Publications by authors named "Roger P Croll"

61 Publications

FMRF-NH -related neuropeptides in Biomphalaria spp., intermediate hosts for schistosomiasis: Precursor organization and immunohistochemical localization.

J Comp Neurol 2021 May 26. Epub 2021 May 26.

Institute of Neurobiology and Department of Anatomy and Neurobiology, University of Puerto Rico, Medical Sciences Campus, San Juan, Puerto Rico.

Freshwater snails of the genus Biomphalaria serve as intermediate hosts for the digenetic trematode Schistosoma mansoni, the etiological agent for the most widespread form of intestinal schistosomiasis. As neuropeptide signaling in host snails can be altered by trematode infection, a neural transcriptomics approach was undertaken to identify peptide precursors in Biomphalaria glabrata, the major intermediate host for S. mansoni in the Western Hemisphere. Three transcripts that encode peptides belonging to the FMRF-NH -related peptide (FaRP) family were identified in B. glabrata. One transcript encoded a precursor polypeptide (Bgl-FaRP1; 292 amino acids) that included eight copies of the tetrapeptide FMRF-NH and single copies of FIRF-NH , FLRF-NH , and pQFYRI-NH . The second transcript encoded a precursor (Bgl-FaRP2; 347 amino acids) that comprised 14 copies of the heptapeptide GDPFLRF-NH and 1 copy of SKPYMRF-NH . The precursor encoded by the third transcript (Bgl-FaRP3; 287 amino acids) recapitulated Bgl-FaRP2 but lacked the full SKPYMRF-NH peptide. The three precursors shared a common signal peptide, suggesting a genomic organization described previously in gastropods. Immunohistochemical studies were performed on the nervous systems of B. glabrata and B. alexandrina, a major intermediate host for S. mansoni in Egypt. FMRF-NH -like immunoreactive (FMRF-NH -li) neurons were located in regions of the central nervous system associated with reproduction, feeding, and cardiorespiration. Antisera raised against non-FMRF-NH peptides present in the tetrapeptide and heptapeptide precursors labeled independent subsets of the FMRF-NH -li neurons. This study supports the participation of FMRF-NH -related neuropeptides in the regulation of vital physiological and behavioral systems that are altered by parasitism in Biomphalaria.
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http://dx.doi.org/10.1002/cne.25195DOI Listing
May 2021

The glomerular network of the zebrafish olfactory bulb.

Cell Tissue Res 2021 Jan 23;383(1):255-271. Epub 2021 Jan 23.

Department of Physiology and Biophysics, Dalhousie University, Halifax, Nova Scotia, B3H4R2, Canada.

Each zebrafish olfactory bulb contains ~ 140 glomeruli that are distinguishable based on size, location, neurochemistry and function. Here we examine the mitral cell innervation of differently sized glomeruli in adult zebrafish. Type 1 glomeruli had diameters of 80.9 ± 8.1 μm and were innervated by 5.9 ± 0.9 mitral cells. The Type 1 mediodorsal glomeruli (mdG) were innervated by both uniglomerular (innervating only single glomeruli) and multiglomerular mitral cells (innervating two or more glomeruli). In contrast, the Type 1 ventroposterior (vpG) and lateral glomeruli (lG) were only innervated by uniglomerular mitral cells. Type 2 ventral glomeruli were 46 ± 5.1 μm in diameter and were innervated by 3.3 ± 0.2 mitral cells. Type 2 ventromedial glomeruli (vmG) were innervated exclusively by uniglomerular mitral cells. Type 3 glomeruli had diameters of 17 ± 2.5 μm and were innervated by 1.1 ± 0.6 multiglomerular mitral cells each. Finally, Type 4 glomeruli were small, with average diameters of 4.8 ± 3.9 μm and were restricted to the lateral plexus. These glomeruli were innervated mainly by multiglomerular mitral cells with extensively branching dendrites. This study provides the first specific associations between uni- and multiglomerular mitral cells with known zebrafish glomeruli. Our results suggest that glomeruli are distinguishable based on their postsynaptic compartment and that distinct input-output computations occur in different types of zebrafish glomeruli.
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http://dx.doi.org/10.1007/s00441-020-03394-4DOI Listing
January 2021

Identification and localization of a gonadotropin-releasing hormone-related neuropeptide in Biomphalaria, an intermediate host for schistosomiasis.

J Comp Neurol 2021 Jun 27;529(9):2347-2361. Epub 2021 Jan 27.

Institute of Neurobiology and Department of Anatomy and Neurobiology, University of Puerto Rico, Medical Sciences Campus, San Juan, Puerto Rico.

Freshwater snails of the genus Biomphalaria serve as obligatory hosts for the digenetic trematode Schistosoma mansoni, the causative agent for the most widespread form of intestinal schistosomiasis. Within Biomphalaria, S. mansoni larvae multiply and transform into the cercariae form that can infect humans. Trematode development and proliferation is thought to be facilitated by modifications of host behavior and physiological processes, including a reduction of reproduction known as "parasitic castration." As neuropeptides participate in the control of reproduction across phylogeny, a neural transcriptomics approach was undertaken to identify peptides that could regulate Biomphalaria reproductive physiology. The present study identified a transcript in Biomphalaria alexandrina that encodes a peptide belonging to the gonadotropin-releasing hormone (GnRH) superfamily. The precursor and the predicted mature peptide, pQIHFTPDWGNN-NH (designated Biom-GnRH), share features with peptides identified in other molluscan species, including panpulmonates, opisthobranchs, and cephalopods. An antibody generated against Biom-GnRH labeled neurons in the cerebral, pedal, and visceral ganglia of Biomphalaria glabrata. GnRH-like immunoreactive fiber systems projected to all central ganglia. In the periphery, immunoreactive material was detected in the ovotestis, oviduct, albumen gland, and nidamental gland. As these structures serve crucial roles in the production, transport, nourishment, and encapsulation of eggs, disruption of the GnRH system of Biomphalaria could contribute to reduced reproductive activity in infected snails.
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http://dx.doi.org/10.1002/cne.25099DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8142820PMC
June 2021

Disrupted local innervation results in less VIP expression in CF mice tissues.

J Cyst Fibros 2021 01 27;20(1):154-164. Epub 2020 Jun 27.

