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Zheng, Da‐Jiang; Okobi, Daniel E.; Shu, Ryan; Agrawal, Rania; Smith, Samantha K.; Long, Michael A.; Phelps, Steven M.
doi: 10.1002/cne.25321pmid: 35385140
Vocalizations are often elaborate, rhythmically structured behaviors. Vocal motor patterns require close coordination of neural circuits governing the muscles of the larynx, jaw, and respiratory system. In the elaborate vocalization of Alston's singing mouse (Scotinomys teguina) each note of its rapid, frequency‐modulated trill is accompanied by equally rapid modulation of breath and gape. To elucidate the neural circuitry underlying this behavior, we introduced the polysynaptic retrograde neuronal tracer pseudorabies virus (PRV) into the cricothyroid and digastricus muscles, which control frequency modulation and jaw opening, respectively. Each virus singly labels ipsilateral motoneurons (nucleus ambiguus for cricothyroid, and motor trigeminal nucleus for digastricus). We find that the two isogenic viruses heavily and bilaterally colabel neurons in the gigantocellular reticular formation, a putative central pattern generator. The viruses also show strong colabeling in compartments of the midbrain including the ventrolateral periaqueductal gray and the parabrachial nucleus, two structures strongly implicated in vocalizations. In the forebrain, regions important to social cognition and energy balance both exhibit extensive colabeling. This includes the paraventricular and arcuate nuclei of the hypothalamus, the lateral hypothalamus, preoptic area, extended amygdala, central amygdala, and the bed nucleus of the stria terminalis. Finally, we find doubly labeled neurons in M1 motor cortex previously described as laryngeal, as well as in the prelimbic cortex, which indicate these cortical regions play a role in vocal production. The progress of both viruses is broadly consistent with vertebrate‐general patterns of vocal circuitry, as well as with circuit models derived from primate literature.
Kraus, Kimberly L.; Chordia, Arihant P.; Drake, Austin W.; Herman, James P.; Danzer, Steve C.
doi: 10.1002/cne.25322pmid: 35397117
The hippocampus has become a significant target of stress research in recent years because of its role in cognitive functioning, neuropathology, and regulation of the hypothalamic–pituitary–adrenal (HPA) axis. Despite the pervasive impact of stress on psychiatric and neurological disease, many of the circuit‐ and cell‐dependent mechanisms giving rise to the limbic regulation of the stress response remain unknown. Hippocampal excitatory neurons generally express high levels of glucocorticoid receptors (GRs) and are therefore positioned to respond directly to serum glucocorticoids. These neurons are, in turn, regulated by neighboring interneurons, subtypes of which have been shown to respond to stress exposure. However, GR expression among hippocampal interneurons is not well characterized. To determine whether key interneuron populations are direct targets for glucocorticoid action, we used two transgenic mouse lines to label parvalbumin‐positive (PV+) and somatostatin‐positive (SST+) interneurons. GR immunostaining of labeled interneurons was characterized within the dorsal and ventral dentate hilus, dentate cell body layer, and CA1 and CA3 stratum oriens and stratum pyramidale. While nearly all hippocampal SST+ interneurons expressed GR across all regions, GR labeling of PV+ interneurons showed considerable subregion variability. The percentage of PV+, GR+ cells was highest in the CA3 stratum pyramidale and lowest in the CA1 stratum oriens, with other regions showing intermediate levels of expression. Together, these findings indicate that, under baseline conditions, hippocampal SST+ interneurons are a ubiquitous glucocorticoid target, while only distinct populations of PV+ interneurons are direct targets. This anatomical diversity suggests functional differences in the regulation of stress‐dependent hippocampal responses.
