Cellular and synaptic organization of the Octopus vertical lobe

Abstract

Understanding memory formation and its influence on behavior is a central challenge in neuroscience. Associative learning networks, including the mushroom body in insects, the cerebellum in mammals, and the vertical lobe (VL) in cephalopods, typically exhibit a 3-layered architecture, characterized by divergence (fan-out) followed by convergence (fan-in), facilitating sparse sensory coding (Babadi and Sompolinsky, 2014; Lin et al., 2014; Litwin-Kumar et al., 2017; Turchetti-Maia et al., 2017). Previously, using volumetric electron microscopy, we showed that the VL uniquely comprises 22 million simple amacrine (SAM) interneurons, each receiving a singular input subject to activity-dependent long-term potentiation, contrasting with typical middle-layer interneurons (Bidel, Meirovitch et al., 2023). We also demonstrated that these SAMs provide excitatory feedforward input to the output cell layer, balanced by approximately 400,000 inhibitory complex amacrines (CAM), which are morphologically diverse and integrate numerous inputs (Bidel, Meirovitch et al., 2023). Here, we leverage the same digital tissue to explore the CAMs morphological diversity, identifying correlations between structure, postsynaptic site density, and synaptic input proportions, which led to the classification of CAMs into distinct groups. Further analysis of the input layer in the VL revealed a meticulous structural and synaptic compartmentalization, with distinct synaptic bouton types forming three zones that integrate different inputs towards CAMs. Additionally, we identify the potential presence of a neurogenic niche in the VL, hinting at parallels with neurogenic processes in other species and warranting further investigation, particularly in the context of learning and memory. This study deepens our understanding of the VLs cellular and synaptic architecture, revealing both shared and unique features compared to other associative networks, and highlighting the intricate interplay of structural and functional elements in memory formation. Highlights (85 characters including space)O_LIThe VL both aligns with and deviates from standard associative network features C_LIO_LIThe VL input layer presents a unique compartmentalization by axonal bouton type C_LIO_LIThe minority inhibitory interneurons differentiate into unique functional subtypes C_LIO_LIMirroring the mammalian hippocampus, the VL may contain an adult neurogenic niche C_LI