Department of Physiology and Biophysics, Faculty of Medicine, Dalhousie University, Halifax, NS, Canada. Electronic address:

Vasoactive Intestinal Peptide (VIP) is the major physiological agonist of the Cystic Fibrosis Transmembrane conductance Regulator (CFTR) chloride channel activity. VIP functions as a neuromodulator and neurotransmitter secreted by neurons innervating all exocrine glands. VIP is also a potent vasodilator and bronchodilator that regulates exocrine gland secretions, contributing to local innate defense by stimulating the movement of water and chloride transport across intestinal and tracheobronchial epithelia. Previous human studies have shown that the rich intrinsic neuronal networks for VIP secretion around exocrine glands could be lost in tissues from patients with cystic fibrosis. Our research has since confirmed, in vitro and in vivo, the need for chronic VIP exposure to maintain functional CFTR chloride channels at the cell surface of airways and intestinal epithelium, as well as normal exocrine tissues morphology [1]. The goal of the present study was to examine changes in VIP in the lung, duodenum and sweat glands of 8- and 17-weeks old F508del/F508del mice and to investigate VIPergic innervation in the small intestine of CF mice, before important signs of the disease development. Our data show that a low amount of VIP is found in CF tissues prior to tissue damage. Moreover, we found a specific reduction in VIPergic and cholinergic innervation of the small intestine. The general innervation of the primary and secondary myenteric plexus was lost in CF tissues, with the presence of enlarged ganglionic cells in the tertiary layer. We propose that low amount of VIP in CF tissues is due to a reduction in VIPergic and cholinergic innervation and represents an early defect that constitutes an aggravating factor for CF disease progression.
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http://dx.doi.org/10.1016/j.jcf.2020.06.013DOI Listing
January 2021

Biochemical and apoptotic changes in the nervous and ovotestis tissues of Biomphalaria alexandrina following infection with Schistosoma mansoni.

Exp Parasitol 2020 Jun 26;213:107887. Epub 2020 Mar 26.

Institute of Neurobiology, University of Puerto Rico, Medical Sciences Campus, San Juan, Puerto Rico; Department of Anatomy & Neurobiology, University of Puerto Rico, Medical Science Campus, San Juan, Puerto Rico.

Infection with trematodes produces physiological and behavioural changes in intermediate snail hosts. One response to infection is parasitic castration, in which energy required for reproduction of the host is thought to be redirected to promote development and multiplication of the parasite. This study investigated some reproductive and biochemical parameters in the nervous (CNS) and ovotestis (OT) tissues of Biomphalaria alexandrina during the course of Schistosoma mansoni infection. Antioxidant and oxidative stress parameters including catalase (CAT), nitric oxide (NO) and lipid peroxidation (MDA) were measured. Levels of steroid hormones, including testosterone, progesterone and estradiol, were also assessed. Finally, flow cytometry was used to compare measures of apoptosis between control snails and those shedding cercariae by examining mitochondrial membrane potential with the stain 5,5',6,6'-tetrachloro-1,1',3,3'-tetraethylbenzimi-dazolylcarbocyanine iodide (JC-1) and poly(ADP-ribose) polymerase (PARP). Infection with S. mansoni caused a 47.7% reduction in the net reproductive rate (R) of B. alexandrina. CAT activity was increased in the CNS at 21 days post infection (dpi) but by 28 dpi it was reduced below control values. Also, CAT activity increased significantly in the OT at 14, 21 and 28 dpi. In CNS tissues, NO levels were reduced at 7 dpi, increased at 14 and 21 dpi, and reduced again at 28 dpi. The overall level of lipid peroxidation gradually increased during the course of infection to reach its highest levels at 28 dpi. Steroid hormone measurements showed that concentrations of testosterone and estradiol were reduced in the CNS tissues at 28 dpi, while those of progesterone were slightly increased in the CNS and OT tissues. The percentage of cells that positively stained with JC-1was significantly increased in CNS and OT tissues of infected snails while the percentage of cells positively stained with PARP was decreased compared to controls. Together, these findings indicate that infection initiates diverse biochemical and hormonal changes leading to loss of cells responsible for egg laying and reproduction in B. alexandrina.
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http://dx.doi.org/10.1016/j.exppara.2020.107887DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8105080PMC
June 2020

Histamine and histidine decarboxylase in the olfactory system and brain of the common cuttlefish Sepia officinalis (Linnaeus, 1758).

J Comp Neurol 2020 05 24;528(7):1095-1112. Epub 2019 Nov 24.

Department of Physiology and Biophysics, Dalhousie University, Halifax, Nova Scotia, Canada.

Cephalopods are radically different from any other invertebrate. Their molluscan heritage, innovative nervous system, and specialized behaviors create a unique blend of characteristics that are sometimes reminiscent of vertebrate features. For example, despite differences in the organization and development of their nervous systems, both vertebrates and cephalopods use many of the same neurotransmitters. One neurotransmitter, histamine (HA), has been well studied in both vertebrates and invertebrates, including molluscs. While HA was previously suggested to be present in the cephalopod central nervous system (CNS), Scaros, Croll, and Baratte only recently described the localization of HA in the olfactory system of the cuttlefish Sepia officinalis. Here, we describe the location of HA using an anti-HA antibody and a probe for histidine decarboxylase (HDC), a synthetic enzyme for HA. We extended previous descriptions of HA in the olfactory organ, nerve, and lobe, and describe HDC staining in the same regions. We found HDC-positive cell populations throughout the CNS, including the optic gland and the peduncle, optic, dorso-lateral, basal, subvertical, frontal, magnocellular, and buccal lobes. The distribution of HA in the olfactory system of S. officinalis is similar to the presence of HA in the chemosensory organs of gastropods but is different than the sensory systems in vertebrates or arthropods. However, HA's widespread abundance throughout the rest of the CNS of Sepia is a similarity shared with gastropods, vertebrates, and arthropods. Its widespread use with differing functions across Animalia provokes questions regarding the evolutionary history and adaptability of HA as a transmitter.
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http://dx.doi.org/10.1002/cne.24809DOI Listing
May 2020

Localization of keyhole limpet hemocyanin-like immunoreactivity in the nervous system of Biomphalaria alexandrina.

J Neurosci Res 2019 11 4;97(11):1469-1482. Epub 2019 Aug 4.

Department of Physiology & Biophysics, Dalhousie University, Halifax, NS, Canada.

