Impact of central complex lesions on innate and learnt visual navigation in ants.

Wood ants are excellent navigators, using a combination of innate and learnt navigational strategies to travel between their nest and feeding sites. Visual navigation in ants has been studied extensively, however, we have little direct evidence for the underlying neural mechanisms. Here, we perform lateralized mechanical lesions in the central complex (CX) of wood ants, a midline structure known to allow an insect to keep track of the direction of sensory cues relative to its own orientation and to control movement. We lesioned two groups of ants and observed their behaviour in an arena with a large visual landmark present. The first group of ants were naïve and when intact such ants show a clear innate attraction to the conspicuous landmark. The second group of ants were trained to aim to a food location to the side of the landmark. The general heading of naïve ants towards a visual cue was not altered by the lesions, but the heading of ants trained to a landmark adjacent food position was affected. Thus, CX lesions had a specific impact on learnt visual guidance. We also observed that lateralised lesions altered the fine details of turning with lesioned ants spending less time turning to the side ipsilateral of the lesion. The results confirm the role of the CX in turn control and highlight its important role in the implementation of learnt behaviours that rely on information from other brain regions.

Artificial light impairs local attraction to females in male glow-worms.

The negative effects of artificial lighting at night (ALAN) on insects are increasingly recognised and have been postulated as one possible cause of declines in insect populations. Yet, the behavioural mechanisms underpinning ALAN effects on insects remain unclear. ALAN interferes with the bioluminescent signal female glow-worms use to attract males, disrupting reproduction. To determine the behavioural mechanisms that underpin this effect of ALAN, we quantified the effect of white illumination on males' ability to reach a female-mimicking LED within a Y-maze. We show that as the intensity of illumination increases, the proportion of males reaching the female-mimicking LED declines. Brighter illumination also increases the time taken by males to reach the female-mimicking LED. This is a consequence of males spending more time: (i) in the central arm of the Y-maze; and (ii) with their head retracted beneath their head shield. These effects reverse rapidly when illumination is removed, suggesting that male glow-worms are averse to white light. Our results show that ALAN not only prevents male glow-worms from reaching females, but also increases the time they take to reach females and the time they spend avoiding exposure to light. This demonstrates that the impacts of ALAN on male glow-worms extend beyond those previously observed in field experiments, and raises the possibility that ALAN has similar behavioural impacts on other insect species that remain undetected in field experiments.

A unified mechanism for innate and learned visual landmark guidance in the insect central complex.

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.

Predictors of UK postgraduate researcher attendance behaviours and mental health-related attrition intention.

High rates of postgraduate researchers (PGRs) terminate their studies early. This attrition can have detrimental personal consequences, and results in a loss of productivity, and research and innovation for the higher education sector and society as a whole. PGRs are vulnerable to the experience of mental health problems; a factor that appears to be increasing attrition amongst students in the UK. However, investigation of the determinants of problems with PGRs' attendance and influencing intention to discontinue their studies is rare. Here, we consider the relative predictive validity of a set of putative predictors (mental health symptoms, demographic, occupational, psychological, social, and relational) of attendance behaviours (absenteeism, presenteeism, mental health-related intermission) and early attrition intention amongst UK PGRs. Depression, anxiety, and suicidality predicted attendance behaviours and greater attrition intention. Individual demographic and occupational factors predicted all outcomes. Psychological, social and relational factors had less predictive validity, although individual variables in these conceptual clusters did significantly predict some outcomes. Our results suggest that interventions to reduce high rates of mental health problems are likely to improve attendance behaviours, and reduce the extent to which PGRs intermit or consider ending their PhD studies for mental health-related reasons. Initiatives designed to improve supervisory relationships and reduce loneliness may also reduce absenteeism, intermission and attrition intention.

Larval nutrition impacts survival to adulthood, body size and the allometric scaling of metabolic rate in adult honeybees.

Resting metabolic rate (RMR) is a fundamental physiological measure linked to numerous aspects of organismal function, including lifespan. Although dietary restriction in insects during larval growth/development affects adult RMR, the impact of the nutritional composition of larval diets (i.e. diet quality) on adult RMR has not been studied. Using in vitro rearing to control larval diet quality, we determined the effect of dietary protein and carbohydrate on honeybee survival to adulthood, time to eclosion, body mass/size and adult RMR. High carbohydrate larval diets increased survival to adulthood and time to eclosion compared with both low carbohydrate and high protein diets. Upon emergence, bees reared on the high protein diet were smaller and lighter than those reared on other diets, whilst those raised on the high carbohydrate diet varied more in body mass. Newly emerged adult bees reared on the high carbohydrate diet showed a significantly steeper increase in allometric scaling of RMR compared with those reared on other diets. This suggests that the nutritional composition of larval diets influences survival to adulthood, time to eclosion and the allometric scaling of RMR. Given that agricultural intensification and increasing urbanisation have led to a decrease in both forage availability and dietary diversity for bees, our results are critical to improving understanding of the impacts of poor developmental nutrition on bee growth/development and physiology.

