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Katz, P. S.

Publications and source records attributed to Katz, P. S..

11 recordsLinked to original sources

Hunger modulates behavioral responses to olfactory and chemotactile cues in the specialist predator of dangerous prey, Berghia stephanieae

Animals continuously evaluate environmental cues to guide approach-avoidance decisions, with internal states like hunger dynamically shaping how stimuli are acted upon. While most studies examine the valence-switching of stimuli from appetitive to aversive using simplified or ambiguous stimuli, we leveraged a system in which a single prey contains both appetitive and aversive features. The nudibranch Berghia stephanieae, is a specialist predator of the sea anemone, Exaiptasia diaphana. These nudibranchs must resolve conflicting signals where chemical cues signal food, while contact can result in injury or death. The danger posed by Exaiptasia was described and quantified through direct counts of nematocysts fired into Berghia and multiple instances where the Berghia was captured and consumed by its prey. To test how internal state influenced the perception of stimuli from prey we recorded predatory behavior of Berghia after different periods of food deprivation. We found that the olfactory cues from prey were attractive to Berghia, even when animals were sated, and usually led to a contact-mediated investigation of prey. Hunger independently modulated olfactory and contact cue valence at different internal states and time scales of food deprivation. Hunger specifically altered the threshold for avoidance following contact with prey, indicating that somatosensory and chemotactile cues are modulated by hunger unlike olfactory cues. Our results highlight how internal state and sensory modality interact to shape decision making in a biologically relevant, high-risk predation context.

animal behavior and cognition↗

MolluscaGenes: A Transcriptomic Database for the Mollusca

The phylum Mollusca constitutes one of the most taxonomically and morphologically diverse animal clades; however, the genomic exploration of this group has been hampered by fragmented and taxonomically incomplete transcriptomic resources. To address this fundamental limitation, we present MolluscaGenes, a centralized database that unifies transcriptomes from 299 molluscan species spanning all eight recognized classes, encompassing a broad array of tissues and developmental stages. MolluscaGenes provides searchable databases via BLAST and DIAMOND alongside a suite of 196 molluscan-optimized Hidden Markov Models (HMMs) for sensitive protein family identification. To demonstrate the utility of this resource, we performed a comprehensive phylum-wide characterization of the nicotinic acetylcholine receptor (nAChR) superfamily, recovering 3,586 sequences from over 190 species and resolving 15 distinct phylogenetic clades. This analysis revealed substantial lineage-specific expansions across multiple molluscan classes, the identification of novel clades with substitutions in canonical ligand-binding residues, and the evolutionary placement of chemotactile receptors (CRs) and CR-like sequences as predominantly cephalopod clades within the broader nAChR phylogeny. MolluscaGenes constitutes a foundational resource that will accelerate the elucidation of the unique biology and evolutionary history of Mollusca.

genomics↗

Social predation by a nudibranch mollusc

Social predation is a common strategy used by predators to subdue and consume prey. Animals that use this strategy have many ways of finding each other, organizing behaviors and consuming prey. There is wide variation in the extent to which these behaviors are coordinated and the stability of individual roles. This study characterizes social predation by the nudibranch mollusc, Berghia stephanieae, which is a specialist predator that eats only the sea anemone, Exaiptasia diaphana. A combination of experimental and modeling approaches showed that B. stephanieae does predate upon E. diaphana in groups. The extent of social feeding was not altered by length of food deprivation, suggesting that animals are not shifting strategies based on internal state. It was unclear what cues the individual Berghia used to find each other; choice assays testing whether they followed slime trails, were attracted to injured anemones, or preferred conspecifics feeding did not reveal any cues. Individuals did not exhibit stable roles, such as leader or follower, rather the population exhibited fission-fusion dynamics with temporary roles during predation. Thus, the Berghia provides an example of a specialist predator of dangerous prey that loosely organizes social feeding, which persists across hunger states and uses temporary individual roles; however, the cues that it uses for aggregation are unknown. Significance StatementSocial predation is a strategy to hunt dangerous prey and minimize injury. Many nudibranchs specialize as predators of cnidarians, which are dangerous to them. Although nudibranchs are typically characterized as solitary hunters, we provide evidence that social predation strategies may be used by a species that specializes on one species of sea anemone. The study showed that the individual sea slugs assumed temporary roles for establishing groups and that the group dynamics were unstable. However, the cues that the nudibranchs use to aggregate remain elusive.

