bioRxiv Science⌕ Search

Biology subjects

Williams, E. A.

Publications and source records attributed to Williams, E. A..

11 recordsLinked to original sources

Motor automaticity in natural keyboard typing

Certain features of everyday motor skills become automatic while others remain controlled. Here we use a novel keyboard typing task to investigate whether motor automaticity depends on the frequency of naturally learned motor sequences. Participants type five-letter strings that vary in their word and bigram (two-letter sequence) frequency in natural language, allowing us to examine the influence of prior exposure without laboratory training. Novel pseudo word strings are tested as well. We find greater sequence frequency in natural language is associated with faster inter-keypress intervals and lower temporal variability within the sequence. In contrast, latencies to initiate a sequence are slower for novel pseudo-word strings but are otherwise insensitive to natural word frequency. We also find individual differences in inter-keypress speed and variability are robust across frequency levels but are unrelated to conventional measures of typing skill. Our method establishes keyboard typing as a scalable, ethologically valid framework for probing features of a naturally acquired human motor skill. This research will help extend laboratory-based studies of motor sequence learning and sets the stage for future investigations of linguo-motor processes. Moreover, our findings demonstrate which features within naturally acquired motor sequences become automatic and that typing proficiency is not determined solely by automaticity.

neuroscience↗

Ontogeny of settlement behaviours in response to Grammatophora marina diatom biofilms in the marine polychaete, Platynereis dumerilii

Settlement, the transition of a swimming planktonic larva to a crawling or sessile benthic juvenile, is a key process in the development of many marine invertebrates. Successful recruitment via larval settlement is critical for the development and maintenance of seafloor ecosystems. Microbial biofilms act as positive cues for larval settlement across diverse taxa, yet the behavioural processes preceding settlement are poorly understood. Here, we investigated age-dependent changes in settlement behaviour in the marine polychaete Platynereis dumerilii larvae in response to Grammatophora marina diatom biofilms. Settlement behaviours (crawling, crawling speed, and track straightness (tortuosity)) were quantified from recordings of larvae at five developmental stages (mid-trochophore to late-nectochaete) in the presence or absence of diatom biofilms, using image segmentation and spot-tracking software. As larvae developed, the proportion of individuals crawling (settlement) over the biofilm increased. Older larvae colonised biofilms more rapidly and showed greater discrimination between G. marina biofilms and non-biofilmed controls. The movement trajectory of older larvae also straightens compared to individuals swimming in the presence of biofilms, or behaviour witnessed in the absence of biofilms. The proportions and magnitudes of these behaviours may reflect changing prioritisation of sensory inputs from physical and chemical cues as larvae develop. Our findings suggest that behavioural traits that are associated with settlement are developmentally programmed in P. dumerilii. Understanding settlement behaviours in P. dumerilii expands on this species behavioural repertoire and sheds light on the evolutionary relationship between marine larvae and microalgal biofilms.

animal behavior and cognition↗

Microalgal biofilm induces larval settlement in the model marine worm Platynereis dumerilii

A free-swimming larval stage features in many marine invertebrate life cycles. To transition to a seafloor-dwelling juvenile stage, larvae need to settle out of the plankton, guided by specific environmental cues that lead them to an ideal habitat for their future life on the seafloor. Although the marine annelid Platynereis dumerilii has been cultured in research labs since the 1950s and has a free-swimming larval stage, specific environmental cues that induce settlement in this nereid worm are yet to be identified. Here we demonstrate that microalgal biofilm is a key settlement cue for P. dumerilii larvae, inducing earlier onset of settlement, and enhancing subsequent juvenile growth as a primary food source. We tested the settlement response of P. dumerilii to 40 different strains of microalgae, predominantly diatom species, finding that P. dumerilii have species-specific preferences in their choice of settlement substrate. The most effective diatom species for inducing P. dumerilii larval settlement were benthic pennate species including Grammatophora marina, Achnanthes brevipes, and Nitzschia ovalis. The identification of specific environmental cues for P. dumerilii settlement enables a link between its ecology and the sensory and nervous system signalling that regulate larval behaviour and development. Incorporation of diatoms into P. dumerilii culture practices will improve the husbandry of this marine invertebrate model.

zoology↗

Developmental toxicity of pre-production plastic pellets affects a large swathe of invertebrate taxa

Microplastics pose risks to marine organisms through ingestion, entanglement, and as carriers of toxic additives and environmental pollutants. Plastic pre-production pellet leachates have been shown to affect the development of sea urchins and, to some extent, mussels. The extent of those developmental effects on other animal phyla remains unknown. Here, we test the toxicity of environmental mixed nurdle samples and new PVC pellets for the embryonic development or asexual reproduction by regeneration of animals from all the major animal superphyla (Lophotrochozoa, Ecdysozoa, Deuterostomia and Cnidaria). Our results show diverse, concentration-dependent impacts in all the species sampled for new pellets, and for molluscs and deuterostomes for environmental samples. Embryo axial formation, cell specification and, specially, morphogenesis seem to be the main processes affected by plastic leachate exposure. Our study serves as a proof of principle for the potentially catastrophic effects that increasing plastic concentrations in the oceans and other ecosystems can have across animal populations from all major animal superphyla.

