Accurate navigation often requires the maintenance of a robust internal estimate of heading relative to external surroundings. We present a model for angular velocity integration in a desert locust heading circuit, applying concepts from early theoretical work on heading circuits in mammals to a novel biological context in insects. In contrast to similar models proposed for the fruit fly, this circuit model uses a single 360° heading direction representation and is updated by neuromodulatory angular velocity inputs. Our computational model was implemented using steady-state firing rate neurons with dynamical synapses. The circuit connectivity was constrained by biological data, and remaining degrees of freedom were optimised with a machine learning approach to yield physiologically plausible neuron activities. We demonstrate that the integration of heading and angular velocity in this circuit is robust to noise. The heading signal can be effectively used as input to an existing insect goal-directed steering circuit, adapted for outbound locomotion in a steady direction that resembles locust migration. Our study supports the possibility that similar computations for orientation may be implemented differently in the neural hardware of the fruit fly and the locust.

Animals can learn in real-life scenarios where rewards are often only available when a goal is achieved. This 'distal' or 'sparse' reward problem remains a challenge for conventional reinforcement learning algorithms. Here we investigate an algorithm for learning in such scenarios, inspired by the possibility that axo-axonal gap junction connections, observed in neural circuits with parallel fibres such as the insect mushroom body, could form a resistive network. In such a network, an active node represents the task state, connections between nodes represent state transitions and their connection to actions, and current flow to a target state can guide decision making. Building on evidence that gap junction weights are adaptive, we propose that experience of a task can modulate the connections to form a graph encoding the task structure. We demonstrate that the approach can be used for efficient reinforcement learning under sparse rewards, and discuss whether it is plausible as an account of the insect mushroom body.

The insect central complex appears to encode and process spatial information through vector manipulation. Here, we draw on recent insights into circuit structure to fuse previous models of sensory-guided navigation, path integration and vector memory. Specifically, we propose that the allocentric encoding of location provided by path integration creates a spatially stable anchor for converging sensory signals that is relevant in multiple behavioural contexts. The allocentric reference frame given by path integration transforms a goal direction into a goal location and we demonstrate through modelling that it can enhance approach of a sensory target in noisy, cluttered environments or with temporally sparse stimuli. We further show the same circuit can improve performance in the more complex navigational task of route following. The model suggests specific functional roles for circuit elements of the central complex that helps explain their high preservation across insect species.

Neural circuits undergo developmental processes which can be influenced by experience. Here we explore a bio-inspired development process to form the connections in a network used for locality sensitive hashing. The network is a simplified model of the insect mushroom body, which has sparse connections from the input layer to a second layer of higher dimension, forming a sparse code. In previous versions of this model, connectivity between the layers is random. We investigate whether the performance of the hash, evaluated in nearest neighbour query tasks, can be improved by process of developing the connections, in which the strongest input dimensions in successive samples are wired to each successive coding dimension. Experiments show that the accuracy of searching for nearest neighbours is improved, although performance is dependent on the parameter values and datasets used. Our approach is also much faster than alternative methods that have been proposed for training the connections in this model. Importantly, the development process does not impact connections built at an earlier stage, which should provide stable coding results for simultaneous learning in a downstream network.

Many animal behaviors require orientation and steering with respect to the environment. For insects, a key brain area involved in spatial orientation and navigation is the central complex. Activity in this neural circuit has been shown to track the insect's current heading relative to its environment and has also been proposed to be the substrate of path integration. However, it remains unclear how the output of the central complex is integrated into motor commands. Central complex output neurons project to the lateral accessory lobes (LAL), from which descending neurons project to thoracic motor centers. Here, we present a computational model of a simple neural network that has been described anatomically and physiologically in the LALs of male silkworm moths, in the context of odor-mediated steering. We present and analyze two versions of this network, one rate based and one based on spiking neurons. The modeled network consists of an inhibitory local interneuron and a bistable descending neuron (flip-flop) that both receive input in the LAL. The flip-flop neuron projects onto neck motor neurons to induce steering. We show that this simple computational model not only replicates the basic parameters of male silkworm moth behavior in a simulated odor plume but can also take input from a computational model of path integration in the central complex and use it to steer back to a point of origin. Furthermore, we find that increasing the level of detail within the model improves the realism of the model's behavior, leading to the emergence of looping behavior as an orientation strategy. Our results suggest that descending neurons originating in the LALs, such as flip-flop neurons, are sufficient to mediate multiple steering behaviors. This study is therefore a first step to close the gap between orientation circuits in the central complex and downstream motor centers.

