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Ragsdale, C. W.

Publications and source records attributed to Ragsdale, C. W..

6 recordsLinked to original sources

Multiple longitudinal tracts in the cephalopod arm sensorimotor system

Octopuses have an incredibly rich behavioral repertoire, exhibiting complex motor acts that require the coordination of eight highly flexible arms, each with hundreds of suckers. These movements are controlled by an axial nerve cord (ANC), equivalent to the spinal cord, situated in the center of the arm musculature. The ANC has a cell body layer which forms a U-shape around its neuropil and is capped aborally, or opposite the sucker, by the cerebrobrachial tract (CBT), a massive fiber bundle known to interconnect the arms and the brain. In vertebrate spinal cords, in addition to the major fiber tracts that interconnect the brain and spinal cord, there are spinospinal connectives that coordinate complex motor behaviors across the appendages. Here, we asked with tract-tracing and immunohistochemistry, whether an octopus arms ANC might also have intrinsic longitudinal connections for coordinated arm and sucker movements. We found that the ANC neuropil is enriched in longitudinal fibers. These fibers form distinct tracts, two within the oral (sucker-side) neuropil and two in the aboral (brachial-side) neuropil. In addition, CBT itself demonstrates four major subtracts, and DiI labeling and dextran tracing suggests that (1) the CBT also carries arm-intrinsic longitudinal connections and (2) the CBT and the neuropil tracts can be subcategorized into those that primarily connect with the sucker and those that serve the arm musculature. We also examined the organization of fiber-tracts in the ANC of the arms and tentacles of two species of squid, establishing that an aboral, extra-neuropil tract is a shared feature across all cephalopod species studied. In addition, the squids also had an oral longitudinal tract, though its positioning and size varied with species and appendage. In sum, these findings describe the neural substrate for coordinating motor behaviors across the length of a cephalopod appendage.

neuroscience↗

Genome reorganisation and expansion shape 3D genome architecture and define a distinct regulatory landscape in coleoid cephalopods

How genomic changes translate into organismal novelties is often confounded by the multi-layered nature of genome architecture and the long evolutionary timescales over which molecular changes accumulate. Coleoid cephalopods (squid, cuttlefish, and octopus) provide a unique system to study these processes due to a large-scale chromosomal rearrangement in the coleoid ancestor that resulted in highly modified karyotypes, followed by lineage-specific fusions, translocations, and repeat expansions. How these events have shaped gene regulatory patterns underlying the evolution of coleoid innovations, including their large and elaborately structured nervous systems, novel organs, and complex behaviours, remains poorly understood. To address this, we integrate Micro-C, RNA-seq, and ATAC-seq across multiple coleoid species, developmental stages, and tissues. We find that while topological compartments are broadly conserved, hundreds of chromatin loops are species- and context-specific, with distinct regulation signatures and dynamic expression profiles. CRISPR-Cas9 knockout of a putative regulatory sequence within a conserved region demonstrates the role of loops in neural development and the prevalence of long-range, inter-compartmental interactions. We propose that differential evolutionary constraints across the coleoid 3D genome allow macroevolutionary processes to shape genome topology in distinct ways, facilitating the emergence of novel regulatory entanglements and ultimately contributing to the evolution and maintenance of complex traits in coleoids.

evolutionary biology↗

Molecular and morphological circuitry of the octopus sucker ganglion

The octopus sucker is a profoundly complex sensorimotor structure. Each of the hundreds of suckers that line the octopus arm can move independently or in concert with one another. These suckers also contain an intricate sensory epithelium, enriched with chemotactile receptors. Much of the massive nervous system embedded in the octopus arm mediates control of the suckers. Each arm houses a large axial nerve cord (ANC), which features local enlargements corresponding to each sucker. There is also a sucker ganglion, a peripheral nervous element, situated in the stalk of every sucker. The structure and function of the sucker ganglion remains obscure. We examined the cellular organization and molecular composition of the sucker ganglion in Octopus bimaculoides. The sucker ganglion has an ellipsoid shape and features an unusual organization: the neuropil of the ganglion is distributed as a cap aborally (away from the sucker) and a small pocket orally (towards the sucker), with neuronal cell bodies concentrated in the space between. Using in situ hybridization, we detected positive expression of sensory (PIEZO) and motor (LHX3 and MNX) neuron markers in the sucker ganglion cell bodies. Nerve fibers spread out from the sucker ganglion, targeting the surrounding sucker musculature and the oral roots extending to the ANC. Our results indicate that the sucker ganglion is composed of both sensory and motor elements and suggest that this ganglion is not a simple relay for the ANC but facilitates local reflexes for each sucker.

