scholarly journals Non-thalamic origin of zebrafish sensory relay nucleus: convergent evolution of visual pathways in amniotes and teleosts

2020 ◽  
Author(s):  
Solal Bloch ◽  
Hanako Hagio ◽  
Manon Thomas ◽  
Aurélie Heuzé ◽  
Jean-Michel Hermel ◽  
...  

AbstractAscending visual projections similar to the mammalian thalamocortical pathway are found in a wide range of vertebrate species, but their homologous relationship is debated. To get better insights into their evolutionary origin, we examined the developmental origin of a visual relay nucleus in zebrafish (a teleost fish). Similarly to the tectofugal visual thalamic nuclei in amniotes, the lateral part of the preglomerular complex (PG) in teleosts receives tectal information and projects to the pallium. However, our cell lineage study reveals that the majority of PG cells are derived from the midbrain, not from the forebrain. We also demonstrate that the PG projection neurons develop gradually until juvenile stage, unlike the thalamic projection neurons. Our data suggest that teleost PG is not homologous to the amniote thalamus and that thalamocortical-like projections can evolve from a non-forebrain cell population. Thus, sensory pathways in vertebrate brains exhibit a surprising degree of variation.

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Solal Bloch ◽  
Hanako Hagio ◽  
Manon Thomas ◽  
Aurélie Heuzé ◽  
Jean-Michel Hermel ◽  
...  

Ascending visual projections similar to the mammalian thalamocortical pathway are found in a wide range of vertebrate species, but their homology is debated. To get better insights into their evolutionary origin, we examined the developmental origin of a thalamic-like sensory structure of teleosts, the preglomerular complex (PG), focusing on the visual projection neurons. Similarly to the tectofugal thalamic nuclei in amniotes, the lateral nucleus of PG receives tectal information and projects to the pallium. However, our cell lineage study in zebrafish reveals that the majority of PG cells are derived from the midbrain, unlike the amniote thalamus. We also demonstrate that the PG projection neurons develop gradually until late juvenile stages. Our data suggest that teleost PG, as a whole, is not homologous to the amniote thalamus. Thus, the thalamocortical-like projections evolved from a non-forebrain cell population, which indicates a surprising degree of variation in the vertebrate sensory systems.


Author(s):  
Ray Guillery

My thesis studies had stimulated an interest in the mamillothalamic pathways but also some puzzlement because we knew nothing about the nature of the messages passing along these pathways. Several laboratories were studying the thalamic relay of sensory pathways with great success during my post-doctoral years. Each sensory relay could be understood in terms of the appropriate sensory input, but we had no way of knowing the meaning of the mamillothalamic messages. I introduce these nuclei as an example of the many thalamic nuclei about whose input functions we still know little or nothing. Early clinical studies of mamillary lesions had suggested a role in memory formation, whereas evidence from cortical lesions suggested a role in emotional experiences. Studies of the smallest of the three nuclei forming these pathways then showed it to be concerned with sensing head direction, relevant but not sufficient for defining an animal’s position in space. More recent studies based on studies of cortical activity or cortical damage have provided a plethora of suggestions: as so often, the answers reported depend on the questions asked. That simple conclusion is relevant for all transthalamic pathways. The evidence introduced in Chapter 1, that thalamocortical messages have dual meanings, suggests that we need to rethink our questions. It may prove useful to look at the motor outputs of relevant cortical areas to get clues about some appropriate questions.


