Primary sensory map formations reflect unique needs and molecular cues specific to each sensory system

. 2019 ; 8 () : . [epub] 20190327

Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection

Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid30984379

Grantová podpora
R01 AG060504 NIA NIH HHS - United States
R03 DC015333 NIDCD NIH HHS - United States

Interaction with the world around us requires extracting meaningful signals to guide behavior. Each of the six mammalian senses (olfaction, vision, somatosensation, hearing, balance, and taste) has a unique primary map that extracts sense-specific information. Sensory systems in the periphery and their target neurons in the central nervous system develop independently and must develop specific connections for proper sensory processing. In addition, the regulation of sensory map formation is independent of and prior to central target neuronal development in several maps. This review provides an overview of the current level of understanding of primary map formation of the six mammalian senses. Cell cycle exit, combined with incompletely understood molecules and their regulation, provides chemoaffinity-mediated primary maps that are further refined by activity. The interplay between cell cycle exit, molecular guidance, and activity-mediated refinement is the basis of dominance stripes after redundant organ transplantations in the visual and balance system. A more advanced level of understanding of primary map formation could benefit ongoing restoration attempts of impaired senses by guiding proper functional connection formations of restored sensory organs with their central nervous system targets.

Zobrazit více v PubMed

Shepherd GM: Smell images and the flavour system in the human brain. PubMed DOI

D'Elia KP, Dasen JS: Topographic Maps: Motor Axons Wait Their Turn. PubMed DOI

Hebb DO:

Laumonnerie C, Bechara A, Vilain N, et al. : Facial whisker pattern is not sufficient to instruct a whisker-related topographic map in the mouse somatosensory brainstem. PubMed DOI

Erzurumlu RS, Murakami Y, Rijli FM: Mapping the face in the somatosensory brainstem. PubMed DOI PMC

Brecht M: The Body Model Theory of Somatosensory Cortex. PubMed DOI

Triplett JW: Molecular guidance of retinotopic map development in the midbrain. PubMed DOI

Dhande OS, Huberman AD: Retinal ganglion cell maps in the brain: implications for visual processing. PubMed DOI PMC

Muniak MA, Connelly CJ, Suthakar K, et al. : Central Projections of Spiral Ganglion Neurons. In DOI

Schreiner CE, Polley DB: Auditory map plasticity: Diversity in causes and consequences. PubMed DOI PMC

Schreiner CE, Winer JA: Auditory cortex mapmaking: principles, projections, and plasticity. PubMed DOI PMC

Seabrook TA, Burbridge TJ, Crair MC, et al. : Architecture, Function, and Assembly of the Mouse Visual System. PubMed DOI

Huberman AD, Feller MB, Chapman B: Mechanisms underlying development of visual maps and receptive fields. PubMed DOI PMC

Jeffress LA: A place theory of sound localization. PubMed DOI

Carr CE, Peña JL: Cracking an improbable sensory map. PubMed DOI

McAlpine D, Grothe B: Sound localization and delay lines--do mammals fit the model? PubMed DOI

Chagnaud BP, Engelmann J, Fritzsch B, et al. : Sensing External and Self-Motion with Hair Cells: A Comparison of the Lateral Line and Vestibular Systems from a Developmental and Evolutionary Perspective. PubMed DOI PMC

Krahe R, Maler L: Neural maps in the electrosensory system of weakly electric fish. PubMed DOI

Dang P, Fisher SA, Stefanik DJ, et al. : Coordination of olfactory receptor choice with guidance receptor expression and function in olfactory sensory neurons. PubMed DOI PMC

Mori K, Sakano H: How is the olfactory map formed and interpreted in the mammalian brain? PubMed DOI

Straka H, Fritzsch B, Glover JC: Connecting ears to eye muscles: evolution of a 'simple' reflex arc. PubMed DOI

Maklad A, Fritzsch B: Development of vestibular afferent projections into the hindbrain and their central targets. PubMed DOI PMC

Wu A, Dvoryanchikov G, Pereira E, et al. : Breadth of tuning in taste afferent neurons varies with stimulus strength. PubMed DOI PMC

Smith DV, Margolskee RF: Making sense of taste. PubMed DOI

Chamma H, Jebai F, Sater FA, et al. : Taste mapping: A new approach for the taste regions.

