Elisa Frasnelli | University of Trento (original) (raw)

Papers by Elisa Frasnelli

Scientific Reports, Jan 4, 2024

Evidence of lateralization has been provided in Apis mellifera in olfactory learning and social i... more Evidence of lateralization has been provided in Apis mellifera in olfactory learning and social interactions, but not much is known about how it influences visuo-motor tasks. This study investigates visuo-motor biases in free-flying honeybees by analysing left/right choices related to foraging in a Y-maze. Individual bees were trained to associate a visual stimulus (a blue or yellow target) with a reward/punishment: the Blue + group was reinforced for the blue and punished for the yellow, and vice versa for the Yellow + group. In unrewarded tests, we assessed for each bee the directional choice for one of the two identical targets (12 trials with blue targets and 12 with yellow targets) placed in the left and right arms of the maze as well as the flight times to reach the target chosen. The results did not reveal a significant directional preference at the population level, but only at the individual level, with some individuals presenting a strong bias for choosing the right or left stimulus. However, the data revealed an interesting new factor: the influence of both direction and colour on flight times. Overall, bees took less time to choose the stimulus in the left arm. Furthermore, the yellow target, when previously associated with a punishment, was reached on average faster than the punished blue target, with a higher number of no-choices for punished blue targets than for punished yellow targets. This opens new perspectives not only on the study of lateralization in Apis mellifera, but also on the bees' chromatic preferences. The concept of lateralization, which refers to the distinct functional specialisation of the left and right hemispheres of the brain, is a characteristic found in both simple and more complex nervous systems. In fact, there is extensive evidence of behavioural and brain asymmetry in both vertebrates 1 and invertebrates 2,3. These asymmetries manifest in various ways, including limb use preferences, directional biases, as well as differences in sensory and cognitive abilities. Moreover, they can occur at a population level, where the majority of individuals in a population exhibit the same directional bias (either right or left), or at an individual level, where a similar number of individuals within the population displays lateralization in each direction. Population-level lateralization has been proposed to result from social pressures encountered during evolution 3-5 and may be linked to behaviours that necessitate interaction and possibly coordination among individuals 6,7. This idea finds support in studies on insects 1,3,8 emphasising the importance of investigating lateralization even in simpler nervous systems. An illustrative example of this phenomenon can be observed in the fruit fly, Drosophila melanogaster, which displays individual-level motor biases both in Y-maze navigation and circling behaviour 9. Interestingly, these motor biases are not associated with any observable morphological traits, such as gut twisting laterality, leg length asymmetry, or wing-folding preferences, nor are they linked to specific genetic strains, but, instead, these biases appear to originate centrally, as their strength increases when neurons in the central complex of the brain are silenced 9. In the species of ants, there are also instances of motor biases. For instance, 12 species of Lasius ants tend to keep the right side of their foraging "streets," while one species prefers the left 10. Another ant species, Formica pratensis, which does not rely on trail pheromones, demonstrates a population-level tendency to keep the left to avoid encounters with other workers when returning to the nest with food, but not when leaving the nest to search for food 11. Among ants, Temnothorax albipennis displays a population-level inclination to explore unknown nest sites in a leftward direction 12. Similar patterns are observed in honeybees (Apis mellifera). They exhibit a population-level motor bias when exploring unfamiliar open cavities, predominantly favouring the right direction (unlike ants, which favour the left 12), with individuals strongly biased to the right making quicker decisions 13. Furthermore, individual honeybee workers, when presented with a pair of identical apertures to fly through, display individual-level preferences for either the right or left aperture, with some individuals displaying no preference 14. Some species of bumblebees,

bioRxiv (Cold Spring Harbor Laboratory), Nov 4, 2022

The start of a bumblebee's first learning flight from its nest provides an opportunity to examine... more The start of a bumblebee's first learning flight from its nest provides an opportunity to examine the bee's learning behaviour on its initial view of the nest's unfamiliar surroundings. Bumblebees like many other ants, bees and wasps learn views of their nest surroundings while facing their nest. A bumblebee's first fixation of the nest is a coordinated manoeuvre in which the insect faces the nest with its body oriented towards a particular visual feature within its surroundings. The manoeuvre's utility is that during return flights after foraging bees, when close to the nest, adopt the same preferred body-orientation (Hempel de Ibarra et al., 2009; Robert et al., 2018). A translational scan oriented orthogonally to the bee's body-orientation helps the bee reach the preferred conjunction of nest-fixation and body-orientation. How does a bee, unacquainted with its surroundings, know when it is facing its nest? The details of nest-fixation argue that, like desert ants (Fleischmann et al., 2018), the bee relies on path integration. Path integration gives bees continuously updated information about the current direction of their nest and enables them to fixate the nest when the body points in the appropriate direction. We relate the three components of the coordinated manoeuvre to events in the central complex, noting that nest fixation is in egocentric. CC-BY-NC-ND 4.

