Topographic organization of tufted cell axonal projections in the hamster main olfactory bulb: An intrabulbar associational system

The organization of intrinsic axonal projections of principal neurons in the main olfactory bulb (MOB) was studied in hamsters by using wheat germ agglutinin‐horseradish peroxidase (WGA‐HRP) and fluorescent dyes. Punctate injections of either WGA‐HRP or fast blue (FB) that are restricted to small sectors on one side of the MOB produce comparably restricted fields of retrograde labeling on the opposite side. Label is found predominantly in superficially situated (middle and external) tufted cells that lie near and at the border between the external plexiform and glomerular layers. Few of the deeper middle tufted, internal tufted, or mitral cells and no external tufted cells that lie in the superficial two‐thirds of the glomerular layer are labeled in regions remote to the injection site. Anterograde transport of WGA‐HRP from the injection site labels axons that travel dorsally and ventrally in restricted bands through the internal plexiform layer and then terminate within this layer in the punctate sector on the opposite side that contains retrogradely labeled neurons. Such reciprocal projections between opposing regions of the medial and lateral sides of the MOB are found at all rostrocaudal and dorsoventral levels. When punctate injections of FB into the MOB are paired with restricted injections of a second fluorescent tracer (nuclear yellow or diamidino yellow dihydrochloride) into the appropriate sector of pars externa (pE) of the anterior olfactory nucleus, the punctate region of remote retrogradely labeled principal neurons is embedded within a topographically restricted longitudinal wedge of retrogradely labeled mitral and tufted cells that project extrinsically to or through pE. However, extremely few of these neurons are double‐retrogradely labeled. The results reveal the existence of an intrabulbar associational system in which principal neurons engage in point‐to‐point, reciprocal projections between opposing regions of the medial and lateral MOB. Moreover, the results indicate that this associational system largely arises from superficially situated tufted cells distinct from those that support bulbofugal projections into the topographically organized interbulbar commissural system via pE.

[1]  G M Shepherd,et al.  Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. , 1966, Experimental neurology.

[2]  T. Powell,et al.  The synaptology of the granule cells of the olfactory bulb. , 1970, Journal of cell science.

[3]  T. Powell,et al.  The neuron types of the glomerular layer of the olfactory bulb. , 1971, Journal of cell science.

[4]  T. Powell,et al.  The neuropil of the glomeruli of the olfactory bulb. , 1971, Journal of cell science.

[5]  R. Nicoll Pharmacological evidence for GABA as the transmitter in granule cell inhibition in the olfactory bulb. , 1971, Brain research.

[6]  T. Powell,et al.  The neuropil of the periglomerular region of the olfactory bulb. , 1971, Journal of cell science.

[7]  Gordon M. Shephero Physiological evidence for dendrodendritic synaptic interactions in the rabbit's olfactory glomerulus , 1971 .

[8]  L. J. Land Localized projection of olfactory nerves to rabbit olfactory bulb. , 1973, Brain research.

[9]  W J Freeman,et al.  Topographic organization of primary olfactory nerve in cat and rabbit as shown by evoked potentials. , 1974, Electroencephalography and clinical neurophysiology.

[10]  W J Freeman,et al.  Stability characteristics of positive feedback in a neural population. , 1974, IEEE transactions on bio-medical engineering.

[11]  W J Freeman,et al.  Relation of glomerular neuronal activity to glomerular transmission attenuation. , 1974, Brain research.

[12]  G. Shepherd,et al.  Autoradiographic analysis of olfactory receptor projections in the rabbit. , 1974, Brain research.

[13]  G. Shepherd,et al.  Short‐axon cells in the olfactory bulb: dendrodendritic synaptic interactions. , 1975, The Journal of physiology.

[14]  G. Shepherd,et al.  Synaptic actions on mitral and tufted cells elicited by olfactory nerve volleys in the rabbit. , 1975, The Journal of physiology.

[15]  G. Shepherd,et al.  Olfactory stimulation with controlled and monitored step pulses of odor , 1975, Brain Research.

[16]  F. Macrides 3 – Olfactory Influences on Neuroendocrine Function in Mammals , 1976 .

[17]  M. Devor Fiber trajectories of olfactory bulb efferents in the hamster , 1976, The Journal of comparative neurology.

[18]  W. C. Hall,et al.  Efferent projections of the main and the accessory olfactory bulb in the tree shrew (Tupaia glis) , 1977, The Journal of comparative neurology.

[19]  Dynamic Aspects of Central Olfactory Processing , 1977 .

[20]  James E. Vaughn,et al.  Glutamate decarboxylase localization in neurons of the olfactory bulb , 1977, Brain Research.

[21]  L. C. Skeen Odor-induced patterns of deoxyglucose consumption in the olfactory bulb of the tree shrew,Tupaia glis , 1977, Brain Research.

[22]  Lewis B. Haberly,et al.  The axonal projection patterns of the mitral and tufted cells of the olfactory bulb in the rat , 1977, Brain Research.

[23]  R. M. Costanzo,et al.  Spatially organized projections of hamster olfactory nerves , 1978, Brain Research.

[24]  F. Macrides,et al.  Efferents and centrifugal afferents of the main and accessory olfactory bulbs in the hamster , 1978, Brain Research Bulletin.

[25]  L. Heimer,et al.  The afferent connections of the main and the accessory olfactory bulb formations in the rat: An experimental HRP‐study , 1978, The Journal of comparative neurology.