Recent years have led to increased effort to describe and understand the peripheral nervous system and its influence on central mechanisms and behavior in gastropod molluscs. This study revealed that an antibody raised against keyhole limpet hemocyanin (KLH) cross-reacts with an antigen(s) found extensively in both the central and the peripheral nervous systems of Biomphalaria alexandrina. The results revealed KLH-like immunoreactive (LIR) neurons in the cerebral, pedal, buccal, left pleural, right parietal, and visceral ganglion within the CNS with fibers projecting throughout all the peripheral nerves. Numerous KLH-LIR peripheral sensory neurons located in the foot, lips, tentacles, mantle, esophagus, and penis exhibited a bipolar morphology with long tortuous dendrites. KLH-LIR cells were also present in the eye and statocyst, thus suggesting the labeling of multiple sensory modalities/cell types. KLH-LIR cells did not co-localize with tyrosine hydroxylase (TH)-LIR cells, which have previously been described in this and other gastropods. The results thus provide descriptions of thousands of peripheral sensory neurons, not previously described in detail. Future research should seek to pair sensory modalities with peripheral cell type and attempt to further elucidate the nature of KLH-like reactivity. These findings also emphasize the need for caution when analyzing results obtained through use of antibodies raised against haptens conjugated to carrier proteins, suggesting the need for stringent controls to help limit potential confounds caused by cross-reactivity. In addition, this study is the first to describe neuronal cross-reactivity with KLH in Biomphalaria, which could provide a substrate for host-parasite interactions with a parasitic trematode, Schistosoma.
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http://dx.doi.org/10.1002/jnr.24497DOI Listing
November 2019

An immunohistochemical analysis of peptidergic neurons apparently associated with reproduction and growth in Biomphalaria alexandrina.

Gen Comp Endocrinol 2019 09 26;280:1-8. Epub 2019 Mar 26.

Department of Physiology & Biophysics, Dalhousie University, Halifax, NS, Canada. Electronic address:

Peptide hormones and neurotransmitters involved in reproduction and growth have been studied extensively in certain gastropod molluscs, such as Lymnaea stagnalis and Aplysia californica. The present study employs antisera that have been used to study peptidergic neurons in those species to probe the central nervous system of another gastropod, Biomphalaria alexandrina, an intermediate host of the parasitic trematode that causes schistosomiasis in humans. Whole mount preparations of central ganglia were stained immunohistochemically, and several populations of neurons appeared to be homologous to those forming the neuroendocrine axis that has been previously described in L. stagnalis. These cells include the caudodorsal cells and the light green and canopy cells, which produce hormones that regulate ovulation and growth, respectively. Other populations of cells containing APGWamide, FMRFamide and/or related peptides are consistent with ones that innervate the penis in L. stagnalis and other gastropods. Identification of neurons that might be responsible for the control of reproduction and growth in Biomphalaria provides an important initial step toward the development of novel methods of disease control and pest management directed toward reducing snail populations.
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http://dx.doi.org/10.1016/j.ygcen.2019.03.017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6635034PMC
September 2019

Animal Models in the Pathophysiology of Cystic Fibrosis.

Front Pharmacol 2018 4;9:1475. Epub 2019 Jan 4.

Department of Physiology and Biophysics, Faculty of Medicine, Dalhousie University, Halifax, NS, Canada.

Our understanding of the multiorgan pathology of cystic fibrosis (CF) has improved impressively during the last decades, but we still lack a full comprehension of the disease progression. Animal models have greatly contributed to the elucidation of specific mechanisms involved in CF pathophysiology and the development of new therapies. Soon after the cloning of the CF transmembrane conductance regulator () gene in 1989, the first mouse model was generated and this model has dominated CF research ever since. Nonetheless, the failure of murine models to mirror human disease severity in the pancreas and lung has led to the generation of larger animal models such as pigs and ferrets. The following review presents and discusses data from the current animal models used in CF research.
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http://dx.doi.org/10.3389/fphar.2018.01475DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6328443PMC
January 2019

Etiology and functional validation of gastrointestinal motility dysfunction in a zebrafish model of CHARGE syndrome.

FEBS J 2018 06 27;285(11):2125-2140. Epub 2018 Apr 27.

Department of Pediatrics, Dalhousie University, Halifax, Canada.

CHARGE syndrome is linked to autosomal-dominant mutations in the CHD7 gene and results in a number of physiological and structural abnormalities, including heart defects, hearing and vision loss, and gastrointestinal (GI) problems. Of these challenges, GI problems have a profound impact throughout an individual's life, resulting in increased morbidity and mortality. A homolog of CHD7 has been identified in the zebrafish, the loss of which recapitulates many of the features of the human disease. Using a morpholino chd7 knockdown model complemented by a chd7 null mutant zebrafish line, we examined GI structure, innervation, and motility in larval zebrafish. Loss of chd7 resulted in physically smaller GI tracts with normal epithelial and muscular histology, but decreased and disorganized vagal projections, particularly in the foregut. chd7 morphant larvae had significantly less ability to empty their GI tract of gavaged fluorescent beads, and this condition was only minimally improved by the prokinetic agents, domperidone and erythromycin, in keeping with mixed responses to these agents in patients with CHARGE syndrome. The conserved genetics and transparency of the zebrafish have provided new insights into the consequences of chd7 gene dysfunction on the GI system and cranial nerve patterning. These findings highlight the opportunity of the zebrafish to serve as a preclinical model for studying compounds that may improve GI motility in individuals with CHARGE syndrome.
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http://dx.doi.org/10.1111/febs.14473DOI Listing
June 2018

GABA-like immunoreactivity in Biomphalaria: Colocalization with tyrosine hydroxylase-like immunoreactivity in the feeding motor systems of panpulmonate snails.

J Comp Neurol 2018 08 6;526(11):1790-1805. Epub 2018 May 6.

Institute of Neurobiology and Department of Anatomy & Neurobiology, University of Puerto Rico, Medical Sciences Campus, San Juan, Puerto Rico.