Lundy RF, Norgren R: Gustatory System. In DOI

Sperry RW: Chemoaffinity in the orderly growth of nerve fiber patterns and connections. PubMed DOI PMC

Hebb DO: The Organization of Behavior. Wiley, New York,1949. Reference Source PubMed

Ruthazer ES, Akerman CJ, Cline HT: Control of axon branch dynamics by correlated activity PubMed DOI

Babola TA, Li S, Gribizis A, et al. : Homeostatic Control of Spontaneous Activity in the Developing Auditory System. PubMed DOI PMC

Yu CR, Power J, Barnea G, et al. : Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. PubMed DOI

Leighton AH, Lohmann C: The Wiring of Developing Sensory Circuits-From Patterned Spontaneous Activity to Synaptic Plasticity Mechanisms. PubMed DOI PMC

Luo L, Flanagan JG: Development of continuous and discrete neural maps. PubMed DOI

Dahmani L, Patel RM, Yang Y, et al. : An intrinsic association between olfactory identification and spatial memory in humans. PubMed DOI PMC

Yu L, Cuppini C, Xu J, et al. : Cross-Modal Competition: The Default Computation for Multisensory Processing. PubMed DOI PMC

Schier LA, Spector AC: The Functional and Neurobiological Properties of Bad Taste. PubMed DOI PMC

Buck L, Axel R: A novel multigene family may encode odorant receptors: A molecular basis for odor recognition. PubMed DOI

Nishizumi H, Sakano H: Developmental regulation of neural map formation in the mouse olfactory system. PubMed DOI

Mombaerts P, Wang F, Dulac C, et al. : Visualizing an olfactory sensory map. PubMed DOI

Bozza T, Vassalli A, Fuss S, et al. : Mapping of class I and class II odorant receptors to glomerular domains by two distinct types of olfactory sensory neurons in the mouse. PubMed DOI PMC

Flanagan JG: Neural map specification by gradients. PubMed DOI

Kishida T, Thewissen J, Usip S, et al. : Organization and distribution of glomeruli in the bowhead whale olfactory bulb. PubMed DOI PMC

Yu CR, Wu Y: Regeneration and rewiring of rodent olfactory sensory neurons. PubMed DOI

Shipley M, Ennis M, Puche A: Olfactory System. (Academic Press, Amsterdam)2004;923–964. 10.1016/B978-012547638-6/50030-4 DOI

Stout RP, Graziadei PP: Influence of the olfactory placode on the development of the brain in PubMed DOI

Steventon B, Mayor R, Streit A: Neural crest and placode interaction during the development of the cranial sensory system. PubMed DOI PMC

Maier EC, Saxena A, Alsina B, et al. : Sensational placodes: neurogenesis in the otic and olfactory systems. PubMed DOI PMC

Mombaerts P: Genes and ligands for odorant, vomeronasal and taste receptors. PubMed DOI

Crapon de Caprona MD, Fritzsch B: The development of the retinopetal nucleus olfacto-retinalis of two cichlid fish as revealed by horseradish peroxidase. PubMed DOI

Kawauchi S, Kim J, Santos R, et al. : PubMed DOI PMC

Panaliappan TK, Wittmann W, Jidigam VK, et al. : Sox2 is required for olfactory pit formation and olfactory neurogenesis through BMP restriction and PubMed DOI PMC

Tan L, Xie XS: A Near-Complete Spatial Map of Olfactory Receptors in the Mouse Main Olfactory Epithelium. PubMed DOI PMC