Sarko, Diana K.; Reep, Roger L.
doi: 10.1002/cne.25323pmid: 35434802
Florida manatees (Trichechus manatus latirostris) and rock hyraxes (Procavia capensis) exhibit expanded tactile arrays of vibrissae that are distributed not only on the face but also on the entire postfacial body. In contrast, the vibrissae of most mammals are principally restricted to the face. These facial vibrissae may be associated with central nervous system representations known as barrels in the cerebral cortex, barreloids in the thalamus, and barrelettes in the trigeminal nuclei of the brainstem. To date, vibrissae representations found within the brainstem have been principally limited to facial vibrissae representations in the trigeminal nuclei. We hypothesized that the tactile specializations of the manatee and rock hyrax would produce a unique modification of typical mammalian central nervous system organization, with postfacial vibrissae representations appearing in the cuneate and gracile nuclei as “body barrelettes.” Using histological and histochemical methods, including cresyl violet, myelin, and cytochrome oxidase processing, we first delineated the rostral, middle, and caudal zones of the cuneate and gracile nuclei. Within the middle zone, divisions were present, including extensive parcellation in the cluster region, particularly in manatees. These clusters were particularly densely distributed and distinguishable in the presumptive postfacial body representations in the cuneate and gracile nuclei but otherwise shared many attributes with the barrelettes found in the trigeminal nuclei of other species. This study represents the first characterization of postfacial body vibrissae representations, or “body barrelettes,” in the brainstem of any species. Previous studies have predominantly focused on facial vibrissae representations, which have served for decades as a model for sensory organization and plasticity. Our results extend what is known about vibrissae representations in the central nervous system to include expansions related to peripheral specializations of the postfacial body. Unusual somatosensory adaptations in the manatee and rock hyrax are highly informative regarding how mammalian brain organization responds to evolutionary pressures on sensory systems.
Yi, Wenjing; Mueller, Thomas; Rücklin, Martin; Richardson, Michael K.
doi: 10.1002/cne.25324pmid: 35470436
Bitterlings are carp‐like teleost fish (Cypriniformes: Acheilanathidae) known for their specialized brood parasitic lifestyle. Bitterling embryos, in fact, develop inside the gill chamber of their freshwater mussel hosts. However, little is known about how their parasitic lifestyle affects brain development in comparison to nonparasitic species. Here, we document the development of the brain of the rosy bitterling, Rhodeus ocellatus, at four embryonic stages of 165, 185, 210, 235 hours postfertilization (hpf) using micro‐computed tomography (microCT). Focusing on developmental regionalization and brain ventricular organization, we relate the development of the brain divisions to those described for zebrafish using the prosomeric model as a reference paradigm. Segmentation and three‐dimensional visualization of the ventricular system allowed us to identify changes in the longitudinal brain axis as a result of cephalic flexure during development. The results show that during early embryonic and larval development, histological differentiation, tissue boundaries, periventricular proliferation zones, and ventricular spaces are all detectable by microCT. The results of this study visualized with differential CT profiles are broadly consistent with comparable histological studies, and with the genoarchitecture of teleosts like the zebrafish. Compared to the zebrafish, our study identifies distinct developmental heterochronies in the rosy bitterling, such as a precocious development of the inferior lobe.
