Production of adaptive movement patterns via an insect inspired spiking neural network central pattern generator.

Navigation in ever-changing environments requires effective motor behaviors. Many insects have developed adaptive movement patterns which increase their success in achieving navigational goals. A conserved brain area in the insect brain, the Lateral Accessory Lobe, is involved in generating small scale search movements which increase the efficacy of sensory sampling. When the reliability of an essential navigational stimulus is low, searching movements are initiated whereas if the stimulus reliability is high, a targeted steering response is elicited. Thus, the network mediates an adaptive switching between motor patterns. We developed Spiking Neural Network models to explore how an insect inspired architecture could generate adaptive movements in relation to changing sensory inputs. The models are able to generate a variety of adaptive movement patterns, the majority of which are of the zig-zagging kind, as seen in a variety of insects. Furthermore, these networks are robust to noise. Because a large spread of network parameters lead to the correct movement dynamics, we conclude that the investigated network architecture is inherently well-suited to generating adaptive movement patterns.

Non-synaptic interactions between olfactory receptor neurons, a possible key feature of odor processing in flies.

When flies explore their environment, they encounter odors in complex, highly intermittent plumes. To navigate a plume and, for example, find food, they must solve several challenges, including reliably identifying mixtures of odorants and their intensities, and discriminating odorant mixtures emanating from a single source from odorants emitted from separate sources and just mixing in the air. Lateral inhibition in the antennal lobe is commonly understood to help solving these challenges. With a computational model of the Drosophila olfactory system, we analyze the utility of an alternative mechanism for solving them: Non-synaptic ("ephaptic") interactions (NSIs) between olfactory receptor neurons that are stereotypically co-housed in the same sensilla. We find that NSIs improve mixture ratio detection and plume structure sensing and do so more efficiently than the traditionally considered mechanism of lateral inhibition in the antennal lobe. The best performance is achieved when both mechanisms work in synergy. However, we also found that NSIs decrease the dynamic range of co-housed ORNs, especially when they have similar sensitivity to an odorant. These results shed light, from a functional perspective, on the role of NSIs, which are normally avoided between neurons, for instance by myelination.

Arpra: An Arbitrary Precision Range Analysis Library.

Motivated by the challenge of investigating the reproducibility of spiking neural network simulations, we have developed the Arpra library: an open source C library for arbitrary precision range analysis based on the mixed Interval Arithmetic (IA)/Affine Arithmetic (AA) method. Arpra builds on this method by implementing a novel mixed trimmed IA/AA, in which the error terms of AA ranges are minimised using information from IA ranges. Overhead rounding error is minimised by computing intermediate values as extended precision variables using the MPFR library. This optimisation is most useful in cases where the ratio of overhead error to range width is high. Three novel affine term reduction strategies improve memory efficiency by merging affine terms of lesser significance. We also investigate the viability of using mixed trimmed IA/AA and other AA methods for studying reproducibility in unstable spiking neural network simulations.

PyGeNN: A Python Library for GPU-Enhanced Neural Networks.

More than half of the Top 10 supercomputing sites worldwide use GPU accelerators and they are becoming ubiquitous in workstations and edge computing devices. GeNN is a C++ library for generating efficient spiking neural network simulation code for GPUs. However, until now, the full flexibility of GeNN could only be harnessed by writing model descriptions and simulation code in C++. Here we present PyGeNN, a Python package which exposes all of GeNN's functionality to Python with minimal overhead. This provides an alternative, arguably more user-friendly, way of using GeNN and allows modelers to use GeNN within the growing Python-based machine learning and computational neuroscience ecosystems. In addition, we demonstrate that, in both Python and C++ GeNN simulations, the overheads of recording spiking data can strongly affect runtimes and show how a new spike recording system can reduce these overheads by up to 10×. Using the new recording system, we demonstrate that by using PyGeNN on a modern GPU, we can simulate a full-scale model of a cortical column faster even than real-time neuromorphic systems. Finally, we show that long simulations of a smaller model with complex stimuli and a custom three-factor learning rule defined in PyGeNN can be simulated almost two orders of magnitude faster than real-time.

Learning with reinforcement prediction errors in a model of the Drosophila mushroom body.

Effective decision making in a changing environment demands that accurate predictions are learned about decision outcomes. In Drosophila, such learning is orchestrated in part by the mushroom body, where dopamine neurons signal reinforcing stimuli to modulate plasticity presynaptic to mushroom body output neurons. Building on previous mushroom body models, in which dopamine neurons signal absolute reinforcement, we propose instead that dopamine neurons signal reinforcement prediction errors by utilising feedback reinforcement predictions from output neurons. We formulate plasticity rules that minimise prediction errors, verify that output neurons learn accurate reinforcement predictions in simulations, and postulate connectivity that explains more physiological observations than an experimentally constrained model. The constrained and augmented models reproduce a broad range of conditioning and blocking experiments, and we demonstrate that the absence of blocking does not imply the absence of prediction error dependent learning. Our results provide five predictions that can be tested using established experimental methods.