Imai T, Yamazaki T, Kobayakawa R, et al. : Pre-target axon sorting establishes the neural map topography. PubMed DOI

Zapiec B, Bressel OC, Khan M, et al. : Neuropilin-1 and the Positions of Glomeruli in the Mouse Olfactory Bulb. PubMed DOI PMC

Rubel EW, Fritzsch B: Auditory system development: primary auditory neurons and their targets. PubMed DOI

Macova I, Pysanenko K, Chumak T, et al. : Neurod1 Is Essential for the Primary Tonotopic Organization and Related Auditory Information Processing in the Midbrain. PubMed DOI PMC

Matei V, Pauley S, Kaing S, et al. : Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. PubMed DOI PMC

Shepard AR, Scheffel JL, Yu WM: Relationships between neuronal birthdates and tonotopic positions in the mouse cochlear nucleus. PubMed DOI PMC

Sweeney LB, Couto A, Chou YH, et al. : Temporal target restriction of olfactory receptor neurons by Semaphorin-1a/PlexinA-mediated axon-axon interactions. PubMed DOI

Wang Y, Bao X, Wu S, et al. : Semaphorin 3A as an inhibitive factor for migration of olfactory ensheathing cells through cofilin activation is involved in formation of olfactory nerve layer. PubMed DOI

Cloutier JF, Sahay A, Chang EC, et al. : Differential requirements for semaphorin 3F and Slit-1 in axonal targeting, fasciculation, and segregation of olfactory sensory neuron projections. PubMed DOI PMC

Albeanu DF, Provost AC, Agarwal P, et al. : Olfactory marker protein regulates refinement of the glomerular map. PubMed DOI PMC

Glover JC, Elliott KL, Erives A, et al. : Wilhelm His' lasting insights into hindbrain and cranial ganglia development and evolution. PubMed DOI PMC

Fritzsch B, Sarai PA, Barbacid M, et al. : Mice with a targeted disruption of the neurotrophin receptor PubMed DOI

Fritzsch B, Gregory D, Rosa-Molinar E: The development of the hindbrain afferent projections in the axolotl: evidence for timing as a specific mechanism of afferent fiber sorting. PubMed DOI PMC

Fritzsch B, Elliott KL: Gene, cell, and organ multiplication drives inner ear evolution. PubMed DOI PMC

Morrison EE, Graziadei PP: Transplants of olfactory mucosa in the rat brain I. A light microscopic study of transplant organization. PubMed DOI

Kersigo J, D'Angelo A, Gray BD, et al. : The role of sensory organs and the forebrain for the development of the craniofacial shape as revealed by Foxg1-cre-mediated microRNA loss. PubMed DOI PMC

Sperry R: How a developing brain gets itself properly wired for adaptive function. In:

Gierer A: Directional cues for growing axons forming the retinotectal projection.

Bridge H, Bell AH, Ainsworth M, et al. : Intact extrastriate visual network without primary visual cortex in a Rhesus macaque with naturally occurring Blindsight. DOI

Cowey A, Stoerig P: Blindsight in monkeys. PubMed DOI

Maharana SK, Schlosser G: A gene regulatory network underlying the formation of pre-placodal ectoderm in PubMed DOI PMC

Manns M, Fritzsch B: The eye in the brain: retinoic acid effects morphogenesis of the eye and pathway selection of axons but not the differentiation of the retina in PubMed DOI

Osterhout JA, El-Danaf RN, Nguyen PL, et al. : Birthdate and outgrowth timing predict cellular mechanisms of axon target matching in the developing visual pathway. PubMed DOI PMC

Roberts JM, Vetter ML: From Retina to Stem Cell and Back Again: Memories of a Chromatin Journey. PubMed DOI

Wu S, Chang KC, Goldberg JL: Retinal Cell Fate Specification. PubMed DOI PMC

Wang S, Sengel C, Emerson MM, et al. : A gene regulatory network controls the binary fate decision of rod and bipolar cells in the vertebrate retina. PubMed DOI PMC

