Neuropeptide expression and action in the reproductive system of the starfish Asterias rubensPiñon Gonzalez, Victor M.; Feng, Yuling; Egertová, Michaela; Elphick, Maurice R.
doi: 10.1002/cne.25585pmid: 38289190
Reproductive processes are regulated by a variety of neuropeptides in vertebrates and invertebrates. In starfish (phylum Echinodermata), relaxin‐like gonad‐stimulating peptide triggers oocyte maturation and spawning. However, little is known about other neuropeptides as potential regulators of reproduction in starfish. To address this issue, here, we used histology and immunohistochemistry to analyze the reproductive system of the starfish Asterias rubens at four stages of the seasonal reproductive cycle in male and female animals, investigating the expression of eight neuropeptides: the corticotropin‐releasing hormone‐type neuropeptide ArCRH, the calcitonin‐type neuropeptide ArCT, the pedal peptide‐type neuropeptides ArPPLN1b and ArPPLN2h, the vasopressin/ocytocin‐type neuropeptide asterotocin, the gonadotropin‐releasing hormone‐type neuropeptide ArGnRH, and the somatostatin/allatostatin‐C‐type neuropeptides ArSS1 and ArSS2. The expression of five neuropeptides, ArCRH, ArCT, ArPPLN1b, ArPPLN2h, and asterotocin, was detected in the gonoducts and/or gonads. For example, extensive ArPPLN2h expression was revealed in the coelomic epithelial layer of the gonads throughout the seasonal reproductive cycle in both males and females. However, seasonal and/or sexual differences in the patterns of neuropeptide expression were also observed. Informed by these findings, the in vitro pharmacological effects of neuropeptides on gonad preparations from male and female starfish were investigated. This revealed that ArSS1 causes gonadal contraction and that ArPPLN2h causes gonadal relaxation, with both neuropeptides being more effective on ovaries than testes. Collectively, these findings indicate that multiple neuropeptide signaling systems are involved in the regulation of reproductive function in starfish, with some neuropeptides exerting excitatory or inhibitory effects on gonad contractility that may be physiologically relevant when gametes are expelled during spawning.
Fetal development of the human amygdalaMulc, Damir; Smilović, Dinko; Krsnik, Željka; Junaković‐Munjas, Alisa; Kopić, Janja; Kostović, Ivica; Šimić, Goran; Vukšić, Mario
doi: 10.1002/cne.25580pmid: 38289194
The intricate development of the human amygdala involves a complex interplay of diverse processes, varying in speed and duration. In humans, transient cytoarchitectural structures deliquesce, leading to the formation of functionally distinct nuclei as a result of multiple interdependent developmental events. This study compares the amygdala's cytoarchitectural development in conjunction with specific antibody reactivity for neuronal, glial, neuropil, and radial glial fibers, synaptic, extracellular matrix, and myelin components in 39 fetal human brains. We recognized that the early fetal period, as a continuation of the embryonic period, is still dominated by relatively uniform histogenetic processes. The typical appearance of ovoid cell clusters in the lateral nucleus during midfetal period is most likely associated with the cell migration and axonal growth processes in the developing human brain. Notably, synaptic markers are firstly detected in the corticomedial group of nuclei, while immunoreactivity for the panaxonal neurofilament marker SMI 312 is found dorsally. The late fetal period is characterized by a protracted migration process evidenced by the presence of doublecortin and SOX‐2 immunoreactivity ventrally, in the prospective paralaminar nucleus, reinforced by vimentin immunoreactivity in the last remaining radial glial fibers. Nearing the term period, SMI 99 immunoreactivity indicates that perinatal myelination becomes prominent primarily along major axonal pathways, laying the foundation for more pronounced functional maturation. This study comprehensively elucidates the rate and sequence of maturational events in the amygdala, highlighting the key role of prenatal development in its behavioral, autonomic, and endocrine regulation, with subsequent implications for both normal functioning and psychiatric disorders.