Dynamics of a Mutual Inhibition Circuit between Pyramidal Neurons Compared to Human Perceptual Competition.

Neural competition plays an essential role in active selection processes of noisy and ambiguous input signals, and it is assumed to underlie emergent properties of brain functioning, such as perceptual organization and decision-making. Despite ample theoretical research on neural competition, experimental tools to allow neurophysiological investigation of competing neurons have not been available. We developed a "hybrid" system where real-life neurons and a computer-simulated neural circuit interacted. It enabled us to construct a mutual inhibition circuit between two real-life pyramidal neurons. We then asked what dynamics this minimal unit of neural competition exhibits and compared them with the known behavioral-level dynamics of neural competition. We found that the pair of neurons shows bistability when activated simultaneously by current injections. The addition of modeled synaptic noise and changes in the activation strength showed that the dynamics of the circuit are strikingly similar to the known properties of bistable visual perception: The distribution of dominance durations showed a right-skewed shape, and the changes of the activation strengths caused changes in dominance, dominance durations, and reversal rates as stated in the well-known empirical laws of bistable perception known as Levelt's propositions.SIGNIFICANCE STATEMENT Visual perception emerges as the result of neural systems actively organizing visual signals that involves selection processes of competing neurons. While the neural competition, realized by a "mutual inhibition" circuit has been examined in many theoretical studies, its properties have not been investigated in real neurons. We have developed a "hybrid" system where two real-life pyramidal neurons in a mouse brain slice interact through a computer-simulated mutual inhibition circuit. We found that simultaneous activation of the neurons leads to bistable activity. We investigated the effect of noise and the effect of changes in the activation strength on the dynamics. We observed that the pair of neurons exhibit dynamics strikingly similar to the known properties of bistable visual perception.

Larger GPU-accelerated brain simulations with procedural connectivity.

Simulations are an important tool for investigating brain function but large models are needed to faithfully reproduce the statistics and dynamics of brain activity. Simulating large spiking neural network models has, until now, needed so much memory for storing synaptic connections that it required high performance computer systems. Here, we present an alternative simulation method we call 'procedural connectivity' where connectivity and synaptic weights are generated 'on the fly' instead of stored and retrieved from memory. This method is particularly well suited for use on graphical processing units (GPUs)-which are a common fixture in many workstations. Using procedural connectivity and an additional GPU code generation optimization, we can simulate a recent model of the macaque visual cortex with 4.13 × 106 neurons and 24.2 × 109 synapses on a single GPU-a significant step forward in making large-scale brain modeling accessible to more researchers.

Brian2GeNN: accelerating spiking neural network simulations with graphics hardware.

"Brian" is a popular Python-based simulator for spiking neural networks, commonly used in computational neuroscience. GeNN is a C++-based meta-compiler for accelerating spiking neural network simulations using consumer or high performance grade graphics processing units (GPUs). Here we introduce a new software package, Brian2GeNN, that connects the two systems so that users can make use of GeNN GPU acceleration when developing their models in Brian, without requiring any technical knowledge about GPUs, C++ or GeNN. The new Brian2GeNN software uses a pipeline of code generation to translate Brian scripts into C++ code that can be used as input to GeNN, and subsequently can be run on suitable NVIDIA GPU accelerators. From the user's perspective, the entire pipeline is invoked by adding two simple lines to their Brian scripts. We have shown that using Brian2GeNN, two non-trivial models from the literature can run tens to hundreds of times faster than on CPU.

The Emergence of a Stable Neuronal Ensemble from a Wider Pool of Activated Neurons in the Dorsal Medial Prefrontal Cortex during Appetitive Learning in Mice.

Animals selectively respond to environmental cues associated with food reward to optimize nutrient intake. Such appetitive conditioned stimulus-unconditioned stimulus (CS-US) associations are thought to be encoded in select, stable neuronal populations or neuronal ensembles, which undergo physiological modifications during appetitive conditioning. These ensembles in the medial prefrontal cortex (mPFC) control well-established, cue-evoked food seeking, but the mechanisms involved in the genesis of these ensembles are unclear. Here, we used male Fos-GFP mice that express green fluorescent protein (GFP) in recently behaviorally activated neurons, to reveal how dorsal mPFC neurons are recruited and modified to encode CS-US memory representations using an appetitive conditioning task. In the initial conditioning session, animals did not exhibit discriminated, cue-selective food seeking, but did so in later sessions indicating that a CS-US association was established. Using microprism-based in vivo 2-Photon imaging, we revealed that only a minority of neurons activated during the initial session was consistently activated throughout subsequent conditioning sessions and during cue-evoked memory recall. Notably, using ex vivo electrophysiology, we found that neurons activated following the initial session exhibited transient hyperexcitability. Chemogenetically enhancing the excitability of these neurons throughout subsequent conditioning sessions interfered with the development of reliable cue-selective food seeking, indicated by persistent, nondiscriminated performance. We demonstrate how appetitive learning consistently activates a subset of neurons to form a stable neuronal ensemble during the formation of a CS-US association. This ensemble may arise from a pool of hyperexcitable neurons activated during the initial conditioning session.SIGNIFICANCE STATEMENT Appetitive conditioning endows cues associated with food with the ability to guide food-seeking, through the formation of a food-cue association. Neuronal ensembles in the mPFC control established cue-evoked food-seeking. However, how neurons undergo physiological modifications and become part of an ensemble during conditioning remain unclear. We found that only a minority of dorsal mPFC neurons activated on the initial conditioning session became consistently activated during conditioning and memory recall. These initially activated neurons were also transiently hyperexcitable. We demonstrate the following: (1) how stable neuronal ensemble formation in the dorsal mPFC underlies appetitive conditioning; and (2) how this ensemble may arise from hyperexcitable neurons activated before the establishment of cue-evoked food seeking.

