Tract-Tracing in Developing Systems and in Postmortem Human Material Using Carbocyanine Dyes

Rapid progress in neurobiology and genetics demands knowledge of fundamental aspects of brain development including the connectivity patterns within developing and adult brains. The primary focus of this chapter is on neuroanatomical tract-tracing using carbocyanine dyes which have several advantages over traditional tracing methods. First utilized for in vitro studies, a major breakthrough in the late 1980s was the demonstration that carbocyanine dyes act as anterograde and retrograde tracers in fixed tissue, eliminating the need for diffusion of tracers in vivo. Moreover, carbocyanine dyes are more efficacious than classical tracing methodologies especially during early stages of development, and consequently have been used to reveal the spatiotemporal patterns of axonal development in different species. Furthermore, the unique properties of the carbocyanine dye tracing method have opened up new avenues for tracing connections in human postmortem specimens. This is a key step in determining the precise connectivity of neural circuits in the human brain, and subsequently to relate this knowledge to pathological cases.

[1]  S. Clarke,et al.  Occipital cortex in man: Organization of callosal connections, related myelo‐ and cytoarchitecture, and putative boundaries of functional visual areas , 1990, The Journal of comparative neurology.

[2]  J. Lichtman,et al.  Multicolor “DiOlistic” Labeling of the Nervous System Using Lipophilic Dye Combinations , 2000, Neuron.

[3]  S. Thanos,et al.  A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. , 1987, Development.

[4]  Colin Blakemore,et al.  Lack of regional specificity for connections formed between thalamus and cortex in coculture , 1991, Nature.

[5]  Successful Silver Impregnation of Degenerating Axons after Long Survivals in the Human Brain , 1980, Journal of neuropathology and experimental neurology.

[6]  Timothy Edward John Behrens,et al.  Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[7]  C. Blakemore,et al.  Activity-dependent Regulation of Synapse and Dendritic Spine Morphology in Developing Barrel Cortex Requires Phospholipase C-β1 Signalling , 2005 .

[8]  N. Tamamaki,et al.  A Procedure for In Situ Hybridization Combined with Retrograde Labeling of Neurons: Application to the Study of Cell Adhesion Molecule Expression in DiI-labeled Rat Pyramidal Neurons , 1997, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[9]  C. Shatz,et al.  Subplate neurons pioneer the first axon pathway from the cerebral cortex. , 1989, Science.

[10]  P. Raymond,et al.  R‐cadherin expression in the developing and adult zebrafish visual system , 1999, The Journal of comparative neurology.

[11]  G. Fishell,et al.  Dispersion of neural progenitors within the germinal zones of the forebrain , 1993, Nature.

[12]  A L Pearlman,et al.  Thalamocortical axons extend along a chondroitin sulfate proteoglycan- enriched pathway coincident with the neocortical subplate and distinct from the efferent path , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  B. Gähwiler,et al.  Selective neurofilament (SMI-32, FNP-7 and N200) expression in subpopulations of layer V pyramidal neurons in vivo and in vitro. , 2004, Cerebral cortex.

[14]  C. Blakemore,et al.  Normal Development of Embryonic Thalamocortical Connectivity in the Absence of Evoked Synaptic Activity , 2002, The Journal of Neuroscience.

[15]  C. Métin,et al.  The Ganglionic Eminence May Be an Intermediate Target for Corticofugal and Thalamocortical Axons , 1996, The Journal of Neuroscience.

[16]  M. G. Honig,et al.  Dil and DiO: versatile fluorescent dyes for neuronal labelling and pathway tracing , 1989, Trends in Neurosciences.

[17]  H. Heinzl,et al.  Carbocyanine Postmortem Neuronal Tracing: Influence of Different Parameters on Tracing Distance and Combination with Immunocytochemistry , 1998, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[18]  H. Kinney,et al.  Anatomic Relationships of the Human Arcuate Nucleus of the Medulla: A Dil‐Labeling Study , 1997, Journal of neuropathology and experimental neurology.

[19]  G. Papadopoulos,et al.  DiI labeling combined with conventional immunocytochemical techniques for correlated light and electron microscopic studies , 1993, Journal of Neuroscience Methods.

[20]  R. Masland,et al.  Photoconversion of some fluorescent markers to a diaminobenzidine product. , 1988, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[21]  H. Kinney,et al.  Anatomic relationships of the human nucleus of the solitary tract in the medulla oblongata: a DiI labeling study , 2003, Autonomic Neuroscience.

[22]  M. G. Honig,et al.  Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures , 1986, The Journal of cell biology.

