Program Chair: Martin Giurfa, Sorbonne University

Associative learning is a capacity found in all animals with a nervous system. This ability enables organisms to extract the logical structure of the world by evaluating the temporal relationships between events. It leads to the formation and storage of memories, which can be retrieved in appropriate contexts to generate adaptive responses to a changing environment.


Insects, with their relatively simple and accessible nervous systems, have played a crucial role in advancing our understanding of learning and memory at behavioral, cellular, and molecular levels. Not only do they demonstrate various forms of associative learning, such as Pavlovian conditioning (associating a conditioned stimulus with an unconditioned stimulus) and operant conditioning (associating a specific action with a particular outcome), but they also display both elemental and non-elemental types of learning. Remarkably, their memory systems follow basic principles similar to those found in vertebrates. In some cases, these phenomena can be traced at the circuit and molecular levels, providing fundamental insights into the biological mechanisms of learning and memory.


In this Specialized Session of the ESA International Branch (IB), we will feature a panel of three distinguished plenary speakers known for their significant contributions to the field of insect learning and memory. Steve Montgomery (University of Bristol, UK) will present his research on learning and brain development in Heliconius butterflies, focusing on the role of mushroom bodies in specific forms of visual learning. Valerie Kuklovsky (University of Konstanz, Germany) will explore interindividual variability in learning performance in honeybees, showing that different learning profiles coexist among foragers within a hive. Finally, Jean-Christophe Sandoz (CNRS, Gif-sur-Yvette, France) will discuss gustatory learning in honeybees, shedding light on the taste modalities that bees perceive and discriminate. Collectively, these presentations will highlight both the shared principles and the unique features that underlie insect learning and memory.


Plenary Speakers

Prof. Dr. Stephen Montgomery, University of Bristol, United Kingdom 

I grew up in the Belfast, Northern Ireland, but moved over to England to study Natural Sciences as an undergrad at Cambridge. I stayed on to do a PhD on primate brain evolution with Nick Mundy, then joined Judith Mank’s lab, briefly in Oxford and then at UCL, under successive early-career fellowships from The Royal Commission for the Exhibition of 1851 and The Leverhulme Trust. During this time I started a series of projects on brain evolution in Neotropical butterflies that developed into the research subject of my Research Fellowship, funded by NERC and the ERC, and brought me back to the Zoology department at Cambridge in 2016. In 2019 I joined the faculty at the School of Biological Sciences, and lead a lab interested in how brains evolve to produce behavioral and ecological diversity. To try to understand these links, we combine a range of approaches, including behavior and ecology, neuroanatomy and development, and comparative genomics.

Specific shifts in learning and memory in long-lived Heliconius butterflies

How animals perceive, process and respond to environmental cues is tightly tuned to the species-specific demands imposed by their ecology and life history. This specialization is likely reflected in neural systems that support cognitive processes, as well as the behaviors expressed by those systems. In Heliconius butterflies the mushroom bodies - insect learning and memory centers - are significantly expanded relative to all other butterflies. Mushroom body expansion in Heliconius coincided with the evolution of a novel dietary shift towards active pollen feeding, and a spatial foraging behavior, trap-lining, which is thought to require long-term spatial memory of visual scenes. I will discuss evidence that selection for trap-line foraging has reshaped Heliconius cognition along specific lines, reflected in both neuroanatomical specializations and shifts in a restricted range of cognitive traits. By following the neural pathways that lead to and from the mushroom bodies, a mosaic pattern of neural adaptations is apparent, with shifts in cells and structures supporting visual and sparse coding within the mushroom body. Behavioral experiments closely mirror these changes, with improved performance in non-elemental learning and long-term memory in Heliconius, but specifically within a visual context. This provides a rare case where memory performance has been compared across species and sensory modalities, to identify a modality specific shift. These results are consistent with visual specialization of the Heliconius mushroom body facilitating a specific enhancement of visual memory, likely due to the requirements of long-term foraging efficiency, and illustrate the precision with which selection can reshape animal cognition. 