Insects can navigate efficiently in both novel and familiar environments, and this requires flexiblity in how they are guided by sensory cues. A prominent landmark, for example, can elicit strong innate behaviours (attraction or menotaxis) but can also be used, after learning, as a specific directional cue as part of a navigation memory. However, the mechanisms that allow both pathways to co-exist, interact or override each other are largely unknown. Here we propose a model for the behavioural integration of innate and learned guidance based on the neuroanatomy of the central complex (CX), adapted to control landmark guided behaviours. We consider a reward signal provided either by an innate attraction to landmarks or a long-term visual memory in the mushroom bodies (MB) that modulates the formation of a local vector memory in the CX. Using an operant strategy for a simulated agent exploring a simple world containing a single visual cue, we show how the generated short-term memory can support both innate and learned steering behaviour. In addition, we show how this architecture is consistent with the observed effects of unilateral MB lesions in ants that cause a reversion to innate behaviour. We suggest the formation of a directional memory in the CX can be interpreted as transforming rewarding (positive or negative) sensory signals into a mapping of the environment that describes the geometrical attractiveness (or repulsion). We discuss how this scheme might represent an ideal way to combine multisensory information gathered during the exploration of an environment and support optimal cue integration.

Monocular simultaneous localisation and mapping (SLAM) is a cheap and energy efficient way to enable Unmanned Aerial Vehicles (UAVs) to safely navigate managed forests and gather data crucial for monitoring tree health. SLAM research, however, has mostly been conducted in structured human environments, and as such is poorly adapted to unstructured forests. In this paper, we compare the performance of state of the art monocular SLAM systems on forest data and use visual appearance statistics to characterise the differences between forests and other environments, including a photorealistic simulated forest. We find that SLAM systems struggle with all but the most straightforward forest terrain and identify key attributes (lighting changes and in-scene motion) which distinguish forest scenes from “classic” urban datasets. These differences offer an insight into what makes forests harder to map and open the way for targeted improvements. We also demonstrate that even simulations that look impressive to the human eye can fail to properly reflect the difficult attributes of the environment they simulate, and provide suggestions for more closely mimicking natural scenes.

Many insects navigate by integrating the distances and directions travelled on an outward path, allowing direct return to the starting point. Fundamental to the reliability of this process is the use of a neural compass based on external celestial cues. Here we examine how such compass information could be reliably computed by the insect brain, given realistic constraints on the sky polarisation pattern and the insect eye sensor array. By processing the degree of polarisation in different directions for different parts of the sky, our model can directly estimate the solar azimuth and also infer the confidence of the estimate. We introduce a method to correct for tilting of the sensor array, as might be caused by travel over uneven terrain. We also show that the confidence can be used to approximate the change in sun position over time, allowing the compass to remain fixed with respect to 'true north' during long excursions. We demonstrate that the compass is robust to disturbances and can be effectively used as input to an existing neural model of insect path integration. We discuss the plausibility of our model to be mapped to known neural circuits, and to be implemented for robot navigation.

The Drosophila larva executes a stereotypical exploratory routine that appears to consist of stochastic alternation between straight peristaltic crawling and reorientation events through lateral bending. We present a model of larval mechanics for axial and transverse motion over a planar substrate, and use it to develop a simple, reflexive neuromuscular model from physical principles. The mechanical model represents the midline of the larva as a set of point masses which interact with each other via damped translational and torsional springs, and with the environment via sliding friction forces. The neuromuscular model consists of: 1. segmentally localised reflexes that amplify axial compression in order to counteract frictive energy losses, and 2. long-range mutual inhibition between reflexes in distant segments, enabling overall motion of the model larva relative to its substrate. In the absence of damping and driving, the mechanical model produces axial travelling waves, lateral oscillations, and unpredictable, chaotic deformations. The neuromuscular model counteracts friction to recover these motion patterns, giving rise to forward and backward peristalsis in addition to turning. Our model produces spontaneous exploration, even though the nervous system has no intrinsic pattern generating or decision making ability, and neither senses nor drives bending motions. Ultimately, our model suggests a novel view of larval exploration as a deterministic superdiffusion process which is mechanistically grounded in the chaotic mechanics of the body. We discuss how this may provide new interpretations for existing observations at the level of tissue-scale activity patterns and neural circuitry, and provide some experimental predictions that would test the extent to which the mechanisms we present translate to the real larva.