[23]  Colin Blakemore,et al.  How do thalamic axons find their way to the cortex? , 1995, Trends in Neurosciences.

[24]  Timothy Edward John Behrens,et al.  Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging , 2003, Nature Neuroscience.

[25]  M. Marín‐padilla Structural organization of the human cerebral cortex prior to the appearance of the cortical plate , 2004, Anatomy and Embryology.

[26]  C Blakemore,et al.  Morphology and Growth Patterns of Developing Thalamocortical Axons , 2000, The Journal of Neuroscience.

[27]  S. Clarke,et al.  The Long Distance Effects of Brain Lesions: Visualization of Axonal Pathways and Their Terminations in the Human Brain by the Nauta Method , 1991, Journal of neuropathology and experimental neurology.

[28]  J. Lübke Photoconversion of diaminobenzidine with different fluorescent neuronal markers into a light and electron microscopic dense reaction product , 1993, Microscopy research and technique.

[29]  E J Holborow,et al.  Fading of immunofluorescence during microscopy: a study of the phenomenon and its remedy. , 1982, Journal of immunological methods.

[30]  A. Agmon,et al.  Functional GABAergic Synaptic Connection in Neonatal Mouse Barrel Cortex , 1996, The Journal of Neuroscience.

[31]  J. Rubenstein,et al.  Cortical and thalamic axon pathfinding defects in Tbr1, Gbx2, and Pax6 mutant mice: Evidence that cortical and thalamic axons interact and guide each other , 2002, The Journal of comparative neurology.

[32]  Z. Molnár,et al.  Connections between cells of the internal capsule, thalamus, and cerebral cortex in embryonic rat , 1999, The Journal of comparative neurology.

[33]  F. Valverde,et al.  Dynamics of Cell Migration from the Lateral Ganglionic Eminence in the Rat , 1996, The Journal of Neuroscience.

[34]  Henry Kennedy,et al.  Maturation and connectivity of the visual cortex in monkey is altered by prenatal removal of retinal input , 1989, Nature.

[35]  D F Swaab,et al.  Postmortem anterograde tracing of intrahypothalamic projections of the human dorsomedial nucleus of the hypothalamus , 1998, The Journal of comparative neurology.

[36]  Z. Molnár,et al.  Role of Emx2 in the development of the reciprocal connectivity between cortex and thalamus , 2002, The Journal of comparative neurology.

[37]  M. Marín‐Padilla,et al.  Early prenatal ontogenesis of the cerebral cortex (neocortex) of the cat (Felis domestica). A Golgi study , 2004, Zeitschrift für Anatomie und Entwicklungsgeschichte.

[38]  S. Clarke,et al.  Intrinsic connectivity of human auditory areas: a tracing study with DiI , 2001, The European journal of neuroscience.

[39]  G. Fishell,et al.  Tracking fluorescently labeled neurons in developing brain , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[40]  Afonso C. Silva,et al.  In vivo neuronal tract tracing using manganese‐enhanced magnetic resonance imaging , 1998, Magnetic resonance in medicine.

[41]  G. Paxinos,et al.  Central vagal sensory and motor connections: human embryonic and fetal development , 2004, Autonomic Neuroscience.

[42]  H. Kennedy,et al.  Cell-Cycle Kinetics of Neocortical Precursors Are Influenced by Embryonic Thalamic Axons , 2001, The Journal of Neuroscience.

[43]  H. Bleckmann,et al.  Effect of temperature and calcium on transneuronal diffusion of DiI in fixed brain preparations , 1999, Journal of Neuroscience Methods.

[44]  S. Mcconnell,et al.  Neurotrophin-3 Is Required for Appropriate Establishment of Thalamocortical Connections , 2002, Neuron.

[45]  T. Voigt Development of glial cells in the cerebral wall of ferrets: Direct tracing of their transformation from radial glia into astrocytes , 1989, The Journal of comparative neurology.

[46]  D. Sparks,et al.  Neural tract tracing using Di-I: a review and a new method to make fast Di-I faster in human brain , 2000, Journal of Neuroscience Methods.

[47]  C. Blakemore,et al.  Characterization of nodular neuronal heterotopia in children. , 1999, Brain : a journal of neurology.

[48]  T. Beach,et al.  Retrograde filling of pyramidal neurons in postmortem human cerebral cortex using horseradish peroxidase , 1988, Journal of Neuroscience Methods.

[49]  E. Mugnaini,et al.  Cartwheel neurons of the dorsal cochlear nucleus: A Golgi‐electron microscopic study in rat , 1984, The Journal of comparative neurology.

