Whole-head recording of chemosensory activity in the marine annelid Platynereis dumerilii

Abstract

Chemical detection is key to various behaviours in both marine and terrestrial animals. Marine species, though highly diverse, have been underrepresented so far in studies on chemosensory systems, and our knowledge mostly concerns the detection of airborne cues. A broader comparative approach is therefore desirable. Marine annelid worms with their rich behavioural repertoire represent attractive models for chemosensation. Here, we study the marine worm Platynereis dumerilii to provide the first comprehensive investigation of head chemosensory organ physiology in an annelid. By combining microfluidics and calcium imaging, we record neuronal activity in the entire head of early juveniles upon chemical stimulation. We find that Platynereis uses four types of organs to detect stimuli such as alcohols, esters, amino acids and sugars. Antennae are the main chemosensory organs, compared to the more differentially responding nuchal organs or palps. We report chemically evoked activity in possible downstream brain regions including the mushroom bodies (MBs), which are anatomically and molecularly similar to insect MBs. We conclude that chemosensation is a major sensory modality for marine annelids and propose early Platynereis juveniles as a model to study annelid chemosensory systems.

Whole-body integration of gene expression and single-cell morphology

“…Intermediate filaments are also visible in the ciliated support cells (Supplementary Figure 1A). These cells in the head, posterior to the adult eyes, are part of the sensory nuchal organ (Chartier et al, 2018;Schmidtberg and Dorresteijn, 2010). They show an enrichment of mitochondria at their apical side, and similar to epithelial cells, they form junctions with the underlying muscles ( Supplementary Figure 1A inset).…”

“…With our new resource, this can now be extended to include connectomics and transcriptomics information for an entire animal, and for different developmental stages. Additionally, using the multimodal capacity of the PlatyBrowser, we will be able to incorporate physiological data for identified cell types using tools such as calcium imaging (Chartier et al, 2018) and Crispr-cas9 (Bezares-Calderón et al, 2018).…”

“…In addition to the tissue segmentation (see Figure 2C for the entire musculature segmentation), we subdivided the body (and cells) into head, the first body segment (cryptic segment), the ventral nerve cord, the unsegmented posterior part of the body (pygidium), the lateral ectoderm, the foregut and the midgut (see Supplementary Table 1). Since at 6 dpf the head is already morphologically highly diverse (Chartier et al, 2018), we also segmented the head into morphologically discernible subunits or ganglia. These include the paired palpae, antennae, cirri, and adult eyes representing sensory organs, and central complex as well as mushroom bodies as brain parts (Supplementary Figure 2D).…”

“…These include the paired palpae, antennae, cirri, and adult eyes representing sensory organs, and central complex as well as mushroom bodies as brain parts (Supplementary Figure 2D). The detail in the 3D ultrastructure volume and the cell segmentation provide an unprecedented resolution and framework to do this anatomical classification in a complete and unbiased manner (as compared to previous efforts recognising brain anatomy mostly based on immunohistochemistry (Chartier et al, 2018;Tomer et al, 2010)).…”

Whole-animal connectome and cell-type complement of the three-segmentedPlatynereis dumeriliilarva

“…However, it is now possible to combine genetics, behaviour and neuronal activity imaging in Platynereis to functionally characterise sensory cell types. Recent work has identified larval UV photoreceptors (Verasztó et al, 2018), hydrodynamic vibration detectors (Bezares-Calderón et al, 2018), chemosensory neurons (Chartier et al, 2018), or the Go-opsin1-expressing shadow detectors in sensory appendages of adult worms (Ayers et al, 2018). The connectome nevertheless allowed us to identify new types of putative mechanosensory neurons -including the SNblunt, SNFVa and SNbronto cells -based on connectivity and morphology alone (Figure 9).…”