Catecholaminergic connectivity to the inner ear, central auditory, and vocal motor circuitry in the plainfin midshipman fish porichthys notatusForlano, Paul M.; Kim, Spencer D.; Krzyminska, Zuzanna M.; Sisneros, Joseph A.
doi: 10.1002/cne.23638pmid: N/A
Although the neuroanatomical distribution of catecholaminergic (CA) neurons has been well documented across all vertebrate classes, few studies have examined CA connectivity to physiologically and anatomically identified neural circuitry that controls behavior. The goal of this study was to characterize CA distribution in the brain and inner ear of the plainfin midshipman fish (Porichthys notatus) with particular emphasis on their relationship with anatomically labeled circuitry that both produces and encodes social acoustic signals in this species. Neurobiotin labeling of the main auditory end organ, the saccule, combined with tyrosine hydroxylase immunofluorescence (TH‐ir) revealed a strong CA innervation of both the peripheral and central auditory system. Diencephalic TH‐ir neurons in the periventricular posterior tuberculum, known to be dopaminergic, send ascending projections to the ventral telencephalon and prominent descending projections to vocal–acoustic integration sites, notably the hindbrain octavolateralis efferent nucleus, as well as onto the base of hair cells in the saccule via nerve VIII. Neurobiotin backfills of the vocal nerve in combination with TH‐ir revealed CA terminals on all components of the vocal pattern generator, which appears to largely originate from local TH‐ir neurons but may include input from diencephalic projections as well. This study provides strong neuroanatomical evidence that catecholamines are important modulators of both auditory and vocal circuitry and acoustic‐driven social behavior in midshipman fish. This demonstration of TH‐ir terminals in the main end organ of hearing in a nonmammalian vertebrate suggests a conserved and important anatomical and functional role for dopamine in normal audition. J. Comp. Neurol. 522:2887‐2927, 2014. © 2014 Wiley Periodicals, Inc.
Catecholaminergic connectivity to the inner ear, central auditory, and vocal motor circuitry in the plainfin midshipman fish porichthys notatusForlano, Paul M.; Kim, Spencer D.; Krzyminska, Zuzanna M.; Sisneros, Joseph A.
doi: 10.1002/cne.23596pmid: 24715479
Although the neuroanatomical distribution of catecholaminergic (CA) neurons has been well documented across all vertebrate classes, few studies have examined CA connectivity to physiologically and anatomically identified neural circuitry that controls behavior. The goal of this study was to characterize CA distribution in the brain and inner ear of the plainfin midshipman fish (Porichthys notatus) with particular emphasis on their relationship with anatomically labeled circuitry that both produces and encodes social acoustic signals in this species. Neurobiotin labeling of the main auditory end organ, the saccule, combined with tyrosine hydroxylase immunofluorescence (TH‐ir) revealed a strong CA innervation of both the peripheral and central auditory system. Diencephalic TH‐ir neurons in the periventricular posterior tuberculum, known to be dopaminergic, send ascending projections to the ventral telencephalon and prominent descending projections to vocal–acoustic integration sites, notably the hindbrain octavolateralis efferent nucleus, as well as onto the base of hair cells in the saccule via nerve VIII. Neurobiotin backfills of the vocal nerve in combination with TH‐ir revealed CA terminals on all components of the vocal pattern generator, which appears to largely originate from local TH‐ir neurons but may include input from diencephalic projections as well. This study provides strong neuroanatomical evidence that catecholamines are important modulators of both auditory and vocal circuitry and acoustic‐driven social behavior in midshipman fish. This demonstration of TH‐ir terminals in the main end organ of hearing in a nonmammalian vertebrate suggests a conserved and important anatomical and functional role for dopamine in normal audition. J. Comp. Neurol. 522:2887‐2927, 2014. © 2014 Wiley Periodicals, Inc.
