The mammalian neocortex mediates complex cognitive behaviors, such as sensory perception, decision making, and language. The evolutionary history of the cortex, and the cells and circuitry underlying similar capabilities in nonmammals, are poorly understood, however. Two distinct features of the mammalian neocortex are lamination and radially arrayed columns that form functional modules, characterized by defined neuronal types and unique intrinsic connections. The seeming inability to identify these characteristic features in nonmammalian forebrains with earlier methods has often led to the assumption of uniqueness of neocortical cells and circuits in mammals. Using contemporary methods, we demonstrate the existence of comparable columnar functional modules in laminated auditory telencephalon of an avian species (Gallus gallus). A highly sensitive tracer was placed into individual layers of the telencephalon within the cortical region that is similar to mammalian auditory cortex. Distribution of anterograde and retrograde transportable markers revealed extensive interconnections across layers and between neurons within narrow radial columns perpendicular to the laminae. This columnar organization was further confirmed by visualization of radially oriented axonal collaterals of individual intracellularly filled neurons. Common cell types in birds and mammals that provide the cellular substrate of columnar functional modules were identified. These findings indicate that laminar and columnar properties of the neocortex are not unique to mammals and may have evolved from cells and circuits found in more ancient vertebrates. Specific functional pathways in the brain can be analyzed in regard to their common phylogenetic origins, which introduces a previously underutilized level of analysis to components involved in higher cognitive functions. neocortex evolution | columnar organization | primary auditory cortex | intrinsic circuitry | granule cell T he origins and evolution of the forebrain and the mammalian neocortex,* where complex cognitive functions are centered, have long been of broad interest to scientists and nonscientists alike. For more than 100 y, the neocortex was considered an independently evolved structure unique to mammals. The nonmammalian telencephalon was frequently compared with the mammalian basal ganglia, which was thought to be involved in stereotypical instinctive behaviors (1). A revolutionary revision in our concept of the nature of vertebrate brain organization was recently accepted in the revised nomenclature of the avian brain (2, 3). The avian Wulst and dorsal ventricular ridge, two prominent components of the telencephalon, are recognized as being homologous to pallial components of mammalian brains, which is consistent with the idea that avian telencephalon includes a large cortical component ( Fig. 1 A-C) (4-6). However, this postulated homology addresses only the most general aspects of the evolutionary relationship of the avian brain to the mammal brain, that is, in indicating that ...
The nucleus isthmi pars magnocellularis (Imc) and pars parvocellularis (Ipc) influence the receptive field structure of neurons in the optic tectum (TeO). To understand better the anatomical substrate of isthmotectal interactions, neuronal morphology and connections of Imc were examined in chicks (Gallus gallus). Cholera toxin B injection into TeO demonstrated a coarse topographical projection from TeO upon Imc. Retrogradely labeled neurons were scattered throughout Imc and in low density within the zone of anterogradely labeled terminals, suggesting a heterotopic projection from Imc upon TeO. This organization differed from the precise homotopic reciprocal connections of Ipc and the nucleus isthmi pars semilunaris (SLu) with TeO. By using slice preparations, extracellular biotinylated dextran amine injections demonstrated a dense projection from most neurons in Imc upon both Ipc and SLu. Intracellular filling of Imc neurons with biocytin revealed two cell types. The most common, Imc-Is, formed a widely ramifying axonal field in both Ipc and SLu, without obvious topography. A less frequently observed cell type, Imc-Te, formed a widely ramifying terminal field in layers 10-12 of TeO. No neurons were found to project upon both Ipc/SLu and TeO. Both types possessed local axon collaterals and flat dendritic fields oriented parallel to the long axis of Imc. Imc neurons contain glutamic acid decarboxylase, which is consistent with Imc participating in center-surround or other wide-field inhibitory isthmotectal interactions. The laminar and columnar pattern of isthmotectal terminals also suggests a means of interacting with multiple tectofugal pathways, including the stratified subpopulations of tectorotundal neurons participating in motion detection.