Lateralization of short- and long-term visual memories in an insect.

The formation of memories within the vertebrate brain is lateralized between hemispheres across multiple modalities. However, in invertebrates evidence for lateralization is restricted to olfactory memories, primarily from social bees. Here, we use a classical conditioning paradigm with a visual conditioned stimulus to show that visual memories are lateralized in the wood ant, Formica rufa. We show that a brief contact between a sugar reward and either the right or left antenna (reinforcement) is sufficient to produce a lateralized memory, even though the visual cue is visible to both eyes throughout training and testing. Reinforcement given to the right antenna induced short-term memories, whereas reinforcement given to the left antenna induced long-term memories. Thus, short- and long-term visual memories are lateralized in wood ants. This extends the modalities across which memories are lateralized in insects and suggests that such memory lateralization may have evolved multiple times, possibly linked to the evolution of eusociality in the Hymenoptera.

Artificial lighting impairs mate attraction in a nocturnal capital breeder.

Artificial lighting at night (ALAN) is increasingly recognised as having negative effects on many organisms, though the exact mechanisms remain unclear. Glow worms are likely susceptible to ALAN because females use bioluminescence to signal to attract males. We quantified the impact of ALAN by comparing the efficacy of traps that mimicked females to attract males in the presence or absence of a white artificial light source (ALS). Illuminated traps attracted fewer males than did traps in the dark. Illuminated traps closer to the ALS attracted fewer males than those further away, whereas traps in the dark attracted similar numbers of males up to 40 m from the ALS. Thus, ALAN impedes females' ability to attract males, the effect increasing with light intensity. Consequently, ALAN potentially affects glow worms' fecundity and long-term population survival. More broadly, this study emphasises the potentially severe deleterious effects of ALAN upon nocturnal insect populations.

A motion compensation treadmill for untethered wood ants (Formica rufa): evidence for transfer of orientation memories from free-walking training.

The natural scale of insect navigation during foraging makes it challenging to study under controlled conditions. Virtual reality and trackball setups have offered experimental control over visual environments while studying tethered insects, but potential limitations and confounds introduced by tethering motivates the development of alternative untethered solutions. In this paper, we validate the use of a motion compensator (or 'treadmill') to study visually driven behaviour of freely moving wood ants (Formica rufa). We show how this setup allows naturalistic walking behaviour and preserves foraging motivation over long time frames. Furthermore, we show that ants are able to transfer associative and navigational memories from classical maze and arena contexts to our treadmill. Thus, we demonstrate the possibility to study navigational behaviour over ecologically relevant durations (and virtual distances) in precisely controlled environments, bridging the gap between natural and highly controlled laboratory experiments.

Prey speed influences the speed and structure of the raptorial strike of a 'sit-and-wait' predator.

Predators must often employ flexible strategies to capture prey. Particular attention has been given to the strategies of visual predators that actively pursue their prey, but sit-and-wait predators have been largely overlooked, their strategies often characterized as stereotyped. Praying mantids are primarily sit-and-wait predators that often employ crypsis to catch their prey using a raptorial strike produced by their highly modified forelimbs. Here, we show that the raptorial strike of the Madagascan marbled mantis (Polyspilota aeruginosa) varies in duration from 60 to 290 ms due to the tibial extension alone; slower strikes involve slower tibial extensions that may also be interrupted by a pause. The success of a strike is independent of its duration or the presence of these pauses. However, prey speed affects the duration of tibial extension and the probability of a pause occurring, both increasing at slower prey speeds. Adjusting the duration of the tibial extension according to prey speed allows mantids to time the final downward sweep of the tibia to their prey's approach. The use of visual inputs to adjust the motor pattern controlling forelimb movements shows that not all aspects of the strike are stereotyped and that sit-and-wait predators can produce behavioural flexibility.

Modulation of voltage-dependent K+ conductances in photoreceptors trades off investment in contrast gain for bandwidth.