Adenosine triphosphate‐induced photoreceptor death and retinal remodeling in ratsVessey, Kirstan A.; Greferath, Ursula; Aplin, Felix P.; Jobling, Andrew I.; Phipps, Joanna A.; Ho, Tracy; De Iongh, Robbert U.; Fletcher, Erica L.
doi: 10.1002/cne.23558pmid: 24639102
Many common causes of blindness involve the death of retinal photoreceptors, followed by progressive inner retinal cell remodeling. For an inducible model of retinal degeneration to be useful, it must recapitulate these changes. Intravitreal administration of adenosine triphosphate (ATP) has recently been found to induce acute photoreceptor death. The aim of this study was to characterize the chronic effects of ATP on retinal integrity. Five‐week‐old, dark agouti rats were administered 50 mM ATP into the vitreous of one eye and saline into the other. Vision was assessed using the electroretinogram and optokinetic response and retinal morphology investigated via histology. ATP caused significant loss of visual function within 1 day and loss of 50% of the photoreceptors within 1 week. At 3 months, 80% of photoreceptor nuclei were lost, and total photoreceptor loss occurred by 6 months. The degeneration and remodeling were similar to those found in heritable retinal dystrophies and age‐related macular degeneration and included inner retinal neuronal loss, migration, and formation of new synapses; Müller cell gliosis, migration, and scarring; blood vessel loss; and retinal pigment epithelium migration. In addition, extreme degeneration and remodeling events, such as neuronal and glial migration outside the neural retina and proliferative changes in glial cells, were observed. These extreme changes were also observed in the 2‐year‐old P23H rhodopsin transgenic rat model of retinitis pigmentosa. This ATP‐induced model of retinal degeneration may provide a valuable tool for developing pharmaceutical therapies or for testing electronic implants aimed at restoring vision. J. Comp. Neurol. 522:2928–2950, 2014. © 2014 Wiley Periodicals, Inc.
The cholinergic system in the olfactory center of the terrestrial slug LimaxMatsuo, Ryota; Kobayashi, Suguru; Wakiya, Kyoko; Yamagishi, Miki; Fukuoka, Masayuki; Ito, Etsuro
doi: 10.1002/cne.23559pmid: 24523205
Acetylcholine plays various important roles in the central nervous system of invertebrates as well as vertebrates. In the olfactory center of the terrestrial slug Limax, the local field potential (LFP) oscillates, and the change in its oscillatory frequency is thought to correlate with the detection of odor that potentially changes an ongoing behavior of the animal. Acetylcholine is known to upregulate the frequency of the LFP oscillation, and is one of the candidates for the neurotransmitters that are involved in such higher cognitive functions. However, there have been no histological data on the cholinergic system in gastropods, nor are there data on the receptors that are responsible for the upregulation of the oscillatory frequency of LFP due to the lack of analytical tools (such as antibodies or cDNA sequence information on cholinergic system‐related genes). Here we cloned the cDNAs of choline acetyltransferase (ChAT), acetylcholinesterase, vesicular acetylcholine transporter, and several nicotinic acetylcholine receptors (nAChRs), and investigated their localization in the brain of Limax. We also generated a polyclonal antibody against ChAT to examine its localization, and investigated pharmacologically the involvement of nAChRs in the LFP oscillation. Our data showed: 1) dense distribution of the neurons expressing mRNAs of ChAT and vesicular acetylcholine transporter in the olfactory center; 2) spatially unique expression patterns of different nAChRs in the olfactory center; 3) involvement of nAChRs in the upregulation of the oscillation; 4) localization of ChAT protein in nerve fibers and/or terminals; and 5) the presence of cholinergic nerves in the tentacles. J. Comp. Neurol. 522:2951–2966, 2014. © 2014 Wiley Periodicals, Inc.
Piezo2 expression in corneal afferent neuronsBron, Romke; Wood, Rhiannon J.; Brock, James A.; Ivanusic, Jason J.
doi: 10.1002/cne.23560pmid: 24549492
Recently, a novel class of mechanically sensitive channels has been identified and have been called Piezo channels. In this study, we explored Piezo channel expression in sensory neurons supplying the guinea pig corneal epithelium, which have well‐defined modalities in this species. We hypothesized that a proportion of corneal afferent neurons express Piezo2, and that these neurons are neurochemically distinct from corneal polymodal nociceptors or cold‐sensing neurons. We used a combination of retrograde tracing to identify corneal afferent neurons and double label in situ hybridization and/or immunohistochemistry to determine their molecular and/or neurochemical profile. We found that Piezo2 expression occurs in ∼26% of trigeminal ganglion neurons and 30% of corneal afferent neurons. Piezo2 corneal afferent neurons are almost exclusively non‐calcitonin gene‐related peptide (CGRP)‐immunoreactive (‐IR), medium‐ to large‐sized neurons that are NF200‐IR, suggesting they are not corneal polymodal nociceptors. There was no coexpression of Piezo2 and transient receptor potential cation channel subfamily M member 8 (TRPM8) transcripts in any corneal afferent neurons, further suggesting that Piezo2 is not expressed in corneal cold‐sensing neurons. We also noted that TRPM8‐IR or CGRP‐IR corneal afferent neurons are almost entirely small and lack NF200‐IR. Piezo2 expression occurs in a neurochemically distinct subpopulation of corneal afferent neurons that are not polymodal nociceptors or cold‐sensing neurons, and is likely confined to a subpopulation of pure mechano‐nociceptors in the cornea. This provides the first evidence in an in vivo system that Piezo2 is a strong candidate for a channel that transduces noxious mechanical stimuli. J. Comp. Neurol. 522:2967–2979, 2014. © 2014 Wiley Periodicals, Inc.