Comparative analyses of the Smith−Magenis syndrome protein RAI1 in mice and common marmoset monkeysChang, Ya‐Ting; Lee, Yu‐Ju; Haque, Minza; Chang, Hao‐Cheng; Javed, Sehrish; Lin, Yu Cheng; Cho, Yoobin; Abramovitz, Joseph; Chin, Gabriella; Khamis, Asma; Raja, Reesha; Murai, Keith K.; Huang, Wei‐Hsiang
doi: 10.1002/cne.25589pmid: 38289192
Retinoic acid‐induced 1 (RAI1) encodes a transcriptional regulator critical for brain development and function. RAI1 haploinsufficiency in humans causes a syndromic autism spectrum disorder known as Smith−Magenis syndrome (SMS). The neuroanatomical distribution of RAI1 has not been quantitatively analyzed during the development of the prefrontal cortex, a brain region critical for cognitive function and social behaviors and commonly implicated in autism spectrum disorders, including SMS. Here, we performed comparative analyses to uncover the evolutionarily convergent and divergent expression profiles of RAI1 in major cell types during prefrontal cortex maturation in common marmoset monkeys (Callithrix jacchus) and mice (Mus musculus). We found that while RAI1 in both species is enriched in neurons, the percentage of excitatory neurons that express RAI1 is higher in newborn mice than in newborn marmosets. By contrast, RAI1 shows similar neural distribution in adult marmosets and adult mice. In marmosets, RAI1 is expressed in several primate‐specific cell types, including intralaminar astrocytes and MEIS2‐expressing prefrontal GABAergic neurons. At the molecular level, we discovered that RAI1 forms a protein complex with transcription factor 20 (TCF20), PHD finger protein 14 (PHF14), and high mobility group 20A (HMG20A) in the marmoset brain. In vitro assays in human cells revealed that TCF20 regulates RAI1 protein abundance. This work demonstrates that RAI1 expression and protein interactions are largely conserved but with some unique expression in primate‐specific cells. The results also suggest that altered RAI1 abundance could contribute to disease features in disorders caused by TCF20 dosage imbalance.
The motor apparatus of head movements in the Oleander hawkmoth (Daphnis nerii, Lepidoptera)Prusty, Agnish D.; Sane, Sanjay P.
doi: 10.1002/cne.25577pmid: 38289189
Head movements of insects play a vital role in diverse locomotory behaviors including flying and walking. Because insect eyes move minimally within their sockets, their head movements are essential to reduce visual blur and maintain a stable gaze. As in most vertebrates, gaze stabilization behavior in insects requires the integration of both visual and mechanosensory feedback by the neck motor neurons. Although visual feedback is derived from the optic flow over the retina of their compound eyes, mechanosensory feedback is derived from their organs of balance, similar to the vestibular system in vertebrates. In Diptera, vestibular feedback is derived from the halteres—modified hindwings that evolved into mechanosensory organs—and is integrated with visual feedback to actuate compensatory head movements. However, non‐Dipteran insects, including Lepidoptera, lack halteres. In these insects, vestibular feedback is obtained from the antennal Johnston's organs but it is not well‐understood how it integrates with visual feedback during head movements. Indeed, although head movements are well‐studied in flies, the underlying motor apparatus in non‐Dipteran taxa has received relatively less attention. As a first step toward understanding compensatory head movements in the Oleander hawkmoth Daphnis nerii, we image the anatomy and architecture of their neck joint sclerites and muscles using X‐ray microtomography, and the associated motor neurons using fluorescent dye fills and confocal microscopy. Based on these morphological data, we propose testable hypotheses about the putative function of specific neck muscles during head movements, which can shed light on their role in neck movements and gaze stabilization.