Journal of Experimental Biology

The start of a bumblebee's first learning flight from its nest provides an opportunity to exa... more The start of a bumblebee's first learning flight from its nest provides an opportunity to examine the bee's learning behaviour during its initial view of the nest's unfamiliar surroundings. Bumblebees like many other bees, wasps and ants learn views of their nest surroundings while they face their nest. We find that a bumblebee's first fixation of the nest is a coordinated manoeuvre in which the insect faces the nest with its body oriented towards a particular visual feature within its surroundings. This conjunction of nest-fixation and body-orientation is preceded and reached by means of a translational scan during which the bee flies perpendicularly to its preferred body orientation. The significance of the coordinated manoeuvre is apparent during return flights after foraging. Bees then adopt a similar preferred body-orientation when they are close to the nest. How does a bee, unacquainted with its surroundings, know when it is facing its nest? A likely answer is ...

Neuroscience & Biobehavioral Reviews, Dec 1, 2022

Animal Cognition

Handedness has proven to be the most effective and least intrusive measure of laterality in many ... more Handedness has proven to be the most effective and least intrusive measure of laterality in many species. Several studies have investigated paw preference in dogs (Canis familiaris) without considering the potential impact that owner’s handedness may have on it, despite dogs being a domesticated species. The aim of this study was to investigate whether owner handedness influences paw preference in their dogs. Sixty-two dogs had their paw preference tested using a Paw Task and a Reach Task in their home over 10 days, recorded by their owners. Interestingly, it was found that left-handed owners were more likely to own a dog with a left paw bias, and right-handed owners were more likely to own a dog with a right paw bias. In the Paw Task, the hand presented to a dog did not significantly predict which paw the dog lifted in response. Furthermore, it was found that females displayed a right paw bias at all age groups. However, males had a left paw bias in puppyhood and right paw bias in ...

Scientific Reports, 2018

Brain lateralization is considered adaptive because it leads to behavioral biases and specializat... more Brain lateralization is considered adaptive because it leads to behavioral biases and specializations that bring fitness benefits. Across species, strongly lateralized individuals perform better in specific behaviors likely to improve survival. What constrains continued exaggerated lateralization? We measured survival of pheasants, finding that individuals with stronger bias in their footedness had shorter life expectancies compared to individuals with weak biases. Consequently, weak, or no footedness provided the highest fitness benefits. If, as suggested, footedness is indicative of more general brain lateralization, this could explain why continued brain lateralization is constrained even though it may improve performance in specific behaviors.

Autism spectrum disorders (ASD) are well-known early onset, neurodevelopmental disorders characte... more Autism spectrum disorders (ASD) are well-known early onset, neurodevelopmental disorders characterized by qualitative impairments in social communication and interaction, and by restricted, repetitive, and stereotyped behaviors, interests and activities. An increasing interest in timely detection of ASD red flags has emerged, mostly driven by the insight that early identification is a fundamental prerequisite for early intervention (Rogers et al., 2014; Venkataraman et al., 2016). Nevertheless, the pathogenesis of the social impairments that characterizes ASD is still largely unknown.Reduced early orienting and attention to social stimuli, such as faces or eye-gaze, but also biological motion, have been hypothesized to play a crucial role in the development of social impairments found in ASD (Hedger et al., 2020). These early signs are thought to have cascading effects on the typical development of the social brain network (Johnson, 2015), restricting the infants’ exposure to typica...

Comparative Cognition & Behavior Reviews, 2018

Although brain size and the concept of intelligence have been extensively used in comparative neu... more Although brain size and the concept of intelligence have been extensively used in comparative neuroscience to study cognition and its evolution, such coarse-grained traits may not be informative enough about important aspects of neurocognitive systems. By taking into account the different evolutionary trajectories and the selection pressures on neurophysiology across species, Logan and colleagues suggest that the cognitive abilities of an organism should be investigated by considering the fine-grained and species-specific phenotypic traits that characterize it. In such a way, we would avoid adopting human-oriented, coarse-grained traits, typical of the standard approach in cognitive neuroscience. We argue that this standard approach can fail in some cases, but can, however, work in others, by discussing two major topics in contemporary neuroscience as examples: general intelligence and brain asymmetries.