2000 ◽  
Vol 17 (2) ◽  
pp. 187-196 ◽  
Author(s):  
JOKUBAS ZIBURKUS ◽  
MARTHA E. BICKFORD ◽  
WILLIAM GUIDO

In normal adult cats, a monoclonal antibody directed toward the NR-1 subunit of the N-methyl-d-aspartate (NMDA) receptor (Pharmingen, clone 54.1) produced dense cellular and neuropil labeling throughout all layers of the lateral geniculate nucleus (LGN) and adjacent thalamic nuclei, including the thalamic reticular, perigeniculate, medial intralaminar, and ventral lateral geniculate nuclei. Cellular staining revealed well-defined somata, and in some cases proximal dendrites. NMDAR-1 cell labeling was also evident in the LGN of early postnatal kittens, suggesting that developing LGN cells possess this receptor subunit at or before eye opening. Within the A-layers of the adult LGN, staining encompassed a wide range of soma sizes. Soma size comparisons of NMDAR-1 stained cells with those stained with an antibody directed toward a nonphosphorylated neurofilament protein (SMI-32), which selectively stains Y-relay cells (Bickford et al., 1998), or an antibody to glutamic acid decarboxylase (GAD), which stains for GABAergic interneurons, suggested that NMDA receptors are utilized by relay cells and interneurons. NMDAR-1 staining was also observed in the LGN of cats with early monocular lid suture. Although labeling was apparent in both deprived and nondeprived A-layers of LGN, the distribution of soma sizes was significantly different. In the deprived A-layers of LGN, staining was limited to small- and medium-sized cells. Cells with relatively large soma were lacking. However, cell density measurements as well as soma size comparisons with cells stained for Nissl substance suggested these differences were due to deprivation-induced cell shrinkage and not to a loss of NMDAR-1 staining in Y-cells. Taken together, these results suggest that NMDA receptors are utilized by both relay cells and interneurons in LGN and that alterations in early visual experience do not necessarily affect the expression of NMDA receptors in the LGN.


1986 ◽  
Vol 56 (6) ◽  
pp. 1475-1497 ◽  
Author(s):  
P. Herron ◽  
R. Dykes

The ventroposterior region of the thalamus of mongrel cats was searched to locate zones activated by somatic stimuli. By using stimuli that selectively excited Pacinian corpuscles, areas activated by this class of afferent fibers were differentiated from regions activated by other classes of cutaneous mechanoreceptors. The results showed that Pacinian inputs excite neurons in the ventroposterior inferior nucleus (VPI) of the thalamus, whereas other more dorsal zones within the ventroposterior thalamus receive inputs from other mechanoreceptor classes. This definition of the VPI tended to be larger and to extend further lateral than some published descriptions. Horseradish peroxidase (HRP) was injected into ventroposterior zones shown by electrophysiological recordings to receive inputs from Pacinian afferents. Subsequently, labeled cell bodies were observed in the caudal poles of the dorsal column nuclei, a region previously shown to be activated by Pacinian afferents. Very few labeled cells were found in the central region of these nuclei, a region previously shown to be activated by other classes of cutaneous mechanoreceptors. Electrophysiological recordings were used to locate a small portion of the second somatosensory cortex driven by Pacinian stimuli. When HRP was injected into this region cell bodies in the VPI and the lateral part of the posterior group were labeled, but few or no labeled cells were found in ventroposterior lateral nucleus. We hypothesize that the VPI receives Pacinian information from a cytoarchitecturally distinct region in the caudal poles of the dorsal column nuclei. Further, we suggest that a major cortical target for the VPI is a subdivision of the second somatosensory cortex. These studies do not exclude the possibility that Pacinian inputs have other thalamic and cortical targets.


2000 ◽  
Vol 84 (5) ◽  
pp. 2204-2216 ◽  
Author(s):  
Marc L. Belleau ◽  
Richard A. Warren