The cholinergic division of the avian nucleus isthmi, the homolog of the mammalian nucleus parabigeminalis, is composed of the pars parvocellularis (Ipc) and pars semilunaris (SLu). Ipc and SLu were studied with in vivo and in vitro tracing and intracellular filling methods. 1) Both nuclei have reciprocal homotopic connections with the ipsilateral optic tectum. The SLu connection is more diffuse than that of Ipc. 2) Tectal inputs to Ipc and SLu are Brn3a-immunoreactive neurons in the inner sublayer of layer 10. Tectal neurons projecting on Ipc possess "shepherd's crook" axons and radial dendritic fields in layers 2-13. 3) Neurons in the mid-portion of Ipc possess a columnar spiny dendritic field. SLu neurons have a large, nonoriented spiny dendritic field. 4) Ipc terminals form a cylindrical brush-like arborization (35-50 microm wide) in layers 2-10, with extremely dense boutons in layers 3-6, and a diffuse arborization in layers 11-13. SLu neurons terminate in a wider column (120-180 microm wide) lacking the dust-like boutonal features of Ipc and extend in layers 4c-13 with dense arborizations in layers 4c, 6, and 9-13. 5) Ipc and SLu contain specialized fast potassium ion channels. We propose that dense arborizations of Ipc axons may be directed to the distal dendritic bottlebrushes of motion detecting tectal ganglion cells (TGCs). They may provide synchronous activation of a group of adjacent bottlebrushes of different TGCs of the same type via their intralaminar processes, and cross channel activation of different types of TGCs within the same column of visual space.
The study of Hemipteran mitochondrial genomes (mitogenomes) began with the Chagas disease vector, Triatoma dimidiata, in 2001. At present, 90 complete Hemipteran mitogenomes have been sequenced and annotated. This review examines the history of Hemipteran mitogenomes research and summarizes the main features of them including genome organization, nucleotide composition, protein-coding genes, tRNAs and rRNAs, and non-coding regions. Special attention is given to the comparative analysis of repeat regions. Gene rearrangements are an additional data type for a few families, and most mitogenomes are arranged in the same order to the proposed ancestral insect. We also discuss and provide insights on the phylogenetic analyses of a variety of taxonomic levels. This review is expected to further expand our understanding of research in this field and serve as a valuable reference resource.
Neuronal dendrites are structurally and functionally dynamic in response to changes in afferent activity. The fragile X mental retardation protein (FMRP) is an mRNA binding protein that regulates activity-dependent protein synthesis and morphological dynamics of dendrites. Loss and abnormal expression of FMRP occur in fragile X syndrome (FXS) and some forms of autism spectrum disorders. To provide further understanding of how FMRP signaling regulates dendritic dynamics, we have examined dendritic expression and localization of FMRP in the reptilian and avian nucleus laminaris (NL) and its mammalian analogue, the medial superior olive (MSO), in rodents and humans. NL/MSO neurons are specialized for temporal processing of low frequency sounds for binaural hearing, which is impaired in FXS. Protein BLAST analyses first demonstrate that the FMRP amino acid sequences in the alligator and chicken are highly similar to human FMRP with identical mRNA-binding and phosphorylation sites, suggesting that FMRP functions similarly across vertebrates. Immunocytochemistry further reveals that NL/MSO neurons have very high levels of dendritic FMRP in low frequency hearing vertebrates including alligator, chicken, gerbil, and human. Remarkably, dendritic FMRP in NL/MSO neurons often accumulates at branch points and enlarged distal tips, loci known to be critical for branch-specific dendritic arbor dynamics. These observations support an important role for FMRP in regulating dendritic properties of binaural neurons that are essential for low frequency sound localization and auditory scene segregation, and support the relevance of studying this regulation in nonhuman vertebrates that use low frequencies in order to further understand human auditory processing disorders.
The fragile X mental retardation protein (FMRP) plays an important role in normal brain development. Absence of FMRP, caused by transcriptional silencing of FMR1 gene, results in abnormal neuronal morphologies in a selected manner throughout the brain and leads to intellectual deficits and sensory dysfunction in the fragile X syndrome (FXS). Despite the paramount importance of FMRP for proper brain function, its overall expression pattern in the mammalian brain at the resolution of individual neuronal cell groups is not known. In this study, we used FMR1 knockout and their isogenic wild type mice to systematically map the distribution of FMRP expression in the entire mouse brain. Using immunocytochemistry and cellular quantification analyses, we identified a large number of prominent cell groups expressing high levels of FMRP at the subcortical levels, in particular sensory and motor neurons in the brainstem and thalamus. In contrast, many cell groups in the midbrain and hypothalamus exhibit low FMRP levels. More importantly, we describe differential patterns of FMRP distribution in both cortical and subcortical brain regions. Almost all major brain areas contain high and low levels of FMRP cell groups adjacent to each other or between layers of the same cortical areas. These differential patterns indicate that FMRP expression is specific to individual neuronal cell groups, instead of associated with brain regions as previously considered. Taken together, these findings support the notion that FMRP mechanisms of neuronal regulation are cell-type specific and strongly implicate the contribution of fundamental sensory and motor processing at subcortical levels to FXS pathology.