Symmetry, 2019

Behavioral asymmetries exhibited by the common octopus, Octopus vulgaris, a cephalopod mollusk, d... more Behavioral asymmetries exhibited by the common octopus, Octopus vulgaris, a cephalopod mollusk, during predatory and exploratory responses were investigated. Animals were tested for eye preferences while attacking a natural (live crab) or an artificial (plastic ball) stimulus, and for side preferences while exploring a T-maze in the absence of any specific intra- or extra-maze cues. We found individual-level asymmetry in some animals when faced with either natural or artificial stimuli, but not when exploring the maze. Our findings suggest that visual lateralization in O. vulgaris is context-dependent.

Scientific Reports, 2016

Comparison of lateralization in social and non-social bees tests the hypothesis that population-l... more Comparison of lateralization in social and non-social bees tests the hypothesis that population-level, directional asymmetry has evolved as an adjunct to social behaviour. Previous research has supported this hypothesis: directional bias of antennal use in responding to odours and learning to associate odours with a food reward is absent in species that feed individually, such as mason bees, whereas it is clearly present in eusocial honeybees and stingless bees. Here we report that, when mason bees engage in agonistic interactions, a species-typical interactive behaviour, they do exhibit a directional bias according to which antenna is available to be used. Aggression was significantly higher in dyads using only their left antennae (LL) than it was in those using only their right antennae (RR). This asymmetry was found in both males and females but it was stronger in females. LL dyads of a male and a female spent significantly more time together than did other dyadic combinations. No asymmetry was present in non-aggressive contacts, latency to first contact or body wiping. Hence, populationlevel lateralization is present only for social interactions common and frequent in the species' natural behaviour. This leads to a refinement of the hypothesis linking directional lateralization to social behaviour.

This symposium aims at providing a general view of the impact that both man-made and natural sele... more This symposium aims at providing a general view of the impact that both man-made and natural selection had and still have on plant and animal species of agricultural relevance. The themes tackled by the symposium will range from the evolution of invasive species, the traits that human being have been selecting during plant and animal domestication, the relationship between biodiversity and the occurrence of the centers of domestication, the co-evolution of crops and the pests affecting them, the relationships between social behavior and the evolution of communication mechanisms in insects and many more topics.

Brain and behavioural asymmetries are widespread in vertebrates (Rogers et al., 2013) and inverte... more Brain and behavioural asymmetries are widespread in vertebrates (Rogers et al., 2013) and invertebrates (Frasnelli, 2013). Among cephalopods, cuttlefish have been shown to present a spontaneous side-turning preference in the T-maze with a population bias to turn left that progressively develops with age (Jozet-Alves et al., 2007; 2012a). Moreover, cuttlefish display a significant population bias towards a larger right peduncle lobe, that is correlated with right eye dominance in the left-turning (Jozet-Alves et al., 2012b). Lateralization in octopuses Octopus vulgaris has been investigated so far for eye use (Byrne et al., 2002; 2004) and arm preference (Byrne et al., 2006a; 2006b). However, no one has ever looked at possible cerebral correlates of lateralization. Here we examined possible asymmetries in the brain and in particular at the level of the optic lobes (OLs). Moreover, we looked at (a) preferential eye use during prey attacks and (b) spontaneous turning preferences in a m...

Neuroscience & Biobehavioral Reviews, 2012

Evidence of left-right asymmetries in invertebrates has begun to emerge, suggesting that laterali... more Evidence of left-right asymmetries in invertebrates has begun to emerge, suggesting that lateralization of the nervous system may be a feature of simpler brains as well as more complex ones. A variety of studies have revealed sensory and motor asymmetries in behaviour, as well as asymmetries in the nervous system, in invertebrates. Asymmetries in behaviour are apparent in olfaction (antennal asymmetries) and in vision (preferential use of the left or right visual hemifield during activities such as foraging or escape from predators) in animals as different as bees, fruitflies, cockroaches, octopuses, locusts, ants, spiders, crabs, snails, water bugs and cuttlefish. Asymmetries of the nervous system include lateralized position of specific brain structures (e.g., in fruitflies and snails) and of specific neurons (e.g., in nematodes). As in vertebrates, lateralization can occur both at the individual and at the population-level in invertebrates. Theoretical models have been developed supporting the hypothesis that the alignment of the direction of behavioural and brain asymmetries at the population-level could have arisen as a result of social selective pressures, when individually asymmetrical organisms had to coordinate with each other. The evidence reviewed suggests that lateralization at the population-level may be more likely to occur in social species among invertebrates, as well as vertebrates.

