Brain and behavioral lateralization in invertebrates

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: individual-level 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

Where the Standard Approach in Comparative Neuroscience Fails and Where It Works: General Intelligence and Brain Asymmetries

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

Distribution of antennal olfactory and non-olfactory sensilla in different species of bees

Several species of social bees exhibit population-level lateralization in learning odors and recalling olfactory memories. Honeybees Apis mellifera and Australian social stingless bees Trigona carbonaria and Austroplebeia australis are better able to recall short- and long-term memory through the right and left antenna respectively, whereas non-social mason bees Osmia rufa are not lateralized in this way. In honeybees, this asymmetry may be partially explained by a morphological asymmetry at the peripheral level—the right antenna has 5% more olfactory sensilla than the left antenna. Here we looked at the possible correlation between the number of the antennal sensilla and the behavioral asymmetry in the recall of olfactory memories in A. australis and O. rufa. We found no population-level asymmetry in the antennal sensilla distribution in either species examined. This suggests that the behavioral asymmetry present in the stingless bees A. australis may not depend on lateral differences in antennal receptor numbers

Individual-Level and Population-Level Lateralization: Two Sides of the Same Coin

Lateralization, i.e., the different functional roles played by the left and right sides of the brain, is expressed in two main ways: (1) in single individuals, regardless of a common direction (bias) in the population (aka individual-level lateralization); or (2) in single individuals and in the same direction in most of them, so that the population is biased (aka population-level lateralization). Indeed, lateralization often occurs at the population-level, with 60–90% of individuals showing the same direction (right or left) of bias, depending on species and tasks. It is usually maintained that lateralization can increase the brain’s efficiency. However, this may explain individual-level lateralization, but not population-level lateralization, for individual brain efficiency is unrelated to the direction of the asymmetry in other individuals. From a theoretical point of view, a possible explanation for population-level lateralization is that it may reflect an evolutionarily stable strategy (ESS) that can develop when individually asymmetrical organisms are under specific selective pressures to coordinate their behavior with that of other asymmetrical organisms. This prediction has been sometimes misunderstood as it is equated with the idea that population-level lateralization should only be present in social species. However, population-level asymmetries have been observed in aggressive and mating displays in so-called “solitary” insects, suggesting that engagement in specific inter-individual interactions rather than “sociality” per se may promote population-level lateralization. Here, we clarify that the nature of inter-individuals interaction can generate evolutionarily stable strategies of lateralization at the individual- or population-level, depending on ecological contexts, showing that individual-level and population-level lateralization should be considered as two aspects of the same continuum

Visual Lateralization in the Cephalopod Mollusk Octopus vulgaris

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

Abnormal visual attention to simple social stimuli in 4-month-old infants at high risk for Autism

Despite an increasing interest in detecting early signs of Autism Spectrum Disorders (ASD), the pathogenesis of the social impairments characterizing ASD is still largely unknown. Atypical visual attention to social stimuli is a potential early marker of the social and communicative deficits of ASD. Some authors hypothesized that such impairments are present from birth, leading to a decline in the subsequent typical functioning of the learning-mechanisms. Others suggested that these early deficits emerge during the transition from subcortically to cortically mediated mechanisms, happening around 2-3 months of age. The present study aimed to provide additional evidence on the origin of the early visual attention disturbance that seems to characterize infants at high risk (HR) for ASD. Four visual preference tasks were used to investigate social attention in 4-month-old HR, compared to low-risk (LR) infants of the same age. Visual attention differences between HR and LR infants emerged only for stimuli depicting a direct eye-gaze, compared to an adverted eye-gaze. Specifically, HR infants showed a significant visual preference for the direct eye-gaze stimulus compared to LR infants, which may indicate a delayed development of the visual preferences normally observed at birth in typically developing infants. No other differences were found between groups. Results are discussed in the light of the hypotheses on the origins of early social visual attention impairments in infants at risk for ASD

Lateralization in the Invertebrate Brain: Left-Right Asymmetry of Olfaction in Bumble Bee, Bombus terrestris

Brain and behavioural lateralization at the population level has been recently hypothesized to have evolved under social selective pressures as a strategy to optimize coordination among asymmetrical individuals. Evidence for this hypothesis have been collected in Hymenoptera: eusocial honey bees showed olfactory lateralization at the population level, whereas solitary mason bees only showed individual-level olfactory lateralization. Here we investigated lateralization of odour detection and learning in the bumble bee, Bombus terrestris L., an annual eusocial species of Hymenoptera. By training bumble bees on the proboscis extension reflex paradigm with only one antenna in use, we provided the very first evidence of asymmetrical performance favouring the right antenna in responding to learned odours in this species. Electroantennographic responses did not reveal significant antennal asymmetries in odour detection, whereas morphological counting of olfactory sensilla showed a predominance in the number of olfactory sensilla trichodea type A in the right antenna. The occurrence of a population level asymmetry in olfactory learning of bumble bee provides new information on the relationship between social behaviour and the evolution of population-level asymmetries in animals

Small and large bumblebees invest differently when learning about flowers

Honeybees [1] and bumblebees [2] perform learning flights on leaving a newly discovered flower. During these flights, bees spend a portion of the time turning back to face the flower when they can memorise views of the flower and its surroundings. In honeybees, learning flights become longer, when the reward offered by a flower is increased [3]. We show here that bumblebees behave in a similar way and we add that bumblebees face an artificial flower more when the concentration of the sucrose solution that the flower provides is higher. The surprising finding is that a bee’s size determines what a bumblebee regards as a 'low' or a 'high' concentration and so affects its learning behaviour. The larger bees in a sample of foragers only enhance their flower facing when the sucrose concentration is in the upper range of the flowers that are naturally available to bees [4]. In contrast, smaller bees invest the same effort in facing flowers, whether the concentration is high or low, but their effort is less than that of larger bees. The way in which different sized bees distribute their effort when learning about flowers parallels the foraging behaviour of a colony. Large bumblebees [5, 6] are able to carry larger loads and explore further from the nest than smaller ones [7]. Small ones with a smaller flight range and carrying capacity cannot afford to be as selective and so accept a wider range of flowers

A multimodal approach for tracing lateralization along the olfactory pathway in the honeybee through electrophysiological recordings, morpho-functional imaging, and behavioural studies

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.Comment: 28 pages, 8 figure