The simpler nervous systems of certain invertebrates provide opportunities to examine colocalized classical neurotransmitters in the context of identified neurons and well defined neural circuits. This study examined the distribution of γ-aminobutyric acid-like immunoreactivity (GABAli) in the nervous system of the panpulmonates Biomphalaria glabrata and Biomphalaria alexandrina, major intermediate hosts for intestinal schistosomiasis. GABAli neurons were localized in the cerebral, pedal, and buccal ganglia of each species. With the exception of a projection to the base of the tentacle, GABAli fibers were confined to the CNS. As GABAli was previously reported to be colocalized with markers for dopamine (DA) in five neurons in the feeding network of the euopisthobranch gastropod Aplysia californica (Díaz-Ríos, Oyola, & Miller, 2002), double-labeling protocols were used to compare the distribution of GABAli with tyrosine hydroxylase immunoreactivity (THli). As in Aplysia, GABAli-THli colocalization was limited to five neurons, all of which were located in the buccal ganglion. Five GABAli-THli cells were also observed in the buccal ganglia of two other intensively studied panpulmonate species, Lymnaea stagnalis and Helisoma trivolvis. These findings indicate that colocalization of the classical neurotransmitters GABA and DA in feeding central pattern generator (CPG) interneurons preceded the divergence of euopisthobranch and panpulmonate taxa. These observations also support the hypothesis that heterogastropod feeding CPG networks exhibit a common universal design.
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http://dx.doi.org/10.1002/cne.24448DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5990452PMC
August 2018

Immunohistochemical Approach to Understanding the Organization of the Olfactory System in the Cuttlefish, Sepia officinalis.

ACS Chem Neurosci 2018 08 5;9(8):2074-2088. Epub 2018 Apr 5.

Sorbonne Université, MNHN, UNICAEN, UA, CNRS, IRD, Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), Paris 75005 , France.

Cephalopods are nontraditional but captivating models of invertebrate neurobiology, particularly in evolutionary comparisons. Cephalopod olfactory systems have striking similarities and fundamental differences with vertebrates, arthropods, and gastropods, raising questions about the ancestral origins of those systems. We describe here the organization and development of the olfactory system of the common cuttlefish, Sepia officinalis, using immunohistochemistry and in situ hybridization. FMRFamide and/or related peptides and histamine are putative neurotransmitters in olfactory sensory neurons. Other neurotransmitters, including serotonin and APGWamide within the olfactory and other brain lobes, suggest efferent control of olfactory input and/or roles in the processing of olfactory information. The distributions of neurotransmitters, along with staining patterns of phalloidin, anti-acetylated α-tubulin, and a synaptotagmin riboprobe, help to clarify the structure of the olfactory lobe. We discuss a key difference, the lack of identifiable olfactory glomeruli, in cuttlefish in comparison to other models, and suggest its implications for the evolution of olfaction.
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http://dx.doi.org/10.1021/acschemneuro.8b00021DOI Listing
August 2018

Differences in Larval Arm Movements Correlate with the Complexity of Musculature in Two Phylogenetically Distant Echinoids, Eucidaris tribuloides (Cidaroidea) and Lytechinus variegatus (Euechinoidea).

Biol Bull 2017 10 20;233(2):111-122. Epub 2017 Dec 20.

Within a common body plan, echinoid planktotrophic larvae are morphologically diverse, with variations in overall size, the length, and number of arms and the presence or absence of epidermal structures. In this report, we are interested in variation in larval arm-flexing behavior and correlated differences in larval musculature. Larvae of the cidaroid Eucidaris tribuloides exhibit conspicuous and regular arm-flexing behavior. In contrast, Lytechinus variegatus, a representative of the euechinoid clade, does not exhibit this behavior. We hypothesized that there were differences in musculature that correlated with this behavioral contrast and compared the development and structure of larval muscles between these species. We report substantial differences in some aspects of larval musculature. In addition to previously described oral musculature, both larvae possessed polygon-shaped musculature at the basal end of the larva. However, larval musculature in E. tribuloides was larger and contained additional muscles not observed in larvae of L. variegatus. Therefore, a conspicuous larval behavior consisting of repeated flexing of the postoral and posterodorsal larval arms was correlated with a larger, more complex musculature. This simple contrast indicates that larval musculature not associated with endoderm evolves in a manner that relates to differences in larval behavior and that additional comparisons are warranted.
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http://dx.doi.org/10.1086/694892DOI Listing
October 2017

Central nervous system transcriptome of Biomphalaria alexandrina, an intermediate host for schistosomiasis.

BMC Res Notes 2017 Dec 11;10(1):729. Epub 2017 Dec 11.

Institute of Neurobiology and Department of Anatomy & Neurobiology, University of Puerto Rico, Medical Sciences Campus, 201 Blvd del Valle, San Juan, Puerto Rico.

Objective: Globally, more than 200 million people live at risk of the neglected tropical disease schistosomiasis (or snail fever). Larval schistosomes require the presence of specific snail species that act as intermediate hosts, supporting their multiplication and transformation into forms that can infect humans. This project was designed to generate a transcriptome from the central nervous system (CNS) of Biomphalaria alexandrina, the major intermediate host for Schistosoma mansoni in Egypt.

Results: A transcriptome was generated from five pooled central nervous systems dissected from uninfected specimens of B. alexandrina. Raw Illumina RNA-seq data (~ 20.3 million paired end reads of 150 base pairs length each) generated a transcriptome consisting of 144,213 transcript elements with an N50 contig size of 716 base pairs. Orthologs of 15,246 transcripts and homologs for an additional 16,810 transcripts were identified in the UniProtKB/Swiss-Prot database. The B. alexandrina CNS transcriptome provides a resource for future research exploring parasite-host interactions in a simpler nervous system. Moreover, increased understanding of the neural signaling mechanisms involved in the response of B. alexandrina to infection by S. mansoni larvae could lead to novel and highly specific strategies for the control of snail populations.
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http://dx.doi.org/10.1186/s13104-017-3018-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5725652PMC
December 2017

Skeletal stiffening in an amphibious fish out of water is a response to increased body weight.

J Exp Biol 2017 10;220(Pt 20):3621-3631

Department of Integrative Biology, University of Guelph, 50 Stone Road East, Guelph, ON, Canada N1G 2W1.