animal behavior and cognition↗

Sample preparation methods for volume electron microscopy in mollusc Berghia stephanieae

Creating a high-resolution brain atlas in diverse species offers crucial insights into general principles underlying brain function and development. A volume electron microscopy approach to generate such neural maps has been gaining importance due to advances in imaging, data storage capabilities, and data analysis protocols. Sample preparation remains challenging and is a crucial step to accelerate the imaging and data processing pipeline. Here, we introduce several replicable methods for processing the brains of the gastropod mollusc, Berghia stephanieae for volume electron microscopy. Although high-pressure freezing is the most reliable method, the depth of cryopreservation is a severe limitation for large tissue samples. We introduce a BROPA-based method using pyrogallol and methods to rapidly process samples that can save hours at the bench. This is the first report on sample preparation and imaging pipeline for volume electron microscopy in a gastropod mollusc, opening up the potential for connectomic analysis and comparisons with other phyla.

neuroscience↗

Egg-laying hormone expression in identified neurons across developmental stages and reproductive states of the nudibranch Berghia stephanieae

Neuropeptides play essential roles in coordinating reproduction. Egg-laying hormone (ELH) is conserved in genetic sequence and behavioral function across molluscs, where neuronal clusters secrete ELH to modulate and induce egg-laying. Here we investigated ELH in the nudibranch mollusc, Berghia stephanieae. ELH preprohormone gene orthologs, which showed clade-specific differences at the C-terminus of the predicted bioactive peptide, were identified in brain transcriptomes across several nudipleuran species, including B. stephanieae. Injection of synthesized B. stephanieae ELH peptide into mature individuals induced egg-laying. ELH gene expression in the brain and body was mapped using in-situ hybridization chain reaction. Across the adult brain, 300-400 neurons expressed ELH. Twenty-one different cell types were identified in adults, three of which were located unilaterally on the right side, which corresponds to the location of the reproductive organs. Ten cell types were present in pre-reproductive juvenile stages. An asymmetric cluster of approximately 100 small neurons appeared in the right pedal ganglion of late-stage juveniles. Additional neurons in the pleural and pedal ganglia expressed ELH only in adults that were actively laying eggs and sub-adults that were on the verge of doing so, implicating their direct role in reproduction. Outside the brain, ELH was expressed on sensory appendages, including in presumptive sensory neurons. ELH shares deep homology with the corticotropin-releasing hormone gene family, which has roles broadly in stress response. Its widespread expression in the nudibranch B. stephanieae suggests that ELH plays a role beyond reproduction in gastropod molluscs. HighlightsO_LIEgg-laying hormone (ELH) preprohormone sequences were identified in the transcriptomes of several nudipleuran molluscs. C_LIO_LIMany ELH-expressing neurons and clusters in the brain could be individually identified based on soma position and morphology. C_LIO_LISome identified ELH-expressing neurons were not observed until later juvenile stages. C_LIO_LISome neurons expressed ELH in adults only when they were actively laying eggs. C_LIO_LIMany hundreds of ELH-expressing neurons were present in peripheral appendages. C_LI