[50]  S. Thanos,et al.  Retinal ganglion cells resistant to advanced glaucoma: a postmortem study of human retinas with the carbocyanine dye DiI. , 2003, Investigative ophthalmology & visual science.

[51]  H. Kinney,et al.  Reciprocal entorhinal‐hippocampal connections established by human fetal midgestation , 1996, The Journal of comparative neurology.

[52]  L. Bruce,et al.  Electron microscopic differentiation of directly and transneuronally transported DiI and applications for studies of synaptogenesis , 1997, Journal of Neuroscience Methods.

[53]  G. Meyer,et al.  Developmental changes in layer I of the human neocortex during prenatal life: A DiI‐tracing and AChE and NADPH‐d histochemistry study , 1993, The Journal of comparative neurology.

[54]  Jeffrey H. Kordower,et al.  Tracing neuronal connections in postmortem human hippocampal complex with the carbocyanine dye DiI , 1990, Neurobiology of Aging.

[55]  B. Connors,et al.  Thalamocortical responses of mouse somatosensory (barrel) cortexin vitro , 1991, Neuroscience.

[56]  D. Swaab,et al.  Human retinohypothalamic tract as revealed by in vitro postmortem tracing , 1998, The Journal of comparative neurology.

[57]  H. Killackey,et al.  Individual axon morphology and thalamocortical topography in developing rat somatosensory cortex , 1996, The Journal of comparative neurology.

[58]  N Yamamoto,et al.  Stop and Branch Behaviors of Geniculocortical Axons: A Time-Lapse Study in Organotypic Cocultures , 1997, The Journal of Neuroscience.

[59]  Walle J. H. Nauta,et al.  Silver impregnation of degenerating axon terminals in the central nervous system: (1) Technic. (2) Chemical notes. , 1951, Stain technology.

[60]  S. Haber Tracing intrinsic fiber connections in postmortem human brain with WGA-HRP , 1988, Journal of Neuroscience Methods.

[61]  J. Miklossy,et al.  The Long-Distance Effects of Brain Lesions: Visualization of Myelinated Pathways in the Human Brain Using Polarizing and Fluorescence Microscopy , 1991, Journal of neuropathology and experimental neurology.

[62]  B. Finlay,et al.  The early development of thalamocortical and corticothalarnic projections , 1993, The Journal of comparative neurology.

[63]  K. Toyama,et al.  Prenatal development of neural excitation in rat thalamocortical projections studied by optical recording , 2002, Neuroscience.

[64]  L. Heimer,et al.  Combinations of Tracer Techniques, Especially HRP and PHA-L, with Transmitter Identification for Correlated Light and Electron Microscopic Studies , 1989 .

[65]  D. Swaab,et al.  Postmortem tracing reveals the organization of hypothalamic projections of the suprachiasmatic nucleus in the human brain , 1998, The Journal of comparative neurology.

[66]  Vivaldo Moura-Neto,et al.  Cortical radial glial cells in human fetuses: depth-correlated transformation into astrocytes. , 2003, Journal of neurobiology.

[67]  C. Blakemore,et al.  The Role of the First Postmitotic Cortical Cells in the Development of Thalamocortical Innervation in the ReelerMouse , 1998, The Journal of Neuroscience.

[68]  C. Blakemore,et al.  Tangential Networks of Precocious Neurons and Early Axonal Outgrowth in the Embryonic Human Forebrain , 2005, The Journal of Neuroscience.

[69]  R. Bunge,et al.  Human sympathetic preganglionic neurons and motoneurons retrogradely labelled with DiI. , 1998, Journal of the autonomic nervous system.

[70]  T. Fitzgibbon The human fetal retinal nerve fiber layer and optic nerve head: A DiI and DiA tracing study , 1997, Visual Neuroscience.

[71]  C. Métin,et al.  Intermediate Zone Cells Express Calcium-Permeable AMPA Receptors and Establish Close Contact with Growing Axons , 2000, The Journal of Neuroscience.

[72]  C Blakemore,et al.  Mechanisms Underlying the Early Establishment of Thalamocortical Connections in the Rat , 1998, The Journal of Neuroscience.

[73]  Timothy Edward John Behrens,et al.  Characterization and propagation of uncertainty in diffusion‐weighted MR imaging , 2003, Magnetic resonance in medicine.

[74]  R. Hevner Development of Connections in the Human Visual System During Fetal Mid‐Gestation: A DiI‐Tracing Study , 2000, Journal of neuropathology and experimental neurology.