Modulation is essential for adjusting neurons to prevailing conditions and differing demands. Yet understanding how modulators adjust neuronal properties to alter information processing remains unclear, as is the impact of neuromodulation on energy consumption. Here we combine two computational models, one Hodgkin-Huxley type and the other analytic, to investigate the effects of neuromodulation upon Drosophila melanogaster photoreceptors. Voltage-dependent K+ conductances in these photoreceptors: (i) activate upon depolarisation to reduce membrane resistance and adjust bandwidth to functional requirements; (ii) produce negative feedback to increase bandwidth in an energy efficient way; (iii) produce shunt-peaking thereby increasing the membrane gain bandwidth product; and (iv) inactivate to amplify low frequencies. Through their effects on the voltage-dependent K+ conductances, three modulators, serotonin, calmodulin and PIP2, trade-off contrast gain against membrane bandwidth. Serotonin shifts the photoreceptor performance towards higher contrast gains and lower membrane bandwidths, whereas PIP2 and calmodulin shift performance towards lower contrast gains and higher membrane bandwidths. These neuromodulators have little effect upon the overall energy consumed by photoreceptors, instead they redistribute the energy invested in gain versus bandwidth. This demonstrates how modulators can shift neuronal information processing within the limitations of biophysics and energy consumption.

Metabolic rate scaling, ventilation patterns and respiratory water loss in red wood ants: activity drives ventilation changes, metabolic rate drives water loss.

Metabolic rate and its relationship with body size is a fundamental determinant of many life history traits and potentially of organismal fitness. Alongside various environmental and physiological factors, the metabolic rate of insects is linked to distinct ventilation patterns. Despite significant attention, however, the precise role of these ventilation patterns remains uncertain. Here, we determined the allometric scaling of metabolic rate and respiratory water loss in the red wood ant, as well as assessing the effect of movement upon metabolic rate and ventilation pattern. Metabolic rate and respiratory water loss are both negatively allometric. We observed both continuous and cyclic ventilation associated with relatively higher and lower metabolic rates, respectively. In wood ants, however, movement not metabolic rate is the primary determinant of which ventilation pattern is performed. Conversely, metabolic rate not ventilation pattern is the primary determinant of respiratory water loss. Our statistical models produced a range of relatively shallow intraspecific scaling exponents between 0.40 and 0.59, emphasising the dependency upon model structure. Previous investigations have revealed substantial variation in morphological allometry among wood ant workers from different nests within a population. Metabolic rate scaling does not exhibit the same variability, suggesting that these two forms of scaling respond to environmental factors in different ways.

Visual associative learning in wood ants.

Wood ants are a model system for studying visual learning and navigation. They can forage for food and navigate to their nests effectively by forming memories of visual features in their surrounding environment. Previous studies of freely behaving ants have revealed many of the behavioural strategies and environmental features necessary for successful navigation. However, little is known about the exact visual properties of the environment that animals learn or the neural mechanisms that allow them to achieve this. As a first step towards addressing this, we developed a classical conditioning paradigm for visual learning in harnessed wood ants that allows us to control precisely the learned visual cues. In this paradigm, ants are fixed and presented with a visual cue paired with an appetitive sugar reward. Using this paradigm, we found that visual cues learnt by wood ants through Pavlovian conditioning are retained for at least 1 h. Furthermore, we found that memory retention is dependent upon the ants' performance during training. Our study provides the first evidence that wood ants can form visual associative memories when restrained. This classical conditioning paradigm has the potential to permit detailed analysis of the dynamics of memory formation and retention, and the neural basis of learning in wood ants.

Differential scaling within an insect compound eye.

Environmental and genetic influences cause individuals of a species to differ in size. As they do so, organ size and shape are scaled to available resources whilst maintaining function. The scaling of entire organs has been investigated extensively but scaling within organs remains poorly understood. By making use of the structure of the insect compound eye, we show that different regions of an organ can respond differentially to changes in body size. Wood ant (Formica rufa) compound eyes contain facets of different diameters in different regions. When the animal body size changes, lens diameters from different regions can increase or decrease in size either at the same rate (a 'grade' shift) or at different rates (a 'slope' shift). These options are not mutually exclusive, and we demonstrate that both types of scaling apply to different regions of the same eye. This demonstrates that different regions within a single organ can use different rules to govern their scaling, responding differently to their developmental environment. Thus, the control of scaling is more nuanced than previously appreciated, diverse responses occurring even among homologous cells within a single organ. Such fine control provides a rich substrate for the diversification of organ morphology.