developmental biology↗

The development of the adult nervous system in the annelid Owenia fusiformis

BackgroundThe evolutionary origins of animal nervous systems remain contentious because we still have a limited understanding of neural development in most major animal clades. Annelids -- a species-rich group with centralised nervous systems -- have played central roles in hypotheses about the origins of animal nervous systems. However, most studies have focused on adults of deeply nested species in the annelid tree. Recently, Owenia fusiformis has emerged as an informative species to reconstruct ancestral traits in Annelida, given its phylogenetic position within the sister clade to all remaining annelids. MethodsCombining immunohistochemistry of the conserved neuropeptides FVamide-lir, RYamide-lir, RGWamide-lir and MIP-lir with gene expression, we comprehensively characterise neural development from larva to adulthood in Owenia fusiformis. ResultsThe early larval nervous system comprises a neuropeptide-rich apical organ connected through peripheral nerves to a prototroch ring and the chaetal sac. There are seven sensory neurons in the prototroch. A bilobed brain forms below the apical organ and connects to the ventral nerve cord of the developing juvenile. During metamorphosis, the brain compresses, becoming ring-shaped, and the trunk nervous system develops several longitudinal cords and segmented lateral nerves. ConclusionsOur findings reveal the formation and reorganisation of the nervous system during the life cycle of O. fusiformis, an early-branching annelid. Despite its apparent neuroanatomical simplicity, this species has a diverse peptidergic nervous system, exhibiting morphological similarities with other annelids, particularly at the larval stages. Our work supports the importance of neuropeptides in animal nervous systems and the evolution of biphasic life cycles.

developmental biology↗

Whole-animal connectome and cell-type complement of the three-segmented Platynereis dumerilii larva

Nervous systems coordinate effectors across the body during movements. We know little about the cellular-level structure of synaptic circuits for such body-wide control. Here we describe the whole-body synaptic connectome and cell-type complement of a three-segmented larva of the marine annelid Platynereis dumerilii. We reconstructed and annotated over 1,500 neurons and 6,500 non-neuronal cells in a whole-body serial electron microscopy dataset. The differentiated cells fall into 180 neuronal and 90 non-neuronal cell types. We analyse the modular network architecture of the entire nervous system and describe polysynaptic pathways from 428 sensory neurons to four effector systems - ciliated cells, glands, pigment cells and muscles. The complete somatic musculature and its innervation will be described in a companion paper. We also investigated intersegmental differences in cell-type complement, descending and ascending pathways, and mechanosensory and peptidergic circuits. Our work provides the basis for understanding whole-body coordination in annelids.

neuroscience↗

CDKN2C homozygous loss identifies a distinct subtype of TP53/RB1-wildtype leiomyosarcoma with frequent CIC genomic alterations and 1p/19q-codeletion

PurposeLeiomyosarcomas (LMS) harbor frequent inactivation of TP53 and RB1, and extensive DNA copy number alterations. Here, we describe a distinct recurrent genomic signature in TP53/RB1-wildtype uterine LMS. MethodsTissues from 276,645 unique advanced cancers, including 2,570 uterine and soft tissue LMS were sequenced by hybrid-capture-based next-generation DNA and RNA sequencing/comprehensive genomic profiling of up to 406 genes. We characterized clinicopathologic features of relevant cases. ResultsWe identified 77 LMS with homozygous copy loss of CDKN2C at chromosome 1p32.3 (3.0% of LMS). Genomic alterations (GAs) in TP53, RB1, and ATRX were rare in comparison with the remainder of the LMS cohort (11.7% vs 73.4%, 0% vs 54.5%, 2.6% vs 24.5%, all p<0.0001). CDKN2C-null LMS cases were significantly enriched for GAs in CIC (40.3% vs 1.4%) at 19q13.2, CDKN2A (46.8% vs 7.0%), and RAD51B (16.9% vs 1.7%; all p<0.0001). Chromosome arm-level aneuploidy analysis of available LMS cases (n=1,251) found that 85% (n=33/39) of CDKN2C-null LMS cases exhibited 1p/19q-codeletion, with significant enrichment in comparison to the remainder of the evaluated LMS cohort (85% vs. 5.1%, p<0.0001). 99% of CDKN2C-null cases were in females; median age was 61 years at surgery (range, 36-81 years). 55 cases were of uterine primary, 4 cases non-uterine, and the remaining 18 of uncertain primary site. 6 patients had a prior history of leiomyomatosis or uterine smooth muscle tumor of uncertain malignant potential. 60% of cases showed at least focal epithelioid variant histology. Most cases were of known advanced stage, with 62% of confirmed uterine primary cases at FIGO stage IVB. ConclusionThe identification of this novel genomic subset may have prognostic and/or therapeutic clinical relevance, including use of specific cyclin-dependent kinase inhibitors.