Terrestrial animals must support their bodies against gravity, while aquatic animals are effectively weightless because of buoyant support from water. Given this evolutionary history of minimal gravitational loading of fishes in water, it has been hypothesized that weight-responsive musculoskeletal systems evolved during the tetrapod invasion of land and are thus absent in fishes. Amphibious fishes, however, experience increased effective weight when out of water - are these fishes responsive to gravitational loading? Contrary to the tetrapod-origin hypothesis, we found that terrestrial acclimation reversibly increased gill arch stiffness (∼60% increase) in the amphibious fish when loaded normally by gravity, but not under simulated microgravity. Quantitative proteomics analysis revealed that this change in mechanical properties occurred via increased abundance of proteins responsible for bone mineralization in other fishes as well as in tetrapods. Type X collagen, associated with endochondral bone growth, increased in abundance almost ninefold after terrestrial acclimation. Collagen isoforms known to promote extracellular matrix cross-linking and cause tissue stiffening, such as types IX and XII collagen, also increased in abundance. Finally, more densely packed collagen fibrils in both gill arches and filaments were observed microscopically in terrestrially acclimated fish. Our results demonstrate that the mechanical properties of the fish musculoskeletal system can be fine-tuned in response to changes in effective body weight using biochemical pathways similar to those in mammals, suggesting that weight sensing is an ancestral vertebrate trait rather than a tetrapod innovation.
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http://dx.doi.org/10.1242/jeb.161638DOI Listing
October 2017

The in vitro zebrafish heart as a model to investigate the chronotropic effects of vapor anesthetics.

Am J Physiol Regul Integr Comp Physiol 2017 Dec 6;313(6):R669-R679. Epub 2017 Sep 6.

Department of Medical Neuroscience, Dalhousie University, Halifax, Nova Scotia, Canada

In addition to their intended clinical actions, all general anesthetic agents in common use have detrimental intrasurgical and postsurgical side effects on organs and systems, including the heart. The major cardiac side effect of anesthesia is bradycardia, which increases the probability of insufficient systemic perfusion during surgery. These side effects also occur in all vertebrate species so far examined, but the underlying mechanisms are not clear. The zebrafish heart is a powerful model for studying cardiac electrophysiology, employing the same pacemaker system and neural control as do mammalian hearts. In this study, isolated zebrafish hearts were significantly bradycardic during exposure to the vapor anesthetics sevoflurane (SEVO), desflurane (DES), and isoflurane (ISO). Bradycardia induced by DES and ISO continued during pharmacological blockade of the intracardiac portion of the autonomic nervous system, but the chronotropic effect of SEVO was eliminated during blockade. Bradycardia evoked by vagosympathetic nerve stimulation was augmented during DES and ISO exposure; nerve stimulation during SEVO exposure had no effect. Together, these results support the hypothesis that the cardiac chronotropic effect of SEVO occurs via a neurally mediated mechanism, while DES and ISO act directly upon cardiac pacemaker cells via an as yet unknown mechanism.
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http://dx.doi.org/10.1152/ajpregu.00467.2016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5814691PMC
December 2017

Distribution and chronotropic effects of serotonin in the zebrafish heart.

Auton Neurosci 2017 09 19;206:43-50. Epub 2017 Jul 19.

Department of Physiology & Biophysics, Faculty of Medicine, Dalhousie University, Halifax, Nova Scotia, Canada. Electronic address:

Several lines of evidence suggest that serotonin (5-HT) has a regulatory role in cardiovascular function from embryogenesis through adulthood. However, the reported actions of 5-HT are often contradictory and include bradycardia or tachycardia, hypotension or hypertension, and vasodilation or vasoconstriction. Clarifying such cardiac effects requires further research and may benefit from utilizing a model simpler than the mammalian hearts traditionally used in these studies. In the present study, we describe the cardiac distribution and chronotropic responses of 5-HT in the zebrafish heart. A combined anatomical, electrophysiological, and pharmacological approach was used to investigate the involvement of 5-HT pathways, and to compare neural and direct myocardial pathways of biological action. Immunohistochemical methods revealed 5-HT in endocardial cells, glial-like cells, and intracardiac neurons in the atrium. Electrocardiogram (ECG) recordings combined with the administration of pharmacological agents demonstrated that 5-HT acted predominantly through direct myocardial pathways resulting in a reduction of heart rate. Overall, the results of this study contribute significant advances in the establishment of the zebrafish as a new model for studies of the role of 5-HT in autonomic cardiac control.
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http://dx.doi.org/10.1016/j.autneu.2017.07.004DOI Listing
September 2017

GABA-, histamine-, and FMRFamide-immunoreactivity in the visual, vestibular and central nervous systems of Hermissenda crassicornis.

J Comp Neurol 2017 Nov 11;525(16):3514-3528. Epub 2017 Aug 11.

Department of Biology, St. Francis Xavier University, Antigonish, Nova Scotia, Canada.

Hermissenda crassicornis is a model for studying the molecular and cellular basis for classical conditioning, based on its ability to associate light with vestibular stimulation. We used confocal microscopy to map histamine (HA), FMRF-amide, and γ-aminobutyric acid (GABA) immunoreactivity in the central nervous system (CNS), eyes, optic ganglia and statocysts of the nudibranchs. For HA immunoreactivity, we documented both consistently and variably labeled CNS structures across individuals. We also noted minor differences in GABA immunoreactivity in the CNS compared to previous work on Hermissenda. Contrary to expectations, we found no evidence for GABA inside the visual or vestibular systems. Instead, we found only FMRFamide- and HA immunoreactivity (FMRFamide: 4 optic ganglion cells, 4-5 hair cells; HA: 3 optic ganglion cells, 8 hair cells). Overall, our results can act as basis for comparisons of nervous systems across nudibranchs, and suggest further exploration of intraspecific plasticity versus evolutionary changes in gastropod nervous systems.
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http://dx.doi.org/10.1002/cne.24286DOI Listing
November 2017

An ancient role for nitric oxide in regulating the animal pelagobenthic life cycle: evidence from a marine sponge.

Sci Rep 2016 11 22;6:37546. Epub 2016 Nov 22.

School of Biological Sciences, University of Queensland, Brisbane QLD 4072, Australia.