Strength of forelimb lateralization predicts motor errors in an insect.

Lateralized behaviours are widespread in both vertebrates and invertebrates, suggesting that lateralization is advantageous. Yet evidence demonstrating proximate or ultimate advantages remains scarce, particularly in invertebrates or in species with individual-level lateralization. Desert locusts (Schistocerca gregaria) are biased in the forelimb they use to perform targeted reaching across a gap. The forelimb and strength of this bias differed among individuals, indicative of individual-level lateralization. Here we show that strongly biased locusts perform better during gap-crossing, making fewer errors with their preferred forelimb. The number of targeting errors locusts make negatively correlates with the strength of forelimb lateralization. This provides evidence that stronger lateralization confers an advantage in terms of improved motor control in an invertebrate with individual-level lateralization.

Acquisition and expression of memories of distance and direction in navigating wood ants.

Wood ants, like other central place foragers, rely on route memories to guide them to and from a reliable food source. They use visual memories of the surrounding scene and probably compass information to control their direction. Do they also remember the length of their route and do they link memories of direction and distance? To answer these questions, we trained wood ant (Formica rufa) foragers in a channel to perform either a single short foraging route or two foraging routes in opposite directions. By shifting the starting position of the route within the channel, but keeping the direction and distance fixed, we tried to ensure that the ants would rely upon vector memories rather than visual memories to decide when to stop. The homeward memories that the ants formed were revealed by placing fed or unfed ants directly into a channel and assessing the direction and distance that they walked without prior performance of the food-ward leg of the journey. This procedure prevented the distance and direction walked being affected by a home vector derived from path integration. Ants that were unfed walked in the feeder direction. Fed ants walked in the opposite direction for a distance related to the separation between start and feeder. Vector memories of a return route can thus be primed by the ants' feeding state and expressed even when the ants have not performed the food-ward route. Tests on ants that have acquired two routes indicate that memories of the direction and distance of the return routes are linked, suggesting that they may be encoded by a common neural population within the ant brain.

Balanced excitatory and inhibitory synaptic currents promote efficient coding and metabolic efficiency.

A balance between excitatory and inhibitory synaptic currents is thought to be important for several aspects of information processing in cortical neurons in vivo, including gain control, bandwidth and receptive field structure. These factors will affect the firing rate of cortical neurons and their reliability, with consequences for their information coding and energy consumption. Yet how balanced synaptic currents contribute to the coding efficiency and energy efficiency of cortical neurons remains unclear. We used single compartment computational models with stochastic voltage-gated ion channels to determine whether synaptic regimes that produce balanced excitatory and inhibitory currents have specific advantages over other input regimes. Specifically, we compared models with only excitatory synaptic inputs to those with equal excitatory and inhibitory conductances, and stronger inhibitory than excitatory conductances (i.e. approximately balanced synaptic currents). Using these models, we show that balanced synaptic currents evoke fewer spikes per second than excitatory inputs alone or equal excitatory and inhibitory conductances. However, spikes evoked by balanced synaptic inputs are more informative (bits/spike), so that spike trains evoked by all three regimes have similar information rates (bits/s). Consequently, because spikes dominate the energy consumption of our computational models, approximately balanced synaptic currents are also more energy efficient than other synaptic regimes. Thus, by producing fewer, more informative spikes approximately balanced synaptic currents in cortical neurons can promote both coding efficiency and energy efficiency.

Why do axons differ in caliber?

CNS axons differ in diameter (d) by nearly 100-fold (∼0.1-10 µm); therefore, they differ in cross-sectional area (d(2)) and volume by nearly 10,000-fold. If, as found for optic nerve, mitochondrial volume fraction is constant with axon diameter, energy capacity would rise with axon volume, also as d(2). We asked, given constraints on space and energy, what functional requirements set an axon's diameter? Surveying 16 fiber groups spanning nearly the full range of diameters in five species (guinea pig, rat, monkey, locust, octopus), we found the following: (1) thin axons are most numerous; (2) mean firing frequencies, estimated for nine of the identified axon classes, are low for thin fibers and high for thick ones, ranging from ∼1 to >100 Hz; (3) a tract's distribution of fiber diameters, whether narrow or broad, and whether symmetric or skewed, reflects heterogeneity of information rates conveyed by its individual fibers; and (4) mitochondrial volume/axon length rises ≥d(2). To explain the pressure toward thin diameters, we note an established law of diminishing returns: an axon, to double its information rate, must more than double its firing rate. Since diameter is apparently linear with firing rate, doubling information rate would more than quadruple an axon's volume and energy use. Thicker axons may be needed to encode features that cannot be efficiently decoded if their information is spread over several low-rate channels. Thus, information rate may be the main variable that sets axon caliber, with axons constrained to deliver information at the lowest acceptable rate.