Using tissue clearing and light sheet fluorescence microscopy for the three‐dimensional analysis of sensory and sympathetic nerve endings that innervate bone and dental tissue of miceThai, Jenny; Fuller‐Jackson, John‐Paul; Ivanusic, Jason J.
doi: 10.1002/cne.25582pmid: 38289188
Bone and dental tissues are richly innervated by sensory and sympathetic neurons. However, the characterization of the morphology, molecular phenotype, and distribution of nerves that innervate hard tissue has so far mostly been limited to thin histological sections. This approach does not adequately capture dispersed neuronal projections due to the loss of important structural information during three‐dimensional (3D) reconstruction. In this study, we modified the immunolabeling‐enabled imaging of solvent‐cleared organs (iDISCO/iDISCO+) clearing protocol to image high‐resolution neuronal structures in whole femurs and mandibles collected from perfused C57Bl/6 mice. Axons and their nerve terminal endings were immunolabeled with antibodies directed against protein gene product 9.5 (pan‐neuronal marker), calcitonin gene–related peptide (peptidergic nociceptor marker), or tyrosine hydroxylase (sympathetic neuron marker). Volume imaging was performed using light sheet fluorescence microscopy. We report high‐quality immunolabeling of the axons and nerve terminal endings for both sensory and sympathetic neurons that innervate the mouse femur and mandible. Importantly, we are able to follow their projections through full 3D volumes, highlight how extensive their distribution is, and show regional differences in innervation patterns for different parts of each bone (and surrounding tissues). Mapping the distribution of sensory and sympathetic axons, and their nerve terminal endings, in different bony compartments may be important in further elucidating their roles in health and disease.
Neural connections of the torus semicircularis in the adult ZebrafishYáñez, Julián; Eguiguren, Maider Hernández; Anadón, Ramón
doi: 10.1002/cne.25586pmid: 38289191
The torus semicircularis (TS) of teleosts is a key midbrain center of the lateral line and acoustic sensory systems. To characterize the TS in adult zebrafish, we studied their connections using the carbocyanine tracers applied to the TS and to other related nuclei and tracts. Two main TS nuclei, central and ventrolateral, were differentiable by their afferent connections. From central TS, (TSc) numerous toropetal cells were labeled bilaterally in several primary octaval nuclei (anterior, magnocellular, descending, and posterior octaval nuclei), in the secondary octaval nucleus, in the caudal octavolateralis nucleus, and in the perilemniscular region. In the midbrain, numerous toropetal cells were labeled in the contralateral TSc. In the diencephalon, toropetal cells labeled from the TSc were observed ipsilaterally in the medial prethalamic nucleus and the periventricular posterior tubercle nucleus. TSc toropetal neurons were also labeled bilaterally in the hypothalamic anterior tuberal nucleus (ATN) and ipsilaterally in the parvicellular preoptic nucleus but not in the telencephalon. Tracer application to the medial octavolateralis nucleus revealed contralateral projections to the ventrolateral TS (TSvl), whereas tracer application to the secondary octaval nucleus labeled fibers bilaterally in TSc and neurons in rostral TSc. The TSc sends ascending fibers to the ipsilateral lateral preglomerular region that, in turn, projects to the pallium. Application of DiI to the optic tectum labeled cells and fibers in the TSvl, whereas application of DiI to the ATN labeled cells and fibers in the TSc. These results reveal that the TSvl and TSc are mainly related with the mechanosensory lateral line and acoustic centers, respectively, and that they show different higher order connections.
Betz cells of the primary motor cortexNolan, Matthew; Scott, Connor; Hof, Patrick. R.; Ansorge, Olaf
doi: 10.1002/cne.25567pmid: 38289193
Betz cells, named in honor of Volodymyr Betz (1834–1894), who described them as “giant pyramids” in the primary motor cortex of primates and other mammalian species, are layer V extratelencephalic projection (ETP) neurons that directly innervate α‐motoneurons of the brainstem and spinal cord. Despite their large volume and circumferential dendritic architecture, to date, no single molecular criterion has been established that unequivocally distinguishes adult Betz cells from other layer V ETP neurons. In primates, transcriptional signatures suggest the presence of at least two ETP neuron clusters that contain mature Betz cells; these are characterized by an abundance of axon guidance and oxidative phosphorylation transcripts. How neurodevelopmental programs drive the distinct positional and morphological features of Betz cells in humans remains unknown. Betz cells display a distinct biphasic firing pattern involving early cessation of firing followed by delayed sustained acceleration in spike frequency and magnitude. Few cell type‐specific transcripts and electrophysiological characteristics are conserved between rodent layer V ETP neurons of the motor cortex and primate Betz cells. This has implications for the modeling of disorders that affect the motor cortex in humans, such as amyotrophic lateral sclerosis (ALS). Perhaps vulnerability to ALS is linked to the evolution of neural networks for fine motor control reflected in the distinct morphomolecular architecture of the human motor cortex, including Betz cells. Here, we discuss histological, molecular, and functional data concerning the position of Betz cells in the emerging taxonomy of neurons across diverse species and their role in neurological disorders.