neuroscience↗

Neuronal segmentation in cephalopod arms

The prehensile arms of the cephalopod are among these animals most remarkable features, but the neural circuitry governing arm and sucker movements remains largely unknown. We studied the neuronal organization of the adult axial nerve cord (ANC) of Octopus bimaculoides with molecular and cellular methods. The ANCs, which lie in the center of every arm, are the largest neuronal structures in the octopus, containing four times as many neurons as found in the central brain. In transverse cross section, the cell body layer (CBL) of the ANC wraps around its neuropil (NP) with little apparent segregation of sensory and motor neurons or nerve exits. Strikingly, when studied in longitudinal sections, the ANC is segmented. ANC neuronal cell bodies form columns separated by septa, with 15 segments overlying each pair of suckers. The segments underlie a modular organization to the ANC neuropil: neuronal cell bodies within each segment send the bulk of their processes directly into the adjoining neuropil, with some reaching the contralateral side. In addition, some nerve processes branch upon entering the NP, forming short-range projections to neighboring segments and mid-range projections to the ANC segments of adjoining suckers. The septa between the segments are employed as ANC nerve exits and as channels for ANC vasculature. Cellular analysis establishes that adjoining septa issue nerves with distinct fiber trajectories, which across two segments (or three septa) fully innervate the arm musculature. Sucker nerves also use the septa, setting up a nerve fiber "suckerotopy" in the sucker-side of the ANC. Comparative anatomy suggests a strong link between segmentation and flexible sucker-laden arms. In the squid Doryteuthis pealeii, the arms and the sucker- rich club of the tentacles have segments, but the sucker-poor stalk of the tentacles does not. The neural modules described here provide a new template for understanding the motor control of octopus soft tissues. In addition, this finding represents the first demonstration of nervous system segmentation in a mollusc.

neuroscience↗

Signaling ligand heterogeneities in the peduncle complex of the cephalopod mollusc Octopus bimaculoides

The octopus peduncle complex is an agglomeration of neural structures with remarkably diverse functional roles. The complex rests on the optic tract, between the optic lobe and the central brain, and comprises the peduncle lobe proper, the olfactory lobe, and the optic gland. The peduncle lobe regulates visuomotor behaviors, the optic glands control sexual maturation and maternal death, and the olfactory lobe is thought to receive input from the olfactory organ. Recent transcriptomic and metabolomic studies have identified candidate peptide and steroid ligands in the Octopus bimaculoides optic gland. With gene expression for these ligands and their biosynthetic enzymes, we show that optic gland neurochemistry extends beyond the traditional optic gland secretory tissue and into lobular territories. A key finding is that the classically defined olfactory lobe is itself a heterogenous territory and includes steroidogenic territories that overlap with cells expressing molluscan neuropeptides and the synthetic enzyme dopamine beta-hydroxylase.

neuroscience↗

Multiple optic gland signaling pathways implicated in octopus maternal behaviors and death

0. Summary statementOctopus optic glands employ a multiplex progression of signaling molecules to regulate maternal behaviors.\n\n1. AbstractPost-reproductive life in the female octopus is characterized by an extreme pattern of maternal care: the mother cares for her clutch of eggs without feeding until her death. These maternal behaviors are completely eradicated if the optic glands, the octopus analog of the vertebrate pituitary gland, are removed from brooding females. Despite the optic glands importance in regulating maternal behavior, the molecular features underlying optic gland function are unknown. Here, we identify major signaling systems of the Octopus bimaculoides optic gland. Through behavioral analyses and transcriptome sequencing, we report that the optic gland undergoes remarkable molecular changes that coincide with transitions between behavioral stages. These include the dramatic up- and down-regulation of catecholamine, steroid, insulin, and feeding peptide pathways. Transcriptome analyses in other tissues demonstrate that these molecular changes are not generalized markers of aging and senescence, but instead, specific features of the optic glands. Our results provide strong evidence for the functional conservation of signaling molecules across evolutionarily distant species. For example, elevated levels of insulin growth factor binding proteins are associated with cachexia-like tissue wasting in flies, humans, and, reported here, octopuses. Our study expands the classic optic gland-pituitary gland analogy and indicates that, rather than a single \"self-destruct\" hormone, the maternal optic glands employ multiple pathways as systemic hormonal signals of behavioral control.

animal behavior and cognition↗