Lamb TD: Evolution of phototransduction, vertebrate photoreceptors and retina. PubMed DOI

Varadarajan SG, Huberman AD: Assembly and repair of eye-to-brain connections. PubMed DOI PMC

Sitko AA, Kuwajima T, Mason CA: Eye-specific segregation and differential fasciculation of developing retinal ganglion cell axons in the mouse visual pathway. PubMed DOI PMC

Kuwajima T, Soares CA, Sitko AA, et al. : SoxC Transcription Factors Promote Contralateral Retinal Ganglion Cell Differentiation and Axon Guidance in the Mouse Visual System. PubMed DOI PMC

Zhang C, Kolodkin AL, Wong RO, et al. : Establishing Wiring Specificity in Visual System Circuits: From the Retina to the Brain. PubMed DOI

Schmitt AM, Shi J, Wolf AM, et al. : Wnt-Ryk signalling mediates medial-lateral retinotectal topographic mapping. PubMed DOI

Brunet I, Weinl C, Piper M, et al. : The transcription factor Engrailed-2 guides retinal axons. PubMed DOI PMC

Wizenmann A, Brunet I, Lam J, et al. : Extracellular Engrailed participates in the topographic guidance of retinal axons PubMed DOI PMC

Harris WA: Neural activity and development. PubMed DOI

Harris WA: The effects of eliminating impulse activity on the development of the retinotectal projection in salamanders. PubMed DOI

Pfeiffenberger C, Cutforth T, Woods G, et al. : Ephrin-As and neural activity are required for eye-specific patterning during retinogeniculate mapping. PubMed DOI PMC

Constantine-Paton M, Cline HT, Debski E: Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. PubMed DOI

Constantine-Paton M, Law MI: Eye-specific termination bands in tecta of three-eyed frogs. PubMed DOI

Wilm C, Fritzsch B: Ipsilateral retinofugal projections in a percomorph bony fish: their experimental induction, specificity and maintenance; pp. 286–292. PubMed DOI

Wilm C, Fritzsch B: Ipsilateral retinal projections into the tectum during regeneration of the optic nerve in the cichlid fish PubMed DOI

Fritzsch B, Himstedt W, Crapon de Caprona MD: Visual projections in larval PubMed DOI

Giorgi PP, Van der Loos H: Axons from eyes grafted in PubMed DOI

Scalia F: Synapse formation in the olfactory cortex by regenerating optic axons: ultrastructural evidence for polyspecific chemoaffinity. PubMed DOI

Scalia F, Grant AC, Reyes M, et al. : Functional properties of regenerated optic axons terminating in the primary olfactory cortex. PubMed DOI

Blackiston DJ, Anderson GM, Rahman N, et al. : A novel method for inducing nerve growth via modulation of host resting potential: gap junction-mediated and serotonergic signaling mechanisms. PubMed DOI PMC

Blackiston DJ, Vien K, Levin M: Serotonergic stimulation induces nerve growth and promotes visual learning via posterior eye grafts in a vertebrate model of induced sensory plasticity. PubMed DOI PMC

Penfield WR, Rasmussen TB: The cerebral cortex of man: a clinical study of localization of function.1950. 10.1001/jama.1950.02920160086033 DOI

Woolsey TA, Van der Loos H: The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. PubMed DOI

Renier N, Dominici C, Erzurumlu RS, et al. : A mutant with bilateral whisker to barrel inputs unveils somatosensory mapping rules in the cerebral cortex. PubMed DOI PMC

Iwasato T, Erzurumlu RS: Development of tactile sensory circuits in the CNS. PubMed DOI PMC

Rothschild G, Mizrahi A: Global order and local disorder in brain maps. PubMed DOI

Kole K, Scheenen W, Tiesinga P, et al. : Cellular diversity of the somatosensory cortical map plasticity. PubMed DOI