Visually targeted reaching in horse-head grasshoppers.

Visually targeted reaching to a specific object is a demanding neuronal task requiring the translation of the location of the object from a two-dimensionsal set of retinotopic coordinates to a motor pattern that guides a limb to that point in three-dimensional space. This sensorimotor transformation has been intensively studied in mammals, but was not previously thought to occur in animals with smaller nervous systems such as insects. We studied horse-head grasshoppers (Orthoptera: Proscopididae) crossing gaps and found that visual inputs are sufficient for them to target their forelimbs to a foothold on the opposite side of the gap. High-speed video analysis showed that these reaches were targeted accurately and directly to footholds at different locations within the visual field through changes in forelimb trajectory and body position, and did not involve stereotyped searching movements. The proscopids estimated distant locations using peering to generate motion parallax, a monocular distance cue, but appeared to use binocular visual cues to estimate the distance of nearby footholds. Following occlusion of regions of binocular overlap, the proscopids resorted to peering to target reaches even to nearby locations. Monocular cues were sufficient for accurate targeting of the ipsilateral but not the contralateral forelimb. Thus, proscopids are capable not only of the sensorimotor transformations necessary for visually targeted reaching with their forelimbs but also of flexibly using different visual cues to target reaches.

A long-latency aversive learning mechanism enables locusts to avoid odours associated with the consequences of ingesting toxic food.

Avoiding food that contains toxins is crucial for the survival of many animals, particularly herbivores, because many plants defend themselves with toxins. Some animals can learn to avoid food containing toxins not through its taste but by the toxins' effects following ingestion, though how they do so remains unclear. We studied how desert locusts (Schistocerca gregaria), which are generalist herbivores, form post-ingestive aversive memories and use them to make appropriate olfactory-based decisions in a Y-maze. Locusts form an aversion gradually to an odour paired with food containing the toxin nicotine hydrogen tartrate (NHT), suggesting the involvement of a long-latency associative mechanism. Pairing of odour and toxin-free food accompanied by NHT injections at different latencies showed that locusts could form an association between an odour and toxic malaise, which could be separated by up to 30 min. Tasting but not swallowing the food, or the temporal separation of odour and food, prevents the formation of these long-latency associations, showing that they are post-ingestive. A second associative mechanism not contingent upon feeding operates only when odour presentation is simultaneous with NHT injection. Post-ingestive memory formation is not disrupted by exposure to a novel odour alone but can be if the odour is accompanied by simultaneous NHT injection. Thus, the timing with which food, odour and toxin are encountered whilst foraging is likely to influence memory formation and subsequent foraging decisions. Therefore, locusts can form specific long-lasting aversive olfactory associations that they can use to avoid toxin-containing foods whilst foraging.

Braking slows passive flexion during goal-directed movements of a small limb.

The movements of animal appendages are determined by extrinsic and intrinsic forces. Extrinsic forces include gravity or friction,1,2 whereas intrinsic forces are generated by active muscle contraction or passive musculoskeletal elements.3,4 For lightweight appendages, such as insect limbs, movements depend more upon intrinsic than extrinsic forces.5,6 Indeed, passive movements of insect limbs can be large and oppose or aid joint flexion, extension, or both.4 Yet, how passive properties contribute to insects' goal-directed limb movements, such as targeted reaching and searching,7-10 remains unclear. Here, we show that mantids make targeted reaches and searches to objects by using their raptorial forelimbs, employing braking to slow passive flexion of the femoro-tibial (FTi) joint. In most reaches, tibial flexion ensures the forelimb contacts the object. Such tibial flexion is particularly clear when the forelimb misses the object and continues on a downward trajectory or during directed searching movements. We characterize the passive properties of the FTi joint by combining passive movements of excised limbs with apodeme ablations and muscle stimulation. These experiments show that passive properties of the flexor tibiae muscle-apodeme complex are the primary structural element producing tibial flexion in excised limbs. During reaching and searching, however, tibial flexion is slower and smaller than predicted. This is due to braking, which opposes passive flexion, thereby reducing the magnitude and velocity of tibial flexion. Braking retarding passive movements is a novel behaviorally relevant control strategy for the goal-directed movements of lightweight limbs, such as those of insects.