We have studied the postnatal development of the physiological characteristics of nucleus accumbens (nAcb) neurons in slices from postnatal day 1 ( P1) to P49 rats using the whole cell patch-clamp technique. The majority of neurons (102/108) were physiologically identified as medium spiny (MS) projection neurons, and only these were subjected to detailed analysis. The remaining neurons displayed characteristics suggesting that they were not MS neurons. Around the time of birth and during the first postnatal weeks, the membrane and firing characteristics of MS neurons were quite different from those observed later. These characteristics changed rapidly during the first 3 postnatal weeks, at which point they began to resemble those found in adults. Both whole cell membrane resistance and membrane time constant decreased more than fourfold during the period studied. The resting membrane potential (RMP) also changed significantly from an average of −50 mV around birth to less than −80 mV by the end of the third postnatal week. During the first postnatal week, the current-voltage relationship of all encountered MS neurons was linear over a wide range of membrane potentials above and below RMP. Through the second postnatal week, the proportion of neurons displaying inward rectification in the hyperpolarized range increased steadily and after P15, all recorded MS neurons displayed significant inward rectification. At all ages, inward rectification was blocked by extracellular cesium and tetra-ethyl ammonium and was not changed by 4-aminopyridine; this shows that inward rectification was mediated by the same currents in young and mature MS neurons. MS neurons fired single and repetitive Na+/K+ action potentials as early as P1. Spike threshold and amplitude remained constant throughout development in contrast to spike duration, which decreased significantly over the same period. Depolarizing current pulses from rest showed that immature MS neurons fired action potentials more easily than their older counterparts. Taken together, the results from the present study suggest that young and adult nAcb MS neurons integrate excitatory synaptic inputs differently because of differences in their membrane and firing properties. These findings provide important insights into signal processing within nAcb during this critical period of development.


2016 ◽  
Vol 113 (21) ◽  
pp. E2906-E2915 ◽  
Author(s):  
Vicente José Planelles-Herrero ◽  
Florian Blanc ◽  
Serena Sirigu ◽  
Helena Sirkia ◽  
Jeffrey Clause ◽  
...  

Myosins containing MyTH4-FERM (myosin tail homology 4-band 4.1, ezrin, radixin, moesin, or MF) domains in their tails are found in a wide range of phylogenetically divergent organisms, such as humans and the social amoeba Dictyostelium (Dd). Interestingly, evolutionarily distant MF myosins have similar roles in the extension of actin-filled membrane protrusions such as filopodia and bind to microtubules (MT), suggesting that the core functions of these MF myosins have been highly conserved over evolution. The structures of two DdMyo7 signature MF domains have been determined and comparison with mammalian MF structures reveals that characteristic features of MF domains are conserved. However, across millions of years of evolution conserved class-specific insertions are seen to alter the surfaces and the orientation of subdomains with respect to each other, likely resulting in new sites for binding partners. The MyTH4 domains of Myo10 and DdMyo7 bind to MT with micromolar affinity but, surprisingly, their MT binding sites are on opposite surfaces of the MyTH4 domain. The structural analysis in combination with comparison of diverse MF myosin sequences provides evidence that myosin tail domain features can be maintained without strict conservation of motifs. The results illustrate how tuning of existing features can give rise to new structures while preserving the general properties necessary for myosin tails. Thus, tinkering with the MF domain enables it to serve as a multifunctional platform for cooperative recruitment of various partners, allowing common properties such as autoinhibition of the motor and microtubule binding to arise through convergent evolution.


2012 ◽  
Vol 92 (4) ◽  
pp. 1543-1576 ◽  
Author(s):  
Anthony M. Carter

Placenta has a wide range of functions. Some are supported by novel genes that have evolved following gene duplication events while others require acquisition of gene expression by the trophoblast. Although not expressed in the placenta, high-affinity fetal hemoglobins play a key role in placental gas exchange. They evolved following duplications within the beta-globin gene family with convergent evolution occurring in ruminants and primates. In primates there was also an interesting rearrangement of a cassette of genes in relation to an upstream locus control region. Substrate transfer from mother to fetus is maintained by expression of classic sugar and amino acid transporters at the trophoblast microvillous and basal membranes. In contrast, placental peptide hormones have arisen largely by gene duplication, yielding for example chorionic gonadotropins from the luteinizing hormone gene and placental lactogens from the growth hormone and prolactin genes. There has been a remarkable degree of convergent evolution with placental lactogens emerging separately in the ruminant, rodent, and primate lineages and chorionic gonadotropins evolving separately in equids and higher primates. Finally, coevolution in the primate lineage of killer immunoglobulin-like receptors and human leukocyte antigens can be linked to the deep invasion of the uterus by trophoblast that is a characteristic feature of human placentation.