Kole K, Komuro Y, Provaznik J, et al. : Transcriptional mapping of the primary somatosensory cortex upon sensory deprivation. PubMed DOI PMC

Fritzsch B, Northcutt RG: Cranial and spinal nerve organization in amphioxus and lampreys: evidence for an ancestral craniate pattern. PubMed DOI

Ter-Avetisyan G, Dumoulin A, Herrel A, et al. : Loss of Axon Bifurcation in Mesencephalic Trigeminal Neurons Impairs the Maximal Biting Force in Npr2-Deficient Mice. PubMed DOI PMC

Hernandez-Miranda LR, Müller T, Birchmeier C: The dorsal spinal cord and hindbrain: From developmental mechanisms to functional circuits. PubMed DOI

Brafman D, Willert K: Wnt/β-catenin signaling during early vertebrate neural development. PubMed DOI PMC

Hornbruch A, Ma G, Ballermann MA, et al. : A BMP-mediated transcriptional cascade involving PubMed DOI

Andrews MG, Del Castillo LM, Ochoa-Bolton E, et al. : BMPs direct sensory interneuron identity in the developing spinal cord using signal-specific not morphogenic activities. PubMed DOI PMC

Ma PM, Woolsey TA: Cytoarchitectonic correlates of the vibrissae in the medullary trigeminal complex of the mouse. PubMed DOI

Maklad A, Fritzsch B: Incomplete segregation of endorgan-specific vestibular ganglion cells in mice and rats. PubMed

Vidal PP, Cullen K, Curthoys IS, et al. : The Vestibular System. In DOI

Hinds JW: Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. PubMed DOI

Pierce ET: Time of Origin of Neurons in the Brain Stem of the Mouse. In: PubMed DOI

Fritzsch B: Development of inner ear afferent connections: forming primary neurons and connecting them to the developing sensory epithelia. PubMed DOI PMC

Ma Q, Chen Z, del Barco Barrantes I, et al. : PubMed DOI

Ruben RJ: Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. PubMed

Fritzsch B, Pan N, Jahan I, et al. : Inner ear development: building a spiral ganglion and an organ of Corti out of unspecified ectoderm. PubMed DOI PMC

Fode C, Gradwohl G, Morin X, et al. : The bHLH protein NEUROGENIN 2 is a determination factor for epibranchial placode-derived sensory neurons. PubMed DOI

Maklad A, Fritzsch B: The developmental segregation of posterior crista and saccular vestibular fibers in mice: a carbocyanine tracer study using confocal microscopy. PubMed DOI

Pujol-Martí J, Zecca A, Baudoin JP, et al. : Neuronal birth order identifies a dimorphic sensorineural map. PubMed DOI PMC

Fritzsch B, López-Schier H: Evolution of Polarized Hair Cells in Aquatic Vertebrates and Their Connection to Directionally Sensitive Neurons. In DOI

Maklad A, Kamel S, Wong E, et al. : Development and organization of polarity-specific segregation of primary vestibular afferent fibers in mice. PubMed DOI PMC

Ter-Avetisyan G, Rathjen FG, Schmidt H: Bifurcation of axons from cranial sensory neurons is disabled in the absence of Npr2-induced cGMP signaling. PubMed DOI PMC

Golding JP, Trainor P, Krumlauf R, et al. : Defects in pathfinding by cranial neural crest cells in mice lacking the neuregulin receptor ErbB4. PubMed DOI

Mao Y, Reiprich S, Wegner M, et al. : Targeted deletion of Sox10 by Wnt1-cre defects neuronal migration and projection in the mouse inner ear. PubMed DOI PMC

Fritzsch B, Matei VA, Nichols DH, et al. : PubMed DOI PMC

Fritzsch B, Kersigo J, Yang T, et al. : Neurotrophic Factor Function During Ear Development: Expression Changes Define Critical Phases for Neuronal Viability. In DOI

Gu C, Rodriguez ER, Reimert DV, et al. : Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. PubMed DOI PMC