A comparative cluster analysis of nicotinamide adenine dinucleotide phosphate (NADPH)‐diaphorase histochemistry in the brains of amphibiansPinelli, Claudia; Rastogi, Rakesh K.; Scandurra, Anna; Jadhao, Arun G.; Aria, Massimo; D'Aniello, Biagio
doi: 10.1002/cne.23561pmid: 24549578
Nicotinamide adenine dinucleotide phosphate–diaphorase (NADPH‐d) is a key enzyme in the synthesis of the gaseous neurotransmitter nitric oxide. We compare the distribution of NADPH‐d in the brain of four species of hylid frogs. NADPH‐d–positive fibers are present throughout much of the brain, whereas stained cell groups are distributed in well‐defined regions. Whereas most brain areas consistently show positive neurons in all species, in some areas species‐specific differences occur. We analyzed our data and those available for other amphibian species to build a matrix on NADPH‐d brain distribution for a multivariate analysis. Brain dissimilarities were quantified by using the Jaccard index in a hierarchical clustering procedure. The whole brain dendrogram was compared with that of its main subdivisions by applying the Fowlkes–Mallows index for dendrogram similarity, followed by bootstrap replications and a permutation test. Despite the differences in the distribution map of the NADPH‐d system among species, cluster analysis of data from the whole brain and hindbrain faithfully reflected the evolutionary history (framework) of amphibians. Dendrograms from the secondary prosencephalon, diencephalon, mesencephalon, and isthmus showed some deviation from the main scheme. Thus, the present analysis supports the major evolutionary stability of the hindbrain. We provide evidence that the NADPH‐d system in main brain subdivisions should be cautiously approached for comparative purposes because specific adaptations of a single species could occur and may affect the NADPH‐d distribution pattern in a brain subdivision. The minor differences in staining pattern of particular subdivisions apparently do not affect the general patterns of staining across species. J. Comp. Neurol. 522:2980–3003, 2014. © 2014 Wiley Periodicals, Inc.
Emergence of sensory structures in the developing epidermis in sepia officinalis and other coleoid cephalopodsBuresi, Auxane; Croll, Roger P.; Tiozzo, Stefano; Bonnaud, Laure; Baratte, Sébastien
doi: 10.1002/cne.23562pmid: 24549606
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. J. Comp. Neurol. 522:3004–3019, 2014. © 2014 Wiley Periodicals, Inc.
Spatiotemporal distribution of SUMOylation components during mouse brain developmentHasegawa, Yuta; Yoshida, Daisuke; Nakamura, Yuki; Sakakibara, Shin‐ichi
doi: 10.1002/cne.23563pmid: 24639124
Posttranslational modification of proteins might play an important role in brain cellular dynamics via the rapid turnover or functional change of critical proteins controlling neuronal differentiation or synaptic transmission. Small ubiquitin‐like modifier protein (SUMO) is a family of ubiquitin‐like small proteins that are covalently attached to target proteins to modify their function posttranslationally. Many cellular processes, such as transcription and protein trafficking, are regulated by SUMOylation, but its functional significance in the brain remains unclear. Although developmental regulation of SUMOylation levels in rat brain was recently demonstrated, no comparative immunohistochemical analysis of the cellular distribution profiles of SUMOylation components, including SUMO1, SUMO2/3, and Ubc9, has been undertaken so far. The present study used immunohistochemical and immunoblot analysis with the different developmental stages of mice and demonstrated the developmentally regulated distribution of SUMO1, SUMO2/3, and Ubc9 in the brain. During embryonic development, SUMOylation by SUMO1 and SUMO2/3 occurred in the nucleoplasm of nestin‐positive neural stem cells. Although the total amount of SUMO‐modified proteins decreased during postnatal brain development, intense and persistent accumulation of SUMO2/3 was detected throughout life in neural progenitor populations in neurogenic regions, including the subventricular zone and the hippocampal subgranular zone. In contrast, many neurons in the adult brain accumulated SUMO1 rather than SUMO2/3. Heavy immunoreactivity of SUMO1 was found in large projection neurons in the brainstem, whereas SUMO2/3 was almost absent from these areas. This heterogeneous distribution implies that both proteins play a specific and unique role in the brain. J. Comp. Neurol. 522:3020–3036, 2014. © 2014 Wiley Periodicals, Inc.
