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Cell types and molecular architecture of the Octopus bimaculoides visual system

ABSTRACT: Cephalopods have a remarkable visual system, with a camera-type eye, high acuity vision, and a wide range of sophisticated visual behaviors. However, the cephalopod brain is organized dramatically differently from that of vertebrates, as well as other invertebrates, and little is known regarding the cell types and molecular determinants of their visual system organization beyond neuroanatomical descriptions. Here we present a comprehensive single-cell molecular atlas of the octopus optic lobe, which is the primary visual processing structure in the cephalopod brain. We combined single-cell RNA sequencing with RNA fluorescence in situ hybridization to both identify putative molecular cell types and determine their anatomical and spatial organization within the optic lobe. Our results reveal six major neuronal cell classes identified by neurotransmitter/neuropeptide usage, in addition to non-neuronal and immature neuronal populations. Moreover, we find that additional markers divide these neuronal classes into subtypes with distinct anatomical localizations, revealing cell type diversity and a detailed laminar organization within the optic lobe. We also delineate the immature neurons within this continuously growing tissue into subtypes defined by evolutionarily conserved fate specification genes as well as novel cephalopod- and octopus- specific genes. Together, these findings outline the organizational logic of the octopus visual system, based on functional determinants, laminar identity, and developmental markers/pathways. The resulting atlas presented here delineates the “parts list” of the neural circuits used for vision in octopus, providing a platform for investigations into the development and function of the octopus visual system as well as the evolution of visual processing.

ORGANISM(S): Octopus bimaculoides

PROVIDER: GSE212528 | GEO | 2022/09/04

REPOSITORIES: GEO

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Project description:Genome-wide transcriptional profiling allows characterization of the molecular underpinnings of neocortical organization, including cortical areal specialization, laminar cell type diversity and functional anatomy. Microarray analysis of individual cortical layers across sensorimotor and association cortices in rhesus macaque demonstrated robust and specific laminar and areal molecular signatures driven by differential expression of genes associated with specialized neuronal function. Gene expression corresponding with laminar architecture was generally similar across cortical areas, although genes with robust areal patterning were often highly laminar as well, and these patterns were more highly conserved between macaque and human as compared to mouse. Layer 4 of primate primary visual cortex displayed a distinct molecular signature compared to other cortical regions, a specialization not observed in mouse. Overall, transcriptome-based relationships were strongest between proximal layers in a cortical area, and between neighboring areas along the rostrocaudal axis, reflecting in vivo cortical spatial topography and therefore a developmental imprint. Tissue from male and female monkeys (n = 2-3 animals/gender) was collected from anterior cingulate gyrus (ACG), layers 2, 3, 5, 6; orbitofrontal cortex (OFC), layers 2, 3, 5, 6; dorsolateral prefrontal cortex (DLPFC), layers 2-6; primary motor cortex (M1), layers 2, 3, 5, 6; primary somatosensory cortex (S1), layers 2-6; primary auditory cortex (A1), layers 2-6; primary visual cortex (V1), layers 2-6 including 4A, 4B, 4Calpha (4Ca), 4Cbeta (4Cb); secondary visual cortex (V2), layers 2-6; middle temporal area (MT), layers 2-6; temporal area (TE), layers 2-6; hippocampus, CA1, CA2, CA3, dentate gyrus (DG); and dorsal lateral geniculate nucleus (LGN), magnocellular, parvocellular and koniocellular divisions. Due to the limited number of samples that could be amplified concurrently, amplifications were performed in 3 batches (batches A-C, containing 102, 119 and 10 experimental samples, respectively). To control for batch effects, common RNA pool control samples were amplified and hybridized in each batch. These included LCM extracted hippocampus CA3 samples from the current study and a whole rhesus brain RNA pool (Biochain). These control samples were hybridized in 6 replicates in batch A and B and in 3 replicates in batch C (3 replicates per 96 well plate).

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Cell types and molecular architecture of the Octopus bimaculoides visual system

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