In many marine invertebrates, larval metamorphosis is induced by environmental cues that activate sensory receptors and signalling pathways. Nitric oxide (NO) is a gaseous signalling molecule that regulates metamorphosis in diverse bilaterians. In most cases NO inhibits or represses this process, although it functions as an activator in some species. Here we demonstrate that NO positively regulates metamorphosis in the poriferan Amphimedon queenslandica. High rates of A. queenslandica metamorphosis normally induced by a coralline alga are inhibited by an inhibitor of nitric oxide synthase (NOS) and by a NO scavenger. Consistent with this, an artificial donor of NO induces metamorphosis even in the absence of the alga. Inhibition of the ERK signalling pathway prevents metamorphosis in concert with, or downstream of, NO signalling; a NO donor cannot override the ERK inhibitor. NOS gene expression is activated late in embryogenesis and in larvae, and is enriched in specific epithelial and subepithelial cell types, including a putative sensory cell, the globular cell; DAF-FM staining supports these cells being primary sources of NO. Together, these results are consistent with NO playing an activating role in induction of A. queenslandica metamorphosis, evidence of its highly conserved regulatory role in metamorphosis throughout the Metazoa.
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http://dx.doi.org/10.1038/srep37546DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5118744PMC
November 2016

Data on horizontal and vertical movements of zebrafish during appetitive conditioning.

Data Brief 2016 Dec 22;9:758-763. Epub 2016 Oct 22.

Department of Physiology & Biophysics, Dalhousie University, Halifax, NS B3H 4R2, Canada.

This article provides supporting data for the research article "A simple automated system for appetitive conditioning of zebrafish in their home tanks" (J.M. Doyle, N. Merovitch, R.C. Wyeth, M.R. Stoyek, M. Schmidt, F. Wilfart, A. Fine, R.P. Croll, 2016) [1]. In that article, we described overall movements of zebrafish toward a food source as a response to auditory or visual cues as conditioned stimuli in a novel learning paradigm. Here, we describe separate analyses of the vertical and horizontal components of the learned response. These data provide evidence that the conditioning might result from both classical conditioning of an innate response of zebrafish to move to the surface in response to food cues and secondary conditioning of the fish to associate a food presentation with a specific location in the tank. Movement data from the twenty trial acquisition period and probe trials from 2-32 days post conditioning are included.
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http://dx.doi.org/10.1016/j.dib.2016.10.007DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5097951PMC
December 2016

A simple automated system for appetitive conditioning of zebrafish in their home tanks.

Behav Brain Res 2017 01 19;317:444-452. Epub 2016 Sep 19.

Department of Physiology & Biophysics, Dalhousie University, Halifax, NS B3H 4R2, Canada. Electronic address:

We describe here an automated apparatus that permits rapid conditioning paradigms for zebrafish. Arduino microprocessors were used to control the delivery of auditory or visual stimuli to groups of adult or juvenile zebrafish in their home tanks in a conventional zebrafish facility. An automatic feeder dispensed precise amounts of food immediately after the conditioned stimuli, or at variable delays for controls. Responses were recorded using inexpensive cameras, with the video sequences analysed with ImageJ or Matlab. Fish showed significant conditioned responses in as few as 5 trials, learning that the conditioned stimulus was a predictor of food presentation at the water surface and at the end of the tank where the food was dispensed. Memories of these conditioned associations persisted for at least 2days after training when fish were tested either as groups or as individuals. Control fish, for which the auditory or visual stimuli were specifically unpaired with food, showed no comparable responses. This simple, low-cost, automated system permits scalable conditioning of zebrafish with minimal human intervention, greatly reducing both variability and labour-intensiveness. It will be useful for studies of the neural basis of learning and memory, and for high-throughput screening of compounds modifying those processes.
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http://dx.doi.org/10.1016/j.bbr.2016.09.044DOI Listing
January 2017

Zebrafish heart as a model to study the integrative autonomic control of pacemaker function.

Am J Physiol Heart Circ Physiol 2016 09 24;311(3):H676-88. Epub 2016 Jun 24.

Department of Medical Neuroscience, Faculty of Medicine, Dalhousie University, Halifax, Nova Scotia, Canada; and

The cardiac pacemaker sets the heart's primary rate, with pacemaker discharge controlled by the autonomic nervous system through intracardiac ganglia. A fundamental issue in understanding the relationship between neural activity and cardiac chronotropy is the identification of neuronal populations that control pacemaker cells. To date, most studies of neurocardiac control have been done in mammalian species, where neurons are embedded in and distributed throughout the heart, so they are largely inaccessible for whole-organ, integrative studies. Here, we establish the isolated, innervated zebrafish heart as a novel alternative model for studies of autonomic control of heart rate. Stimulation of individual cardiac vagosympathetic nerve trunks evoked bradycardia (parasympathetic activation) and tachycardia (sympathetic activation). Simultaneous stimulation of both vagosympathetic nerve trunks evoked a summative effect. Effects of nerve stimulation were mimicked by direct application of cholinergic and adrenergic agents. Optical mapping of electrical activity confirmed the sinoatrial region as the site of origin of normal pacemaker activity and identified a secondary pacemaker in the atrioventricular region. Strong vagosympathetic nerve stimulation resulted in a shift in the origin of initial excitation from the sinoatrial pacemaker to the atrioventricular pacemaker. Putative pacemaker cells in the sinoatrial and atrioventricular regions expressed adrenergic β2 and cholinergic muscarinic type 2 receptors. Collectively, we have demonstrated that the zebrafish heart contains the accepted hallmarks of vertebrate cardiac control, establishing this preparation as a viable model for studies of integrative physiological control of cardiac function by intracardiac neurons.
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http://dx.doi.org/10.1152/ajpheart.00330.2016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5142188PMC
September 2016

Biomphalaria alexandrina as a bioindicator of metal toxicity.

Chemosphere 2016 Aug 19;157:97-106. Epub 2016 May 19.

Department of Physiology and Biophysics, Dalhousie University, Halifax, NS, Canada. Electronic address:

Heavy metals are common environmental pollutants to the aquatic ecosystems. Several aquatic species have been used as bioindicators and biomonitoring subjects for heavy metals pollution. In the present study, the effects of cadmium (Cd) and manganese (Mn) on the survival, attachment, locomotion, and feeding behaviours of the gastropod snail Biomphalaria alexandrina were determined. The short-term (96 h) LC50 for Cd and Mn were found to be 0.219 and 154.2 mg/l, respectively. Long-term exposures (16-20 days) to ascending concentrations of Cd (0.01-1 mg/l) and Mn (50-500 mg/l) also caused gradual decreases in the survival rate of B. alexandrina in a dose-dependent manner. Attachment, locomotion and feeding behaviours of snails exposed to lethal and sublethal concentrations of Cd and Mn at acute (96 h) and chronic exposure (24 days) intervals, respectively, were also recorded. Compared to controls, a significant decrease (p ≤ 0.05) was recorded in the different behaviours of exposed snails. These changes in behaviour would potentially impact the snail's ability to survive in the wild. Although Cd caused a more severe decline in snail survivorship than Mn, the behavioural effects of Mn were much more severe than Cd when the metals were roughly matched for lethality. In sum, the present study demonstrates B. alexandrina to be a sensitive bioindicator and model organism to assess heavy metals risk factors for severe toxicity in freshwater ecosystems.
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http://dx.doi.org/10.1016/j.chemosphere.2016.05.012DOI Listing
August 2016

Histamine Immunoreactive Elements in the Central and Peripheral Nervous Systems of the Snail, Biomphalaria spp., Intermediate Host for Schistosoma mansoni.