Dr. Valerie Kuklovsky, University of Konstanz, Germany 

I did my PhD in Würzburg, Germany, and Toulouse, France, which focused on elucidating consistent individual differences in the cognitive proficiency of bees; we provided thereby first evidence for the existence of ‘general intelligence’ in an insect. I have now almost ten years of experience in performing behavioral experiments, especially learning experiments, with bees. I started working with bees during my bachelor’s degree in Mainz and continued ever since. I conducted the research for my bachelor thesis at the University of Melbourne in Australia and for my master thesis at the University of Paul Sabatier in Toulouse, France at the Research Center on Animal Cognition. Seven months ago, I joined the Neurobiology Department of the University Konstanz as Post-Doc in the Sobee project.

Are some bees smarter than others? Evidence of consistent cognitive proficiency in individual honey bees

Bees are a powerful invertebrate model for the study of learning, memory and cognition. However, the existence of inter-individual variability in cognitive performances is often neglected. In parallel in vertebrate research, there is a growing interest in studying cognitive syndromes as the inter-individual level of analysis offers novel opportunities to explore the factors determining cognitive proficiency, the underling mechanisms and the associated fitness among others. With this project, we first confirmed that individual bees are consistent in their learning performance over time, a prerequisite for the existence of cognitive syndromes. Then, we showed positive correlation of performances within sensory modalities independently of the learning task but not between sensory modalities (vision and olfaction). We also observed cognitive specialization among tasks with bees showing higher level of flexibility in a reversal learning task while others were more skilled in configural processing (negative patterning task). Finally, we explored the potential factors that could impact variability in cognitive performances such as reward motivation, perceptual abilities or genetic diversity. Overall, our results evidenced cognitive specialization within nectar foragers which may have influential ecological impact and pave the way for further dissecting the neurobiological and developmental factors promoting key cognitive proficiency in bees.


Dr. Jean-Christophe Sandoz, CNRS (French National Research Center), Gif-sur-Yvette, France 
JC Sandoz obtained his PhD in behavioral biology at the University of Paris Nord in 1998. During his postdoctoral years, he was trained in chemical ecology (IACR Rothamsted, UK) and insect neurobiology (Free University of Berlin, Germany). He was recruited as a permanent CNRS researcher in Toulouse in 2002 and moved to Paris-Saclay in 2009 to supervise a team on the neuroethology and evolution of perception and cognition in Hymenoptera, with a special focus on honey bees. He has acted as adjunct Director of the EGCE Institute at Paris-Saclay since 2020.

Learning and discrimination of tastants in the honey bee

Our Lab focusses on the perception and learning abilities of Hymenoptera, in particular honey bees, and their neural basis, within an evolutionary framework. Over the years we studied several sensory modalities and learning forms, from appetitive to aversive conditioning and social learning. While much is known about the detection and discrimination abilities of bees with regards to vision and olfaction, information is lacking on their gustatory sense, whose role is crucial in discriminating between toxic and nutritious substances, ensuring proper food selection, and, eventually, survival. The honey bee Apis mellifera is well-known for its ability to associate sensory cues like colour or odour with a sugar reward, a feature that enabled the study of learning, generalization, discrimination as well as memory. However, similar success has not been achieved with gustation, as tastants have traditionally been used as reinforcements rather than as stimuli to be learned and discriminated. Interesting data obtained using aversive conditioning suggest that bees may be able to differentiate between different gustatory qualities (sweet vs salt) but not within these qualities. However, conclusions are currently limited to a few gustatory qualities and only a few gustatory appendages. To add to the discussion on bees’ taste discrimination abilities, we performed a series of experiments, conditioning bees to gustatory stimuli in an appetitive context. First, using a variation of the MultiCaFe assay commonly employed in fruit flies, we evaluated bees’ abilities to detect a range of sixteen different tastants of three qualities (salt, bitter, amino acid), each at six concentrations. Then, choosing tastants from different qualities – equally well detected and with the same hedonic value (slightly repulsive) –, we performed appetitive conditioning experiments in a free-walking arena. Using an absolute conditioning task, we found that bees were able to learn the association between each of these tastants (conditioned stimulus, CS) and a 30% sucrose reward (unconditioned stimulus, US). Bees also differentiated between tastants in a differential conditioning task, in which one gustatory stimulus was explicitly rewarded, while the other explicitly punished (3M salt). The development of such protocols may provide new tools for exploring how fine bees’ gustatory discrimination abilities really are. In parallel, our Lab performs neuroanatomical and neurophysiological experiments to understand the neural basis of these abilities. 

 

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