of glutamatergic synaptic transmission in binaural auditory neurons. J Neurophysiol 104: 1774 -1789, 2010. First published July 28, 2010 doi:10.1152/jn.00468.2010. Glutamatergic synaptic transmission is essential for binaural auditory processing in birds and mammals. Using whole cell voltage clamp recordings, we characterized the development of synaptic ionotropic glutamate receptor (iGluR) function from auditory neurons in the chick nucleus laminaris (NL), the first nucleus responsible for binaural processing. We show that synaptic transmission is mediated by AMPA-and N-methyl-D-aspartate (NMDA)-type glutamate receptors (AMPA-R and NMDA-R, respectively) when hearing is first emerging and dendritic morphology is being established across different sound frequency regions. Puff application of glutamate agonists at embryonic day 9 (E9) revealed that both iGluRs are functionally present prior to synapse formation (E10). Between E11 and E19, the amplitude of isolated AMPA-R currents from high-frequency (HF) neurons increased 14-fold. A significant increase in the frequency of spontaneous events is also observed. Additionally, AMPA-R currents become faster and more rectifying, suggesting developmental changes in subunit composition. These developmental changes were similar in all tonotopic regions examined. However, mid-and low-frequency neurons exhibit fewer spontaneous events and evoked AMPA-R currents are smaller, slower, and less rectifying than currents from age-matched HF neurons. The amplitude of isolated NMDA-R currents from HF neurons also increased, reaching a peak at E17 and declining sharply by E19, a trend consistent across tonotopic regions. With age, NMDA-R kinetics become significantly faster, indicating a developmental switch in receptor subunit composition. Dramatic increases in the amplitude and speed of glutamatergic synaptic transmission occurs in NL during embryonic development. These changes are first seen in HF neurons suggesting regulation by peripheral inputs and may be necessary to enhance coincidence detection of binaural auditory information.
Vertebrates are able to visually identify moving objects and orient toward attractive ones or escape if the objects seem threatening. When there is more than one object in the visual field, they can attend to a particular object. The optic tectum (superior colliculus in mammals) (OT/SC) has long been known to mediate such functions (Schneider, 1969;Ingle, 1973a). Less well known is that the OT/SC is strongly affected by a smaller midbrain area called nucleus isthmi (parabigeminal nucleus in mammals) (NI/PB). We discuss how NI/PB influences OT/SC function and visual behavior.Anatomically, OT/SC makes reciprocal, topographic connections with ipsilateral NI/PB. Adjacent points in OT/SC project to adjacent points in NI/PB. The return projections from NI/PB terminate in many of the same superficial layers as retinotectal fibers, and their effects on tectal processing may facilitate selection of a single stimulus from an array of potential targets. In amphibians and mammals, NI/PB also project to the contralateral OT/SC (Fig. 1). Visual behavior and the frog NIWhen presented with a single prey stimulus anywhere in its visual field, a frog will approach and attack the stimulus. When presented with two prey stimuli, they will select one of the stimuli (Ingle, 1973b;Stull and Gruberg, 1998). After ablation of the optic tectum, frogs will not respond to prey stimuli (or to looming stimuli), although they retain other visual abilities, such as perceiving stationary objects (Ingle, 1973b).Other than the retina, the greatest input to the OT in frogs comes from NI. It can be divided into two functionally discrete regions: one region makes topographic reciprocal connections with the ipsilateral OT; the other region projects topographically to the contralateral tectal lobe. Unilateral ablation of NI results in a scotoma in the contralateral monocular visual field (Gruberg et al., 1991) that is similar to unilateral ablation of the OT. Partial ablation of NI results in a smaller scotoma that always includes the posteriormost part of the monocular field. Within the scotoma, the behavioral threshold to prey stimuli is considerably increased and resembles visual neglect.NI directly influences retinotectal transmission (King and Schmidt, 1991;Dudkin and Gruberg, 2003). Frog isthmotectal fibers are cholinergic (Desan et al., 1987;Wallace et al., 1990) and terminate in retino-recipient layers of the optic tectum. Retinal ganglion cell axons express nicotinic acetylcholine (ACh) receptors (Sargent et al., 1989). There do not appear to be conventional synapses between isthmotectal fibers and retinotectal axons (Gruberg et al., 1994). Nonetheless, by selectively filling retinotectal fibers with a fluorescent calcium-sensitive dye, NI influence on retinotectal fibers can be shown. Single-shock stimulation to the optic nerve causes a brief increase in fluorescence. Singleshock stimulation to NI causes no change in fluorescence. When single-shock stimulation of NI is paired with optic nerve stimulation, there is a greater than twofold incre...
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