neuroscience↗

A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes

How novel phenotypes originate from conserved genes, processes, and tissues remains a major question in biology. Research that sets out to answer this question often focuses on the conserved genes and processes involved, an approach that explicitly excludes the impact of genetic elements that may be classified as clade-specific, even though many of these genes are known to be important for many novel, or clade-restricted, phenotypes. This is especially true for understudied phyla such as mollusks, where limited genomic and functional biology resources for members of this phylum has long hindered assessments of genetic homology and function. To address this gap, we constructed a chromosome-level genome for the gastropod Berghia stephanieae (Valdes, 2005) to investigate the expression of clade-specific genes across both novel and conserved tissue types in this species. The final assembled and filtered Berghia genome is comparable to other high quality mollusk genomes in terms of size (1.05 Gb) and number of predicted genes (24,960 genes), and is highly contiguous. The proportion of upregulated, clade-specific genes varied across tissues, but with no clear trend between the proportion of clade-specific genes and the novelty of the tissue. However, more complex tissue like the brain had the highest total number of upregulated, clade-specific genes, though the ratio of upregulated clade-specific genes to the total number of upregulated genes was low. Our results, when combined with previous research on the impact of novel genes on phenotypic evolution, highlight the fact that the complexity of the novel tissue or behavior, the type of novelty, and the developmental timing of evolutionary modifications will all influence how novel and conserved genes interact to generate diversity.

genomics↗

Mapping neuronal gene expression reveals aspects of ganglionic organization in a gastropod mollusc

Gastropod molluscs such as Aplysia, Lymnaea, and Tritonia have been important for determining fundamental rules of motor control, learning, and memory because of their large, individually identifiable neurons. Yet for the vast majority of gastropod neurons, as well as glia, there are no established molecular markers, limiting the ability to establish brain-wide structure-function relations. Here we combine high-throughput, single-cell RNA sequencing (scRNAseq) with in-situ hybridization chain reaction (HCR) in the nudibranch Berghia stephanieae to identify and visualize the expression of markers for cell types. Broad neuronal classes were characterized by genes associated with neurotransmitters, like acetylcholine, glutamate, serotonin, and GABA, as well as neuropeptides. These classes were subdivided by other genes including transcriptional regulators and unannotated genes. Marker genes expressed by neurons and glia formed discrete, previously unrecognized regions within and between ganglia. This study provides the foundation for understanding the fundamental cellular organization of gastropod nervous systems.

neuroscience↗

mEMbrain: an interactive deep learning MATLAB tool for connectomic segmentation on commodity desktops

Connectomics is fundamental in propelling our understanding of the nervous systems organization, unearthing cells and wiring diagrams reconstructed from volume electron microscopy (EM) datasets. Such reconstructions, on the one hand, have benefited from ever more precise automatic segmentation methods, which leverage sophisticated deep learning architectures and advanced machine learning algorithms. On the other hand, the field of neuroscience at large, and of image processing in particular, has manifested a need for user-friendly and open source tools which enable the community to carry out advanced analyses. In line with this second vein, here we propose mEMbrain, an interactive MATLAB-based software which wraps algorithms and functions that enable labeling and segmentation of electron microscopy datasets in a user-friendly user interface compatible with Linux and Windows. Through its integration as an API to the volume annotation and segmentation tool VAST, mEMbrain encompasses functions for ground truth generation, image preprocessing, training of deep neural networks, and on-the-fly predictions for proofreading and evaluation. The final goals of our tool are to expedite manual labeling efforts and to harness MATLAB users with an array of semi-automatic approaches for instance segmentation. We tested our tool on a variety of datasets that span different species at various scales, regions of the nervous system and developmental stages. To further expedite research in connectomics, we provide an EM resource of ground truth annotation from 4 different animals and 5 datasets, amounting to around 180 hours of expert annotations, yielding more than 1.2 GB of annotated EM images. In addition, we provide a set of 4 pre-trained networks for said datasets. All tools are available from https://lichtman.rc.fas.harvard.edu/mEMbrain/. With our software, our hope is to provide a solution for lab-based neural reconstructions which does not require coding by the user, thus paving the way to affordable connectomics.