Cognitive archaeology, and the psychological assessment of extinct mindsBruner, Emiliano
doi: 10.1002/cne.25583pmid: 38289186
Evolutionary anthropology relies on both neontological and paleontological information. In the latter case, fields such as paleoneurology, neuroarchaeology, and cognitive archaeology are supplying new perspectives in prehistory and neuroscience. Cognitive archaeology, in particular, investigates the behaviors associated with extinct species or cultures according to specific psychological models. For example, changes in working memory, attention, or visuospatial integration can be postulated when related behavioral changes are described in the archaeological record. However, cognition is a process based on different and partially independent functional elements, and extinct species could hence have evolved distinct combinations of cognitive abilities or features, based on both quantitative and qualitative differences. Accordingly, differences in working memory can lead to more conceptual or more holistic mindsets, with important changes in the perception and management of the mental experience. The parietal cortex is particularly interesting, in this sense, being involved in functions associated with body–tool integration, attention, and visual imaging. In some cases, evolutionary mismatches among these elements can induce drawbacks that, despite their positive effects on natural selection, can introduce important constraints in our own mental skills. Beyond the theoretical background, some hypotheses can be tested following methods in experimental psychology. In any case, theories in cognitive evolution must acknowledge that, beyond the brain and its biology, the human mind is also deeply rooted in body perception, in social networks, and in technological extension.
Single axonal characterization of trigeminocerebellar projection patterns in the mouseWang, Tianzhuo; Numata, Naoyuki; Ji, Qing; Mizuno, Yuma; Viet, Nguyen‐Minh; Luo, Yuanjun; Chao, Yuhan; Panezai, Saddam Khan; Sugihara, Izumi
doi: 10.1002/cne.25581pmid: 38289187
The cerebellar projection from the trigeminal nuclear complex is one of the major populations of the cerebellar inputs. Although this projection is essential in cerebellar functional processing and organization, its morphological organization has not been systematically clarified. The present study addressed this issue by lobule‐specific retrograde neuronal labeling and single axonal reconstruction with anterograde labeling. The cerebellar projection arose mainly from the interpolaris subdivision of the spinal trigeminal nucleus (Sp5I) and the principal trigeminal sensory nucleus (Pr5). Although crus II, paramedian lobule, lobule IX, and simple lobule were the major targets, paraflocculus, and other lobules received some projections. Reconstructed single trigeminocerebellar axons showed 77.8 mossy fiber terminals on average often in multiple lobules but no nuclear collaterals. More terminals were located in zebrin‐negative or lightly‐positive compartments than in zebrin‐positive compartments. While Pr5 axons predominantly projected to ipsilateral crus II, Sp5I axons projected either predominantly to crus II and paramedian lobule often bilaterally, or predominantly to lobule IX always ipsilaterally. Lobule IX‐predominant‐type Sp5I neurons specifically expressed Gpr26. Gpr26‐tagged neuronal labeling produced a peculiar mossy fiber distribution, which was dense in the dorsolateral lobule IX and extending transversely to the dorsal median apex in lobule IX. The projection to the cerebellar nuclei was observed in collaterals of ascending Sp5I axons that project to the diencephalon. In sum, multiple populations of trigeminocerebellar projections showed divergent projections to cerebellar lobules. The projection was generally complementary with the pontine projection and partly matched with the reported orofacial receptive field arrangement.