Most approaches for optimisation of neural networks are based on variants of back-propagation. This requires the network to be time invariant and differentiable; neural networks with dynamics are thus generally outside the scope of these methods. Biological neural circuits are highly dynamic yet clearly able to support learning. We propose a reinforcement learning approach inspired by the mechanisms and dynamics of biological synapses. The network weights undergo spontaneous fluctuations, and a reward signal modulates the centre and amplitude of fluctuations to converge to a desired network behaviour. We test the new learning rule on a 2D bipedal walking simulation, using a control system that combines a recurrent neural network, a bio-inspired central pattern generator layer and proportional-integral control, and demonstrate the first successful solution to this benchmark task.

Operant learning is learning based on reinforcement of behaviours. We propose a new hypothesis for operant learning at the single neuron level based on spontaneous fluctuations of synaptic strength caused by receptor dynamics. These fluctuations allow the neural system to explore a space of outputs. If the receptor dynamics are altered by a reinforcement signal the neural system settles to better states, i.e., to match the environmental dynamics that determine reward. Simulations show that this mechanism can support operant learning in a feed-forward neural circuit, a recurrent neural circuit, and a spiking neural circuit controlling an agent learning in a dynamic reward and punishment situation. We discuss how the new principle relates to existing learning rules and observed phenomena of short and long-term potentiation.

Place recognition is a key capability for navigating robots. While significant advances have been achieved on large, stable platforms such as robot cars, achieving robust performance on rapidly manoeuvring platforms in outdoor natural conditions remains a challenge, with few systems able to deal with both variable conditions and large tilt variations caused by rough terrain. Taking inspiration from biology, we propose a novel combination of sensory modality and image processing to obtain a significant improvement in the robustness of sequence-based image matching for place recognition. We use a UV-sensitive fisheye lens camera to segment sky from ground, providing illumination invariance, and encode the resulting binary images using spherical harmonics to enable rotation-invariant image matching. In combination, these methods also produce substantial pitch and roll invariance, as the spherical harmonics for the sky shape are minimally affected, providing the sky remains visible. We evaluate the performance of our method against a leading appearance-invariant technique (SeqSLAM) and a leading viewpoint-invariant technique (FAB-MAP 2.0) on three new outdoor datasets encompassing variable robot heading, tilt, and lighting conditions in both forested and urban environments. The system demonstrates improved condition- and tilt-invariance, enabling robust place recognition during aggressive zigzag manoeuvring along bumpy trails and at tilt angles of up to 60 degrees.

Ants, like many other animals, use visual memory to follow extended routes through complex environments, but it is unknown how their small brains implement this capability. The mushroom body neuropils have been identified as a crucial memory circuit in the insect brain, but their function has mostly been explored for simple olfactory association tasks. We show that a spiking neural model of this circuit originally developed to describe fruitfly (Drosophila melanogaster) olfactory association, can also account for the ability of desert ants (Cataglyphis velox) to rapidly learn visual routes through complex natural environments. We further demonstrate that abstracting the key computational principles of this circuit, which include one-shot learning of sparse codes, enables the theoretical storage capacity of the ant mushroom body to be estimated at hundreds of independent images.

Detailed observations of larval Drosophila chemotaxis have characterised the relationship between the odour gradient and the runs, head casts and turns made by the animal. We use a computational model to test whether hypothesised sensorimotor control mechanisms are sufficient to account for larval behaviour. The model combines three mechanisms based on simple transformations of the recent history of odour intensity at the head location. The first is an increased probability of terminating runs in response to gradually decreasing concentration, the second an increased probability of terminating head casts in response to rapidly increasing concentration, and the third a biasing of run directions up concentration gradients through modulation of small head casts. We show that this model can be tuned to produce behavioural statistics comparable to those reported for the larva, and that this tuning results in similar chemotaxis performance to the larva. We demonstrate that each mechanism can enable odour approach but the combination of mechanisms is most effective, and investigate how these low-level control mechanisms relate to behavioural measures such as the preference indices used to investigate larval learning behaviour in group assays.