neuroscience↗

State-dependent, visually-guided behaviors in the nudibranch Berghia stephanieae

Nudibranch molluscs have structurally simple eyes whose behavioral roles have not been established. We tested the effects of visual stimuli on the behavior of the nudibranch Berghia stephanieae under different food and hunger conditions. In an arena that was half shaded, animals spent most of their time in the dark, where they also decreased their speed and made more changes in heading. These behavioral differences between the light and dark were less evident in uniformly illuminated or darkened arenas, suggesting that they were not caused by the level of illumination. Berghia responded to distant visual targets; animals approached a stripe that was at least 15{degrees} wide and 50% darker than the background. They did not approach a stripe that was lighter than the background but approached a stripe that was isoluminant with the background, suggesting the detection of spatial information. Animals travelled in convoluted paths in a featureless arena but straightened their paths when a visual target was present even if they did not approach it, suggesting that visual cues were used for navigation. Individuals were less responsive to visual stimuli when food-deprived or in the presence of a food odor. Furthermore, when given a food odor, they had a weaker preference for the dark and behaved similarly in the light and dark. Thus, Berghia exhibits visually-guided behaviors that are influenced by odors and hunger state. Summary statementBehavioral analyses demonstrate that the nudibranch Berghia stephanieae is capable of spatial vision and has visually-guided behaviors that are influenced by olfactory information and hunger state.

animal behavior and cognition↗

Synaptic and membrane conductance underlie phase transition in a simple half-center oscillator

Reciprocally inhibitory modules that form half-center oscillators require mechanisms for escaping or being released from inhibition. The central pattern generator (CPG) underlying swimming by the nudibranch mollusc, Dendronotus iris, is composed of only four neurons that are organized into two competing modules of a half center oscillator. In this system, bursting activity in left-right alternation is not driven by any of the neurons but is an emergent property of the network as a whole. We found that the unique synaptic actions and membrane properties of the two neurons in each module (Si2 and Si3) play complementary roles in generating stable bursting in this network oscillator. Only Si2 evokes fast and strong inhibition of its contralateral counterpart, the termination of which initiates post-inhibitory rebound in the Si3 of that module. Only Si3 is responsible for the rebound excitation because it has a hyperpolarization-activated inward current. Within each module, the synaptic actions and membrane properties of the two neurons complement each other: Si3 excites Si2, which then feeds back slow inhibition to Si3, terminating the burst. Using dynamic clamp, we showed that the magnitude of the slow inhibition sets the period of the oscillator. Thus, the synaptic actions of Si2 provide the hyperpolarization needed for the other module to rebound stably, whereas the membrane properties of Si3 in each module cause it to rebound first and excite Si2 and maintain the burst until the cycle repeats and the other module becomes active.

neuroscience↗

Species and individual differences in serotonin receptor expression in identified neurons are correlated with a motor behavior

The marine mollusc, Pleurobranchaea californica varies daily in whether it swims and this correlates with whether serotonin (5-HT) enhances the strength of synapses made by the swim central pattern generator neuron, C2. Another species, Tritonia diomedea, reliably swims and does not vary in serotonergic neuromodulation. A third species, Hermissenda crassicornis, never produces this behavior and lacks the neuromodulation. We found that expression of particular 5-HT receptor genes in C2 correlates with swimming. Seven 5-HT receptor subtype genes were identified from whole-brain transcriptomes. We isolated individual C2 neurons and sequenced their RNA or measured 5-HT receptor gene expression using quantitative PCR. C2 neurons isolated from Pleurobranchaea individuals that produced a swim motor pattern just prior to isolation expressed the 5-HT2a and 5-HT7 receptor genes, as did the Tritonia samples. These subtypes were absent from C2 neurons isolated from Pleurobranchaea individuals that did not swim that day and from Hermissenda C2 neurons. Expression of other receptors did not correlate with swimming. This suggests that 5-HT2a and 5-HT7 receptors mediate the modulation of C2 synaptic strength and play an important role in swimming. Furthermore, the results suggest that regulation of receptor expression might underlie daily changes in behavior as well as behavioral evolution.

neuroscience↗