2016 ◽  
Vol 115 (3) ◽  
pp. 1521-1532 ◽  
Author(s):  
Konstantin I. Bakhurin ◽  
Victor Mac ◽  
Peyman Golshani ◽  
Sotiris C. Masmanidis

As the major input to the basal ganglia, the striatum is innervated by a wide range of other areas. Overlapping input from these regions is speculated to influence temporal correlations among striatal ensembles. However, the network dynamics among behaviorally related neural populations in the striatum has not been extensively studied. We used large-scale neural recordings to monitor activity from striatal ensembles in mice undergoing Pavlovian reward conditioning. A subpopulation of putative medium spiny projection neurons (MSNs) was found to discriminate between cues that predicted the delivery of a reward and cues that predicted no specific outcome. These cells were preferentially located in lateral subregions of the striatum. Discriminating MSNs were more spontaneously active and more correlated than their nondiscriminating counterparts. Furthermore, discriminating fast spiking interneurons (FSIs) represented a highly prevalent group in the recordings, which formed a strongly correlated network with discriminating MSNs. Spike time cross-correlation analysis showed the existence of synchronized activity among FSIs and feedforward inhibitory modulation of MSN spiking by FSIs. These findings suggest that populations of functionally specialized (cue-discriminating) striatal neurons have distinct network dynamics that sets them apart from nondiscriminating cells, potentially to facilitate accurate behavioral responding during associative reward learning.


2018 ◽  
Author(s):  
Rafael F. Guerrero ◽  
Matthew W. Hahn

AbstractConvergent evolution is often inferred when a trait is incongruent with the species tree. However, trait incongruence can also arise from changes that occur on discordant gene trees, a process referred to as hemiplasy. Hemiplasy is rarely taken into account in studies of convergent evolution, despite the fact that phylogenomic studies have revealed rampant discordance. Here, we study the relative probabilities of homoplasy (including convergence and reversal) and hemiplasy for an incongruent trait. We derive expressions for the probabilities of the two events, showing that they depend on many of the same parameters. We find that hemiplasy is as likely— or more likely—than homoplasy for a wide range of conditions, even when levels of discordance are low. We also present a new method to calculate the ratio of these two probabilities (the “hemiplasy risk factor”) along the branches of a phylogeny of arbitrary length. Such calculations can be applied to any tree in order to identify when and where incongruent traits may be more likely to be due to hemiplasy than homoplasy.


2019 ◽  
Author(s):  
Giovanne B. Diniz ◽  
Daniella S. Battagello ◽  
Bianca S. M. Bono ◽  
Jozélia G. P. Ferreira ◽  
Marianne O. Klein ◽  
...  

AbstractMelanin-concentrating hormone (MCH) is a ubiquitous vertebrate neuropeptide predominantly synthesized by neurons of the diencephalon that can act through two G protein-coupled receptors, called MCHR1 and MCHR2. The expression of Mchr1 has been investigated in both rats and mice, but its synthesis remains poorly described. After identifying an antibody that detects MCHR1 with high specificity, we employed immunohistochemistry to map the distribution of MCHR1 in the CNS of rats and mice. Multiple neurochemical markers were also employed to characterize some of the neuronal populations that synthesize MCHR1. Our results show that MCHR1 is abundantly found in a sensory subcellular structure called the neuronal primary cilium, which has been associated with the detection of free neurochemical agents released to act through volume transmission. Ciliary MCHR1 was found in a wide range of areas, including the olfactory bulb, cortical mantle, striatum, hippocampal formation, amygdala, midline thalamic nuclei, periventricular hypothalamic nuclei, and midbrain areas. No differences were observed between male and female mice, and rats and mice diverged in two key areas: the caudate-putamen nucleus and the subgranular zone of the dentate gyrus. Ciliary MCHR1 was found in close association to several neurochemical markers, including tyrosine hydroxylase, calretinin, kisspeptin, estrogen receptor, oxytocin, vasopressin, and corticotropin-releasing factor. Given the role of neuronal primary cilia in sensing free neurochemical messengers in the extracellular fluid, the widespread distribution of ciliary MCHR1, and the diverse neurochemical populations who synthesize MCHR1, our data indicates that volume transmission may play a prominent role in the normal function of the MCH system.


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