cancer biology↗

High cell diversity and complex peptidergic signalling underlie placozoan behaviour

Placozoans, together with sponges, are the only animals devoid of a nervous system and muscles, yet both respond to sensory stimulation in a coordinated manner. How behavioural control in these free-living animals is achieved in the absence of neurons and, more fundamentally, how the first neurons evolved from more primitive communication cells during the rise of animals is not yet understood [1-5]. The placozoan Trichoplax adhaerens is a millimeter-wide, flat, free-living marine animal composed of six morphologically identified cell types distributed across a simple bodyplan [6-9]: a flat upper epithelium and a cylindrical lower epithelium interspersed with a loose layer of fiber cells. Its genome encodes several proneuropeptide genes and genes involved in neurosecretion in animals with a nervous system [10-12]. Here we investigate neuropeptide signalling in Trichoplax adhaerens. We found specific expression of several neuropeptides in non-overlapping cell populations distributed over the three cell layers, revealing an unsuspected cell-type diversity of Trichoplax adhaerens. Using live imaging, we uncovered that treatments with 11 different neuropeptides elicited striking and consistent effects on the animals shape, patterns of movement and velocity that we categorized under three main types: (i) crinkling, (ii) turning, and (iii) flattening and churning. Together, the data demonstrate a crucial role for peptidergic signalling in nerveless placozoans and suggest that peptidergic volume signalling may have predated synaptic signalling in the evolution of nervous systems.

neuroscience↗

Dual signaling of Wamide myoinhibitory peptides through a peptide-gated channel and a GPCR in Platynereis

Neuropeptides commonly signal by metabotropic G-protein coupled receptors (GPCRs). In some mollusks and cnidarians, RFamide neuropeptides mediate fast ionotropic signaling by peptide-gated ion channels that belong to the DEG/ENaC family. Here we describe a neuropeptide system with a dual mode of signaling by both a peptide-gated channel and a GPCR. We identified and characterised a peptide-gated channel in the marine annelid Platynereis dumerilii that is specifically activated by Wamide myoinhibitory peptides derived from the same proneuropeptide. The myoinhibitory peptide-gated ion channel (MGIC) belongs to the DEG/ENaC family and is paralogous to RFamide-gated channels. Platynereis myoinhibitory peptides also activate a previously described GPCR, MAG. We measured the potency of all Wamides on both MGIC and MAG and identified peptides that preferentially activate one or the other receptor. Analysis of a single-cell transcriptome resource indicates that MGIC and MAG signal to distinct target neurons. The identification of a Wamide-gated channel suggests that peptide-gated channels are more diverse and widespread in animals than previously appreciated. The possibility of neuropeptide signaling by both ionotropic and metabotropic receptors to different target cells in the same organism highlights an additional level of complexity in peptidergic signaling networks.

neuroscience↗

Synaptic and peptidergic connectome of a neurosecretory centre in the annelid brain

Neurosecretory centres in animal brains use peptidergic signalling to influence physiology and behaviour. Understanding neurosecretory centre function requires mapping cell types, synapses, and peptidergic networks. Here we use electron microscopy and gene expression mapping to analyse the synaptic and peptidergic connectome of an entire neurosecretory centre. We mapped 78 neurosecretory neurons in the brain of larval Platynereis dumerilii, a marine annelid. These neurons form an anterior neurosecretory organ expressing many neuropeptides, including hypothalamic peptide orthologues and their receptors. Analysis of peptide-receptor pairs revealed sparsely connected networks linking specific neuronal subsets. We experimentally analysed one peptide-receptor pair and found that a neuropeptide can couple neurosecretory and synaptic brain signalling. Our study uncovered extensive non-synaptic signalling within a neurosecretory centre and its connection to the synaptic brain.

neuroscience↗

Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva

Ciliated surfaces harbouring synchronously beating cilia can generate fluid flow or drive locomotion. In ciliary swimmers, ciliary beating, arrests, and changes in beat frequency are often coordinated across extended or discontinuous surfaces. To understand how such coordination is achieved, we studied the ciliated larvae of Platynereis dumerilii, a marine annelid. Platynereis larvae have segmental multiciliated cells that regularly display spontaneous coordinated ciliary arrests. We used whole-body connectomics, activity imaging, transgenesis, and neuron ablation to characterize the ciliomotor circuitry. We identified cholinergic, serotonergic, and catecholaminergic ciliomotor neurons. The synchronous rhythmic activation of cholinergic cells drives the coordinated arrests of all cilia. The serotonergic cells are active when cilia are beating. Serotonin inhibits the cholinergic rhythm, and increases ciliary beat frequency. Based on their connectivity and alternating activity, the catecholaminergic cells may generate the rhythm. The ciliomotor circuitry thus constitutes a stop-and-go pacemaker system for the whole-body coordination of ciliary locomotion.

neuroscience↗