Kalinski, C. A. | bioRxiv Science

bioRxiv2024

Comparative connectomics of two distantly related nematode species reveals patterns of nervous system evolution

Understanding the evolution of the bilaterian brain requires a detailed exploration of the precise nature of cellular and subcellular differences between related brains. To define the anatomical substrates of evolutionary change in the nervous system, we undertook an electron micrographic reconstruction of the brain of the predatory nematode Pristionchus pacificus. A comparison with the brain of Caenorhabditis elegans, which diverged at least 100 million years ago, reveals a conserved nematode core connectome and a wide range of specific substrates of evolutionary change. These changes include differences in neuronal cell death, neuronal cell position, axo-dendritic projection patterns and many changes in synaptic connectivity of homologous neurons that display no obvious changes in overall neurite morphology and projection patterns. Arguing against specific hot spots of evolutionary change, connectivity differences are distributed throughout the nervous system and extend to glia as well. We observed examples of apparent circuit drift, where changes in morphology and connectivity of a neuron do not appear to alter its behavioral output. In conclusion, our comprehensive comparison of distantly related nematode species provides novel vistas on patterns of conservation as well as the substrates of evolutionary change in the brain that span multiple organizational levels.

neuroscience↗

bioRxiv2022

Neuronal contact predicts connectivity in the C. elegans brain

Axons must project to particular brain regions, contact adjacent neurons, and choose appropriate synaptic targets to form a nervous system. Multiple mechanisms have been proposed to explain synaptic partnership choice. In a lock-and-key mechanism, first proposed by Sperrys chemoaffinity model1, a neuron selectively chooses a synaptic partner among several different, adjacent target cells, based on a specific molecular recognition code2. Alternatively, Peters rule posits that neurons indiscriminately form connections with other neuron types in their proximity; hence, neighborhood choice, dictated by initial neuronal process outgrowth and position, is the sole predictor of connectivity3,4. However, whether Peters rule plays an important role in synaptic wiring remains unresolved5. To assess the nanoscale relationship between neuronal adjacency and connectivity, we evaluate the expansive set of C. elegans connectomes. We find that synaptic connectivity can be accurately modeled as a path-length-dependent process of neuronal adjacency and brain strata, offering strong support for Peters rule as an organizational principle of C. elegans brain wiring.

neuroscience↗