Increased neuronal expression of neurokinin‐1 receptor and stimulus‐evoked internalization of the receptor in the rostral ventromedial medulla of the rat after peripheral inflammatory injuryHamity, Marta V.; Walder, Roxanne Y.; Hammond, Donna L.
doi: 10.1002/cne.23564pmid: 24639151
This study examined possible mechanisms by which Substance P (Sub P) assumes a pronociceptive role in the rostral ventromedial medulla (RVM) under conditions of peripheral inflammatory injury, in this case produced by intraplantar (ipl) injection of complete Freund's adjuvant (CFA). In saline‐ and CFA‐treated rats, neurokinin‐1 receptor (NK1R) immunoreactivity was localized to neurons in the RVM. Four days after ipl injection of CFA, the number of NK1R‐immunoreactive neurons in the RVM was increased by 30%, and there was a concomitant increase in NK1R‐immunoreactive processes in CFA‐treated rats. Although NK1R immunoreactivity was increased, tachykinin‐1 receptor (Tacr1) mRNA was not increased in the RVM of CFA‐treated rats. To assess changes in Sub P release, the number of RVM neurons that exhibited NK1R internalization was examined in saline‐ and CFA‐treated rats following noxious heat stimulation of the hind paws. Only CFA‐treated rats that experienced noxious heat stimulation exhibited a significant increase in the number of neurons showing NK1R internalization. These data suggest that tonic Sub P release is not increased as a simple consequence of peripheral inflammation, but that phasic or evoked release of Sub P in the RVM is increased in response to noxious peripheral stimulation in a persistent inflammatory state. These data support the proposal that an upregulation of the NK1R in the RVM, as well as enhanced release of Sub P following noxious stimulation, underlie the pronociceptive role of Sub P under conditions of persistent inflammatory injury. J. Comp. Neurol. 522:3037–3051, 2014. © 2014 Wiley Periodicals, Inc.
Species‐specific differences in the medial prefrontal projections to the pons between rat and rabbitMoya, Maria V.; Siegel, Jennifer J.; McCord, Eedann D.; Kalmbach, Brian E.; Dembrow, Nikolai; Johnston, Daniel; Chitwood, Raymond A.
doi: 10.1002/cne.23566pmid: 24639247
The medial prefrontal cortex (mPFC) of both rats and rabbits has been shown to support trace eyeblink conditioning, presumably by providing an input to the cerebellum via the pons that bridges the temporal gap between conditioning stimuli. The pons of rats and rabbits, however, shows divergence in gross anatomical organization, leaving open the question of whether the topography of prefrontal inputs to the pons is similar in rats and rabbits. To investigate this question, we injected anterograde tracer into the mPFC of rats and rabbits to visualize and map in 3D the distribution of labeled terminals in the pons. Effective mPFC injections showed labeled axons in the ipsilateral descending pyramidal tract in both species. In rats, discrete clusters of densely labeled terminals were observed primarily in the rostromedial pons. Clusters of labeled terminals were also observed contralateral to mPFC injection sites in rats, appearing as a less dense "mirror‐image" of ipsilateral labeling. In rabbits, mPFC labeled corticopontine terminals were absent in the rostral pons, and instead were restricted to the intermediate pons. The densest terminal fields were typically observed in association with the ipsilateral pyramidal tract as it descended ventromedially through the rabbit pons. No contralateral terminal labeling was observed for any injections made in the rabbit mPFC. The results suggest the possibility that mPFC inputs to the pons may be integrated with different sources of cortical inputs between rats and rabbits. The resulting implications for mPFC or pons manipulations for studies of trace eyeblink in each species are discussed. J. Comp. Neurol. 522:3052–3074, 2014. © 2014 Wiley Periodicals, Inc.