Morris JK, Maklad A, Hansen LA, et al. : A disorganized innervation of the inner ear persists in the absence of PubMed DOI PMC

Cramer KS, Miko IJ: Eph-ephrin signaling in nervous system development [version 1; peer review: 2 approved]. PubMed DOI PMC

Cowan CA, Yokoyama N, Bianchi LM, et al. : EphB2 guides axons at the midline and is necessary for normal vestibular function. PubMed DOI

Constantine-Paton M: Trajectories of axons in ectopic VIIIth nerves. PubMed DOI

Elliott KL, Fritzsch B: Ear transplantations reveal conservation of inner ear afferent pathfinding cues. PubMed DOI PMC

Gordy C, Straka H, Houston DW, et al. : Transplantation of Ears Provides Insights into Inner Ear Afferent Pathfinding Properties. PubMed DOI PMC

Elliott KL, Houston DW, Fritzsch B: Sensory afferent segregation in three-eared frogs resemble the dominance columns observed in three-eyed frogs. PubMed DOI PMC

Fattal D, Hansen M, Fritzsch B: Aging-Related Balance Impairment and Hearing Loss. DOI

Malmierca MS: Auditory System. DOI

Goodrich LV: Early Development of the Spiral Ganglion. DOI

Fritzsch B, Eberl DF, Beisel KW: The role of bHLH genes in ear development and evolution: revisiting a 10-year-old hypothesis. PubMed DOI PMC

Jahan I, Kersigo J, Pan N, et al. : PubMed DOI PMC

Appler JM, Lu CC, Druckenbrod NR, et al. : Gata3 is a critical regulator of cochlear wiring. PubMed DOI PMC

Coate TM, Spita NA, Zhang KD, et al. : Neuropilin-2/Semaphorin-3F-mediated repulsion promotes inner hair cell innervation by spiral ganglion neurons. PubMed DOI PMC

Zhang KD, Coate TM: Recent advances in the development and function of type II spiral ganglion neurons in the mammalian inner ear. PubMed DOI PMC

Elliott KL, Kersigo J, Pan N, et al. : Spiral Ganglion Neuron Projection Development to the Hindbrain in Mice Lacking Peripheral and/or Central Target Differentiation. PubMed DOI PMC

Maricich SM, Xia A, Mathes EL, et al. : PubMed DOI PMC

Parr BA, Shea MJ, Vassileva G, et al. : Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. PubMed

Yang T, Kersigo J, Wu S, et al. : Prickle1 regulates neurite outgrowth of apical spiral ganglion neurons but not hair cell polarity in the murine cochlea. PubMed DOI PMC

Pataskar A, Jung J, Smialowski P, et al. : NeuroD1 reprograms chromatin and transcription factor landscapes to induce the neuronal program. PubMed DOI PMC

Karmakar K, Narita Y, Fadok J, et al. : PubMed DOI

Fritzsch B, Fariñas I, Reichardt LF: Lack of neurotrophin 3 causes losses of both classes of spiral ganglion neurons in the cochlea in a region-specific fashion. PubMed DOI PMC

Komiya H, Eggermont JJ: Spontaneous firing activity of cortical neurons in adult cats with reorganized tonotopic map following pure-tone trauma. PubMed DOI

Eggermont JJ: Acquired hearing loss and brain plasticity. PubMed DOI

Harrison RV: Biologic Development of the Auditory System From Periphery to Cortex.

de Villers-Sidani E, Merzenich MM: Lifelong plasticity in the rat auditory cortex: basic mechanisms and role of sensory experience. PubMed DOI

Syka J: Plastic changes in the central auditory system after hearing loss, restoration of function, and during learning. PubMed DOI

Liberman MC: Noise-induced and age-related hearing loss: new perspectives and potential therapies [version 1; peer review: 4 approved]. PubMed DOI PMC