Kowal, Tia J.; Dhande, Onkar S.; Wang, Biao; Wang, Qing; Ning, Ke; Liu, Wendy; Berbari, Nicolas F.; Hu, Yang; Sun, Yang
doi: 10.1002/cne.25326pmid: 35434813
Loss of retinal ganglion cells (RGCs) underlies several forms of retinal disease including glaucomatous optic neuropathy, a leading cause of irreversible blindness. Several rare genetic disorders associated with cilia dysfunction have retinal degeneration as a clinical hallmark. Much of the focus of ciliopathy associated blindness is on the connecting cilium of photoreceptors; however, RGCs also possess primary cilia. It is unclear what roles RGC cilia play, what proteins and signaling machinery localize to RGC cilia, or how RGC cilia are differentiated across the subtypes of RGCs. To better understand these questions, we assessed the presence or absence of a prototypical cilia marker Arl13b and a widely distributed neuronal cilia marker AC3 in different subtypes of mouse RGCs. Interestingly, not all RGC subtype cilia are the same and there are significant differences even among these standard cilia markers. Alpha‐RGCs positive for osteopontin, calretinin, and SMI32 primarily possess AC3‐positive cilia. Directionally selective RGCs that are CART positive or Trhr positive localize either Arl13b or AC3, respectively, in cilia. Intrinsically photosensitive RGCs differentially localize Arl13b and AC3 based on melanopsin expression. Taken together, we characterized the localization of gold standard cilia markers in different subtypes of RGCs and conclude that cilia within RGC subtypes may be differentially organized. Future studies aimed at understanding RGC cilia function will require a fundamental ability to observe the cilia across subtypes as their signaling protein composition is elucidated. A comprehensive understanding of RGC cilia may reveal opportunities to understanding how their dysfunction leads to retinal degeneration.
Thittamranahalli Kariyappa, Jyothi; Zanoni, Simone; Bongers, Andre; Tong, Lydia; Ashwell, Ken W. S.
doi: 10.1002/cne.25328pmid: 35417062
The diversity of the diprotodontids provides an excellent opportunity to study how a basic marsupial cortical plan has been modified for the needs of the mammals living in different habitats. Very little is known about the connections of the cerebral cortex with the deep brain structures (basal ganglia and thalamus) in this evolutionarily significant group of mammals. In this study, we performed mapping of brain regions and connections in a diprotodontid marsupial from data obtained from an excised brain scanned in high‐field (9.4 T) microstructural magnetic resonance imaging (MRI) instrument. The analysis was based on two MRI methodologies. First, high‐resolution structural scans were used to map MRI visible brain regions from T1w and T2w images. Second, extensive diffusion tensor imaging (DTI) data were obtained to elucidate connectivity between brain areas using deterministic diffusion tracking of neuronal brain fibers. From the data, we were able to identify corticostriate connections between the frontal association and dorsomedial isocortex and the head of the caudate, and between the lateral somatosensory cortex and the putamen. We were also able to follow the olfactory and limbic connections by tracing fibers in the fornix, cingulum, intrabulbar part of the anterior commissure, and lateral olfactory tract. There was segregation of fibers in the anterior commissure such that olfactory connections passed through the rostroventral part and successively more dorsal cortical areas connected through more dorsal parts of the commissure. Our findings confirm a common pattern of cortical connectivity in therian mammals, even where brain expansion has occurred independently in diverse groups.
Vitorino, Marta; Simão, Sónia; Moreira, João B.; Nogueira‐Rodrigues, Joana; Silva, Joana; Lourenço, Ana Sofia; Fernandes, Vítor; Sousa, Monica M.; Tiscornia, Gustavo; Araújo, Inês M.
doi: 10.1002/cne.25329pmid:
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The African spiny mouse (Acomys cahirinus) is an emerging model of mammalian epimorphic regeneration that has aroused the interest of the scientific community in the last decade. To date, studies on brain repair have been hindered by the lack of knowledge on the neuroanatomy of this species. Here, we present a coronal brain atlas in stereotaxic coordinates, which allows for three‐dimensional identification and localization of the brain structures of this species. The brain of 12‐week‐old spiny mice was mapped in stereotaxic coordinates using cresyl violet‐stained brain sections obtained from coronal cryosectioning of the brain after transcardial perfusion with fixative. The atlas is presented in 42 plates representing sections spaced 240 μm apart. Stereotaxic coordinates were validated using both a model of Parkinsonian lesion of the striatum with 6‐hydroxydopamine and labeling of the corticospinal tract in the spiny mouse spinal cord using AAV1/2‐GFP intracortical injections. This work presents a new tool in A. cahirinus neurobiology and opens new avenues of research for the investigation of the regenerative ability of A. cahirinus in models of brain disorders.