Animals such as stick insects can adaptively walk on complex terrains by dynamically adjusting their stepping motion patterns. Inspired by the coupled Matsuoka and resonate-and-fire neuron models, we present a nonlinear oscillation model as the neuromorphic central pattern generator (CPG) for rhythmic stepping pattern generation. This dynamic model can also be used to actuate the motoneurons on a leg joint with adjustable driving frequencies and duty cycles by changing a few of the model parameters while operating such that different stepping patterns can be generated. A novel mixed-signal integrated circuit design of this dynamic model is subsequently implemented, which, although simplified, shares the equivalent output performance in terms of the adjustable frequency and duty cycle. Three identical CPG models being used to drive three joints can make an arthropod leg of three degrees of freedom. With appropriate initial circuit parameter settings, and thus suitable phase lags among joints, the leg is expected to walk on a complex terrain with adaptive steps. The adaptation is associated with the circuit parameters mediated both by the higher level nervous system and the lower level sensory signals. The model is realized using a 0.3- complementary metal-oxide-semiconductor process and the results are reported.

(2002). Swarm Intelligence: From Natural to Artificial Systems. Connection Science: Vol. 14, No. 2, pp. 163-164.

Integrating sensorimotor systems is still a difficult problem for robotics. Biological inspiration, which has been effectively used to address single sensorimotor tasks, could also be applied to this problem. Several studies on the cricket suggest that it integrates an optomotor response to improve its sound localization behaviour. We have taken two existing 'biorobots'-one that uses an a VLSI circuit to reproduce the optomotor behaviour and another that models in hardware and software the sound localization of the cricket-and combined their capabilities to investigate whether an additive combination will reproduce these effects. We report the initial results and discuss a number of issues raised by this investigation.

Crickets are able to extract directional information about a wind stimulus through the filiform hairs located on their cerci. This paper describes the design and testing of a neuromorphic sensor that aims to achieve a close correlation with both the physical and functional properties of these hairs. An integrate and fire neural network is used to process the sensory information in real time. The resulting system is shown to be capable of extracting directional information from a wind stimulus and producing an appropriate motor control pattern.

Modelling is most clearly understood as a adjunct in the process of deriving predictions from hypotheses. By representing a hypothesised mechanism in a model we hope by manipulating the model to understand the hypotheses' consequences. Eight dimensions on which models of biological behaviour can vary are described: the degree of realism with which they apply to biology; the level of biology they represent; the generality or range of systems the model is supposed to cover; the abstraction or amount of biological detail represented; the accuracy of representation of the mechanisms; the medium in which the model is built; the match of the model behaviour to biological behaviour; and the utility of the model in providing biological understanding and/or technical insight. It is hoped this framework will help to clarify debates over different approaches to modelling, particularly by pointing out how the above dimensions are relatively independent and should not be conflated.

Behavioral experiments with crickets show that female crickets respond to male calling songs with syllable rates within a certain bandwidth only. We have made a robot model in which we implement a simple neural controller that is less complex than the controllers traditionally hypothesized for cricket phonotaxis and syllable rate preference. The simple controller, which had been successfully used with a slowed and simplified signal, is here demonstrated to function, using songs with identical parameters to those found in real male cricket song, using an analog electronic model of the peripheral auditory morphology of the female cricket as the sensor. We put the robot under the same experimental conditions as the female crickets, and it responds with phonotaxis to calling songs of real male Gryllus bimaculatus. Further, the robot only responds to songs with syllable rates within a bandwidth similar to the bandwidth found for crickets. By making polar plots of the heading direction of the robot, we obtain behavioral data that can be used in statistical analyses. These analyses show that there are statistically significant differences between the behavioral responses to calling songs with syllable rates within the bandwidth and calling songs with syllable rates outside the bandwidth. This gives the verification that the simple neural control mechanism (together with morphological auditory matched filtering) can account for the syllable rate preference found in female crickets. With our robot system, we can now systematically explore the mechanisms controlling recognition and choice behavior in the female cricket by experimental replication.