Cognition in Little Minds: The Utility of Exploring Complex Behaviors in Simple Neural Systems

Abstract

Simple neural systems are increasingly powerful tools in our exploration of cognitive mechanisms and their evolution. From mapping the entirety of the fly neuronal network to the utility of the honeybee genome, the pool of knowledge surrounding invertebrate brains and behaviors is growing. With that said, simple neural systems are often associated with simple behaviors, mechanistically useful but not comparable to the larger, more complex abilities of vertebrates. Polistes fuscatus paper wasps offer an opportunity to shift this perception in a new direction. Polistes fuscatus are cognitively specialized for faces, in that they learn faces more adeptly and efficiently relative to all other stimuli. Until recently, cognitive specialization has been unique to vertebrates, and even still there are only a few known examples. In vertebrates, cognitive specialization is linked to specialized neural mechanisms. Thus far, the link between cognitive specialization and specialized neural mechanisms has not been explored in invertebrates. In this dissertation, I explore not only the complex behaviors of P. fuscatus wasps, but also connect these behaviors to their neural mechanisms. I experimentally utilize the natural geographic variation in P. fuscatus’ ability to learn faces, to explore the phenotypic and genotypic origins of this complex skill. In Chapter II, I explore the development of the behavioral mechanism behind individual recognition – individual face specialization. By rearing wasps from populations with and without face specialization in a common garden, I find that the specialized ability to learn faces is plastic, and can rapidly change based on social environment. Based on the plasticity of their behavioral development, I next explore the potentially paired neurological mechanisms and plasticity of face learning. In Chapter III, I utilize the Immediate Early Gene c-fos, a highly conserved marker of neural activity, to evaluate neural activity during conspecific face learning. I use a negatively reinforced operant conditioning protocol, with a positive (learned) stimulus and a negative (not learned) stimulus to examine neurological reactions to faces in the wasp brain. I found that wasps from a population with individual recognition had distinct neurological activity to faces, as compared to the control stimuli and wasps from populations without individual recognition. This reaction takes place primarily in the central brain, a region suspected, but not confirmed, to play a crucial role in face learning. Chapter III marks the first instance of potential neurological specialization for faces in an invertebrate. However, this approach was targeted, using only one gene. Therefore, in Chapter IV I use RNAseq to generate high-level analyses of brain gene expression during face learning in the brains of P. fuscatus. I find distinctive transcriptomic responses to faces, and differences in gene expression between populations with and without individual recognition, and across sensory and processing regions of the brain. My results show that processing regions of the P. fuscatus brain analogous to the neocortex in vertebrates have the most distinct neurogenomic reaction to faces. The combined results of Chapters III and IV link several processing regions of the insect brain to a specialized learning task, and point to gene expression as a critical tool in exploring convergent mechanisms of cognition. Overall, the results of my dissertation provide the first evidence of a link between cognitive specialization and specialized neural mechanisms in invertebrates, and provide important evidence for the utility of simple neural systems in exploring complex behaviors.