Ren W, Aihara E, Lei W, et al. : Transcriptome analyses of taste organoids reveal multiple pathways involved in taste cell generation. PubMed DOI PMC

May OL, Hill DL: Gustatory terminal field organization and developmental plasticity in the nucleus of the solitary tract revealed through triple-fluorescence labeling. PubMed DOI PMC

Vendrell-Llopis N, Yaksi E: Evolutionary conserved brainstem circuits encode category, concentration and mixtures of taste. PubMed DOI PMC

O'Neill P, Mak SS, Fritzsch B, et al. : The amniote paratympanic organ develops from a previously undiscovered sensory placode. PubMed DOI PMC

Okubo T, Pevny LH, Hogan BL: Sox2 is required for development of taste bud sensory cells. PubMed DOI PMC

Barlow LA: Progress and renewal in gustation: new insights into taste bud development. PubMed DOI PMC

Thirumangalathu S, Harlow DE, Driskell AL, et al. : Fate mapping of mammalian embryonic taste bud progenitors. PubMed DOI PMC

Hellard D, Brosenitsch T, Fritzsch B, et al. : Cranial sensory neuron development in the absence of brain-derived neurotrophic factor in BDNF/Bax double null mice. PubMed DOI

Fritzsch B, Pauley S, Matei V, et al. : Mutant mice reveal the molecular and cellular basis for specific sensory connections to inner ear epithelia and primary nuclei of the brain. PubMed DOI PMC

Qian Y, Fritzsch B, Shirasawa S, et al. : Formation of brainstem (nor)adrenergic centers and first-order relay visceral sensory neurons is dependent on homeodomain protein Rnx/Tlx3. PubMed DOI PMC

Poritsky R, Singer M: Intraperitoneal transplants of taste buds in the newt. PubMed DOI

Poritsky RL, Singer M: The fate of taste buds in tongue transplants to the orbit in the urodele, DOI

Travers S, Breza J, Harley J, et al. : Neurons with diverse phenotypes project from the caudal to the rostral nucleus of the solitary tract. PubMed DOI PMC

Herzog LE, Pascual LM, Scott SC, et al. : Interaction of taste and place coding in the hippocampus. PubMed DOI PMC

Birchall M: Tongue transplantation. PubMed DOI

Kulahci Y, Klimczak A, Madajka M, et al. : Long-term survival of composite hemiface/mandible/tongue allografts correlates with multilineage chimerism development in the lymphoid and myeloid compartments of recipients. PubMed DOI

Ma Q, Anderson DJ, Fritzsch B: PubMed DOI PMC

Fritzsch B, Elliott KL, Glover JC: Gaskell revisited: new insights into spinal autonomics necessitate a revised motor neuron nomenclature. PubMed DOI PMC

Lai HC, Seal RP, Johnson JE: Making sense out of spinal cord somatosensory development. PubMed DOI PMC

Frank D, Sela-Donenfeld D: Hindbrain induction and patterning during early vertebrate development. PubMed DOI PMC

Parker HJ, Bronner ME, Krumlauf R: The vertebrate PubMed DOI

Di Bonito M, Studer M, Puelles L: Nuclear derivatives and axonal projections originating from rhombomere 4 in the mouse hindbrain. PubMed DOI PMC

Zecca A, Dyballa S, Voltes A, et al. : The Order and Place of Neuronal Differentiation Establish the Topography of Sensory Projections and the Entry Points within the Hindbrain. PubMed DOI PMC

Altman J, Bayer SA: Development of the cranial nerve ganglia and related nuclei in the rat. PubMed

Altman J, Bayer SA: Development of the brain stem in the rat. III. Thymidine-radiographic study of the time of origin of neurons of the vestibular and auditory nuclei of the upper medulla. PubMed DOI

McCabe KL, Sechrist JW, Bronner-Fraser M: Birth of ophthalmic trigeminal neurons initiates early in the placodal ectoderm. PubMed DOI PMC

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...