Odor Stimuli: Not Just Chemical Identity.

In most sensory modalities the underlying physical phenomena are well understood, and stimulus properties can be precisely controlled. In olfaction, the situation is different. The presence of specific chemical compounds in the air (or water) is the root cause for perceived odors, but it remains unknown what organizing principles, equivalent to wavelength for light, determine the dimensions of odor space. Equally important, but less in the spotlight, odor stimuli are also complex with respect to their physical properties, including concentration and time-varying spatio-temporal distribution. We still lack a complete understanding or control over these properties, in either experiments or theory. In this review, we will concentrate on two important aspects of the physical properties of odor stimuli beyond the chemical identity of the odorants: (1) The amplitude of odor stimuli and their temporal dynamics. (2) The spatio-temporal structure of odor plumes in a natural environment. Concerning these issues, we ask the following questions: (1) Given any particular experimental protocol for odor stimulation, do we have a realistic estimate of the odorant concentration in the air, and at the olfactory receptor neurons? Can we control, or at least know, the dynamics of odorant concentration at olfactory receptor neurons? (2) What do we know of the spatio-temporal structure of odor stimuli in a natural environment both from a theoretical and experimental perspective? And how does this change if we consider mixtures of odorants? For both topics, we will briefly summarize the underlying principles of physics and review the experimental and theoretical Neuroscience literature, focusing on the aspects that are relevant to animals' physiology and behavior. We hope that by bringing the physical principles behind odor plume landscapes to the fore we can contribute to promoting a new generation of experiments and models.

Role of physical medicine for cancer rehabilitation and return to work under the premise of the "Wiedereingliederungsteilzeitgesetz".

BACKGROUND: With the intention of enabling people a phased return to work after long-term sick leave the so-called "Wiedereingliederungsteilzeitgesetz" (WIETZ) was implemented in Austria on 1 July 2017. METHODS: To explore the overall awareness about the WIETZ and the value of physical modalities together with further supporting measures in return to work of cancer survivors, a survey by using a self-constructed questionnaire was performed in 30 experts 6 months after the WIETZ came into force. RESULTS: The awareness of Austrian specialists regarding the WIETZ seems to be excellent. Regarding expert opinions, return to work in cancer survivors is notable hampered in workplaces with great physical stress even in times of the WIETZ, whereas for professions in offices and banks it is easier to return to work, with and without WIETZ. The highest impact on return to work seems to be due to exercise, as an intervention of the field of physical medicine and rehabilitation to improve sensorimotor functions and to increase endurance capacity as well as muscular strength. CONCLUSION: Early information about cancer rehabilitation and the WIETZ seems to be necessary to facilitate return to work of cancer survivors. Furthermore, exercise interventions seem to be the most important measures from the field of physical medicine and rehabilitation.

An unsupervised neuromorphic clustering algorithm.

Brains perform complex tasks using a fraction of the power that would be required to do the same on a conventional computer. New neuromorphic hardware systems are now becoming widely available that are intended to emulate the more power efficient, highly parallel operation of brains. However, to use these systems in applications, we need "neuromorphic algorithms" that can run on them. Here we develop a spiking neural network model for neuromorphic hardware that uses spike timing-dependent plasticity and lateral inhibition to perform unsupervised clustering. With this model, time-invariant, rate-coded datasets can be mapped into a feature space with a specified resolution, i.e., number of clusters, using exclusively neuromorphic hardware. We developed and tested implementations on the SpiNNaker neuromorphic system and on GPUs using the GeNN framework. We show that our neuromorphic clustering algorithm achieves results comparable to those of conventional clustering algorithms such as self-organizing maps, neural gas or k-means clustering. We then combine it with a previously reported supervised neuromorphic classifier network to demonstrate its practical use as a neuromorphic preprocessing module.

Correction to: Computing reward prediction errors and learning valence in the insect mushroom body.

Following the publication of the original article [1], it was highlighted that an old version of the text for abstract P252 was published, thereby causing the text to no longer correspond with Fig. 1.