Frontiers in Psychology, 2013

Traditionally, only humans were thought to exhibit brain and behavioral asymmetries, but several ... more Traditionally, only humans were thought to exhibit brain and behavioral asymmetries, but several studies have revealed that most vertebrates are also lateralized. Recently, evidence of left-right asymmetries in invertebrates has begun to emerge, suggesting that lateralization of the nervous system may be a feature of simpler brains as well as more complex ones. Here I present some examples in invertebrates of sensory and motor asymmetries, as well as asymmetries in the nervous system. I illustrate two cases where an asymmetric brain is crucial for the development of some cognitive abilities. The first case is the nematode Caenorhabditis elegans, which has asymmetric odor sensory neurons and taste perception neurons. In this worm left/right asymmetries are responsible for the sensing of a substantial number of salt ions, and lateralized responses to salt allow the worm to discriminate between distinct salt ions. The second case is the fruit fly Drosophila melanogaster, where the presence of asymmetry in a particular structure of the brain is important in the formation or retrieval of long-term memory. Moreover, I distinguish two distinct patterns of lateralization that occur in both vertebrates and invertebrates: individuallevel and population-level lateralization. Theoretical models on the evolution of lateralization suggest that the alignment of lateralization at the population level may have evolved as an evolutionary stable strategy in which individually asymmetrical organisms must coordinate their behavior with that of other asymmetrical organisms. This implies that lateralization at the population-level is more likely to have evolved in social rather than in solitary species. I evaluate this new hypothesis with a specific focus on insects showing different level of sociality. In particular, I present a series of studies on antennal asymmetries in honeybees and other related species of bees, showing how insects may be extremely useful to test the evolutionary hypothesis.

European Biophysics Journal, 2011

Recent studies have revealed asymmetries between the left and right sides of the brain in inverte... more Recent studies have revealed asymmetries between the left and right sides of the brain in invertebrate species. Here we present a review of a series of recent studies from our labs, aimed at tracing asymmetries at different stages along the honeybee's (Apis mellifera) olfactory pathway. These include estimates of the number of sensilla present on the two antennae, obtained by scanning electron microscopy, as well as electroantennography recordings of the left and right antennal responses to odorants. We describe investigative studies of the antennal lobes, where multi-photon microscopy is used to search for possible morphological asymmetries between the two brain sides. Moreover, we report on recently published results obtained by two-photon calcium imaging for functional mapping of the antennal lobe aimed at comparing patterns of activity evoked by different odours. Finally, possible links to the results of behavioural tests, measuring asymmetries in single-sided olfactory memory recall, are discussed.

Behavioural Brain Research, 2012

Behavioural and brain left-right asymmetries are a common feature among the animal kingdom. Later... more Behavioural and brain left-right asymmetries are a common feature among the animal kingdom. Lateralization often manifests itself at the population-level with most individuals showing the same direction of lateral bias. Theoretical model based on evolutionary stable strategy predicts that lateralization at the population-level is more likely to characterize social rather than solitary species. Empirical data supporting this hypothesis has been recently obtained in Hymenoptera showing that eusocial honeybees present an asymmetrical use of the antennae: the right antenna is involved in olfactory learning and present more olfactory receptors. However, no evidences about the role of antennal asymmetries in social interactions have been provided so far. Highly social ant species belonging to Formica rufa group are a good model for investigating natural communication because they are able to pass exact information to their nest mates. We applied the "binary tree" experimental paradigm, which allowed us to observe different types of antennal contacts performed by ants out of their nest. To examine possible asymmetrical use of the right and left antenna, we focused on "feeding" (the simplest) contacts where a "donor" ant is exchanging food with a "receiver" ant through trophallaxis. We observed a population-level asymmetry, with the "receiver" ant using the right antenna significantly more often than the left antenna. This study provides the first evidence of lateralization in antennal contacts in ants, and seems to support the hypothesis of mathematical models on the evolution of lateralization suggesting that the alignment of lateralization at the population-level matters in social interactions.