PLoS One 2015 18;10(6):e0129800. Epub 2015 Jun 18.

Department of Physiology and Biophysics, Dalhousie University, Halifax, Nova Scotia, Canada.

Histamine appears to be an important transmitter throughout the Animal Kingdom. Gastropods, in particular, have been used in numerous studies establishing potential roles for this biogenic amine in the nervous system and showing its involvement in the generation of diverse behaviours. And yet, the distribution of histamine has only previously been described in a small number of molluscan species. The present study examined the localization of histamine-like immunoreactivity in the central and peripheral nervous systems of pulmonate snails of the genus Biomphalaria. This investigation demonstrates immunoreactive cells throughout the buccal, cerebral, pedal, left parietal and visceral ganglia, indicative of diverse regulatory functions in Biomphalaria. Immunoreactivity was also present in statocyst hair cells, supporting a role for histamine in graviception. In the periphery, dense innervation by immunoreactive fibers was observed in the anterior foot, perioral zone, and other regions of the body wall. This study thus shows that histamine is an abundant transmitter in these snails and its distribution suggest involvement in numerous neural circuits. In addition to providing novel subjects for comparative studies of histaminegic neurons in gastropods, Biomphalaria is also the major intermediate host for the digenetic trematode parasite, which causes human schistosomiasis. The study therefore provides a foundation for understanding potential roles for histamine in interactions between the snail hosts and their trematode parasites.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0129800PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4472778PMC
April 2016

Morphology, innervation, and peripheral sensory cells of the siphon of aplysia californica.

J Comp Neurol 2015 Nov 12;523(16):2409-25. Epub 2015 May 12.

Department of Biology, St. Francis Xavier University, Antigonish, Nova Scotia, B2G 2W5, Canada.

The siphon of Aplysia californica has several functions, including involvement in respiration, excretion, and defensive inking. It also provides sensory input for defensive withdrawals that have been studied extensively to examine mechanisms that underlie learning. To better understand the neuronal bases of these functions, we used immunohistochemistry to catalogue peripheral cell types and innervation of the siphon in stage 12 juveniles (chosen to allow observation of tissues in whole-mounts). We found that the siphon nerve splits into three major branches, leading ultimately to a two-part FMRFamide-immunoreactive plexus and an apparently separate tyrosine hydroxylase-immunoreactive plexus. Putative sensory neurons included four distinct types of tubulin-immunoreactive bipolar cells (one likely also tyrosine hydroxylase immunoreactive) that bore ciliated dendrites penetrating the epithelium. A fifth bipolar neuron type (tubulin- and FMRFamide-immunoreactive) occurred deeper in the tissue, associated with part of the FMRFamide-immunoreactive plexus. Our observations emphasize the structural complexity of the peripheral nervous system of the siphon, and the importance of direct tests of the various components to better understand the functioning of the entire organ, including its role in defensive withdrawal responses.
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http://dx.doi.org/10.1002/cne.23795DOI Listing
November 2015

Intrinsic and extrinsic innervation of the heart in zebrafish (Danio rerio).

J Comp Neurol 2015 Aug 9;523(11):1683-700. Epub 2015 Apr 9.

Department of Medical Neuroscience, Faculty of Medicine, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada.

In the vertebrate heart the intracardiac nervous system is the final common pathway for autonomic control of cardiac output, but the neuroanatomy of this system is not well understood. In this study we investigated the innervation of the heart in a model vertebrate, the zebrafish. We used antibodies against acetylated tubulin, human neuronal protein C/D, choline acetyltransferase, tyrosine hydroxylase, neuronal nitric oxide synthase, and vasoactive intestinal polypeptide to visualize neural elements and their neurotransmitter content. Most neurons were located at the venous pole in a plexus around the sinoatrial valve; mean total number of cells was 197 ± 23, and 92% were choline acetyltransferase positive, implying a cholinergic role. The plexus contained cholinergic, adrenergic, and nitrergic axons and vasoactive intestinal polypeptide-positive terminals, some innervating somata. Putative pacemaker cells near the plexus showed immunoreactivity for hyperpolarization-activated cyclic nucleotide-gated channel 4 (HCN4) and the transcription factor Islet-1 (Isl1). The neurotracer neurobiotin showed that extrinsic axons from the left and right vagosympathetic trunks innervated the sinoatrial plexus proximal to their entry into the heart; some extrinsic axons from each trunk also projected into the medial dorsal plexus region. Extrinsic axons also innervated the atrial and ventricular walls. An extracardiac nerve trunk innervated the bulbus arteriosus and entered the arterial pole of the heart to innervate the proximal ventricle. We have shown that the intracardiac nervous system in the zebrafish is anatomically and neurochemically complex, providing a substrate for autonomic control of cardiac effectors in all chambers.
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http://dx.doi.org/10.1002/cne.23764DOI Listing
August 2015

The structure of the caudal wall of the zebrafish (Danio rerio) swim bladder: evidence of localized lamellar body secretion and a proximate neural plexus.

J Morphol 2014 Aug 19;275(8):933-48. Epub 2014 Mar 19.

Department of Medical Neuroscience, Dalhousie University, Halifax, Nova Scotia, Canada, B3H 4R2; Department of Biology, Saint Francis Xavier University, Antigonish, Nova Scotia, Canada, B2G 2W5.

In this study, we present a morphological description of the fine structure of the tissues composing the caudal tip of the adult zebrafish swim bladder and an immunochemical survey of the innervation at this site. The internal aspect of the caudal tip is lined by an epithelium specialized to secrete surfactant into the lumen as evinced by the exocytosis of lamellar bodies. The sole innervation to this region consists of a neural plexus, present on the external surface, of nitric oxide synthase-positive (nNOS) neuronal cell bodies that are contacted by axon terminals, some containing neuropeptide Y and vasoactive intestinal polypeptide. As the specialized epithelium and neural plexus are coincident and of common extent, we suggest that the morphological relationship between the two elements allows the nervous system to affect surfactant processing, possibly through a paracrine mechanism.
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http://dx.doi.org/10.1002/jmor.20274DOI Listing
August 2014

Emergence of sensory structures in the developing epidermis in sepia officinalis and other coleoid cephalopods.

J Comp Neurol 2014 Sep 8;522(13):3004-19. Epub 2014 Apr 8.

Museum National d'Histoire Naturelle (MNHN), DMPA, UMR Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), MNHN CNRS 7208, IRD 207, UPMC, CP51 75005, Paris, France; Université Pierre et Marie Curie-Paris, Paris, 6, France.

Embryonic cuttlefish can first respond to a variety of sensory stimuli during early development in the egg capsule. To examine the neural basis of this ability, we investigated the emergence of sensory structures within the developing epidermis. We show that the skin facing the outer environment (not the skin lining the mantle cavity, for example) is derived from embryonic domains expressing the Sepia officinalis ortholog of pax3/7, a gene involved in epidermis specification in vertebrates. On the head, they are confined to discrete brachial regions referred to as "arm pillars" that expand and cover Sof-pax3/7-negative head ectodermal tissues. As revealed by the expression of the S. officinalis ortholog of elav1, an early marker of neural differentiation, the olfactory organs first differentiate at about stage 16 within Sof-pax3/7-negative ectodermal regions before they are covered by the definitive Sof-pax3/7-positive outer epithelium. In contrast, the eight mechanosensory lateral lines running over the head surface and the numerous other putative sensory cells in the epidermis, differentiate in the Sof-pax3/7-positive tissues at stages ∼24-25, after they have extended over the entire outer surfaces of the head and arms. Locations and morphologies of the various sensory cells in the olfactory organs and skin were examined using antibodies against acetylated tubulin during the development of S. officinalis and were compared with those in hatchlings of two other cephalopod species. The early differentiation of olfactory structures and the peculiar development of the epidermis with its sensory cells provide new perspectives for comparisons of developmental processes among molluscs.
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http://dx.doi.org/10.1002/cne.23562DOI Listing
September 2014

Localization of tyrosine hydroxylase-like immunoreactivity in the nervous systems of Biomphalaria glabrata and Biomphalaria alexandrina, intermediate hosts for schistosomiasis.

J Comp Neurol 2014 Aug 4;522(11):2532-52. Epub 2014 Apr 4.

Institute of Neurobiology and Department of Anatomy & Neurobiology, University of Puerto Rico, Medical Sciences Campus, San Juan, Puerto Rico, 00901.

Planorbid snails of the genus Biomphalaria are major intermediate hosts for the digenetic trematode parasite Schistosoma mansoni. Evidence suggests that levels of the neurotransmitter dopamine (DA) are reduced during the course of S. mansoni multiplication and transformation within the snail. This investigation used immunohistochemical methods to localize tyrosine hydroxylase (TH), the rate-limiting enzyme in the biosynthesis of catecholamines, in the nervous system of Biomphalaria. The two species examined, Biomphalaria glabrata and Biomphalaria alexandrina, are the major intermediate hosts for S. mansoni in sub-Saharan Africa, where more than 90% of global cases of human intestinal schistosomiasis occur. TH-like immunoreactive (THli) neurons were distributed throughout the central nervous system (CNS) and labeled fibers were present in all commissures, connectives, and nerves. Some asymmetries were observed, including a large distinctive neuron (LPeD1) in the pedal ganglion described previously in several pulmonates. The majority of TH-like immunoreactive neurons were detected in the peripheral nervous system (PNS), especially in lip and foot regions of the anterior integument. Independent observations supporting the dopaminergic phenotype of THli neurons included 1) block of LPeD1 synaptic signaling by the D2/3 antagonist sulpiride, and 2) the similar localization of aqueous aldehyde (FaGlu)-induced fluorescence. The distribution of THli neurons indicates that, as in other gastropods, dopamine functions as a sensory neurotransmitter and in the regulation of feeding and reproductive behaviors in Biomphalaria. It is hypothesized that infection could stimulate transmitter release from dopaminergic sensory neurons and that dopaminergic signaling could contribute to modifications of both host and parasite behavior.
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http://dx.doi.org/10.1002/cne.23548DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4043854PMC
August 2014

Regional innervation of the heart in the goldfish, Carassius auratus: a confocal microscopy study.

J Comp Neurol 2014 Feb;522(2):456-78

Department of Medical Neuroscience, Dalhousie University, Halifax, Nova Scotia, B3H 4R2, Canada.

The intracardiac nervous system represents the final common pathway for autonomic control of the vertebrate heart in maintaining cardiovascular homeostasis. In teleost fishes, details of the organization of this system are not well understood. Here we investigated innervation patterns in the heart of the goldfish, a species representative of a large group of cyprinids. We used antibodies against the neuronal markers zn-12, acetylated tubulin, and human neuronal protein C/D, as well as choline acetyltransferase, tyrosine hydroxylase, nitric oxide synthetase, and vasoactive intestinal polypeptide (VIP) to detect neural elements and their transmitter contents in wholemounts and sections of cardiac tissue. All chambers of the heart were innervated by choline acetyltransferase-positive axons, implying cholinergic regulation; and by tyrosine hydroxylase-containing axons, implying adrenergic regulation. The mean total number of intracardiac neurons was 713 ± 78 (SE), nearly half of which were cholinergic. Neuronal somata were mainly located in a ganglionated plexus around the sinoatrial valves. Somata were contacted by cholinergic, adrenergic, nitrergic, and VIP-positive terminals. Putative pacemaker cells, identified by immunoreactivity for hyperpolarization activated, cyclic nucleotide-gated channel 4, were located in the base of the sinoatrial valves, and this region was densely innervated by cholinergic and adrenergic terminals. We have shown that the goldfish heart possesses the necessary neuroanatomical substrate for fine, region-by-region autonomic control of the myocardial effectors that are involved in determining cardiac output.
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http://dx.doi.org/10.1002/cne.23421DOI Listing
February 2014