[26]  M. Mesulam,et al.  THE JOURNAL OF HISTOCHEMISTRY AND CYTOCHEMISTRY , 2005 .

[27]  L. Haberly,et al.  Association and commissural fiber systems of the olfactory cortex of the rat II. Systems originating in the olfactory peduncle , 1978, The Journal of comparative neurology.

[28]  L. Haberly,et al.  Association and commissural fiber systems of the olfactory cortex of the rat. I. Systems originating in the piriform cortex and adjacent areas , 1978, The Journal of comparative neurology.

[29]  F. Macrides,et al.  Laminar distributions of interneurons in the main olfactory bulb of the adult hamster , 1978, Brain Research Bulletin.

[30]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[31]  G. Shepherd,et al.  Functional organization of rat olfactory bulb analysed by the 2‐deoxyglucose method , 1979, The Journal of comparative neurology.

[32]  W. Nauta,et al.  The organization of the brain. , 1979, Scientific American.

[33]  N. Onoda,et al.  Depth distribution of temporal firing patterns in olfactory bulb related to air-intake cycles. , 1980, Journal of neurophysiology.

[34]  M. Mesulam,et al.  Additional factors influencing sensitivity in the tetramethyl benzidine method for horseradish peroxidase neurohistochemistry. , 1980, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[35]  J. W. Scott,et al.  The organization of projections from the olfactory bulb to the piriform cortex and olfactory tubercle in the rat , 1980, The Journal of comparative neurology.

[36]  R. Nicoll,et al.  Substance P as a transmitter candidate. , 1980, Annual review of neuroscience.

[37]  R. M. Costanzo,et al.  Receptive fields of second-order neurons in the olfactory bulb of the hamster , 1980, The Journal of general physiology.

[38]  L. Astic,et al.  Spatial distribution of [14C]2-deoxyglucose uptake in the olfactory bulbs of rats stimulated with two different odours , 1980, Brain Research.

[39]  P. Petrusz,et al.  The immunocytochemical localization of enkephalin in the central nervous system of the rat , 1981, The Journal of comparative neurology.

[40]  T. Hökfelt,et al.  Immunohistochemical identification of two types of dopamine neuron in the rat olfactory bulb as seen by serial sectioning , 1981, Journal of neurocytology.

[41]  W. R. Adey The synaptic organization of the brain. 2nd edn. , 1981 .

[42]  F. Macrides,et al.  The organization of centrifugal projections from the anterior olfactory nucleus, ventral hippocampal rudiment, and piriform cortex to the main olfactory bulb in the hamster: An autoradiographic study , 1981, The Journal of comparative neurology.

[43]  M. T. Shipley A simple, low cost hydraulic pressure device for making microinjections in the brain , 1982, Brain Research Bulletin.

[44]  F. Macrides,et al.  Localization of methionine‐enkephalin, substance P, and somatostatin immunoreactivities in the main olfactory bulb of the hamster , 1982, The Journal of comparative neurology.

[45]  M. T. Shipley,et al.  Insular cortex projection to the nucleus of the solitary tract and brainstem visceromotor regions in the mouse , 1982, Brain Research Bulletin.

[46]  F. Macrides,et al.  Laminar organization of mitral and tufted cells in the main olfactory bulb of the adult hamster , 1982, The Journal of comparative neurology.

[47]  M. Luskin,et al.  The distribution of axon collaterals from the olfactory bulb and the nucleus of the horizontal limb of the diagonal band to the olfactory cortex, demonstrated by double retrograde labeling techniques , 1982, The Journal of comparative neurology.

[48]  F. Macrides,et al.  Ultrastructural identification of substance P immunoreactive neurons in the main olfactory bulb of the hamster , 1982, Neuroscience.

[49]  H. Karten,et al.  Distribution of enkephalin-like immunoreactivity in the rat main olfactory bulb , 1982, Neuroscience.

[50]  E Orona,et al.  Different granule cell populations innervate superficial and deep regions of the external plexiform layer in rat olfactory bulb , 1983, The Journal of comparative neurology.

[51]  S. P. Schneider,et al.  Orthodromic response properties of rat olfactory bulb mitral and tufted cells correlate with their projection patterns. , 1983, Journal of neurophysiology.

[52]  F. Macrides,et al.  Tyrosine hydroxylase immunoreactive neurons and fibers in the olfactory system of the hamster , 1983 .

[53]  K Kishi,et al.  Distribution of dendrites of mitral, displaced mitral, tufted, and granule cells in the rabbit olfactory bulb , 1983, The Journal of comparative neurology.

[54]  H. Swadlow Efferent systems of primary visual cortex: A review of structure and function , 1983, Brain Research Reviews.

[55]  M. Luskin,et al.  The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb , 1983, The Journal of comparative neurology.

[56]  T. Joh,et al.  Transneuronal regulation of tyrosine hydroxylase expression in olfactory bulb of mouse and rat , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  F. Macrides,et al.  Topographic organization of connections between the main olfactory bulb and pars externa of the anterior olfactory nucleus in the hamster , 1984, The Journal of comparative neurology.

[58]  K Kishi,et al.  Distribution of local axon collaterals of mitral, displaced mitral, and tufted cells in the rabbit olfactory bulb , 1984, The Journal of comparative neurology.

[59]  F. Macrides,et al.  Substance P and catecholaminergic expression in neurons of the hamster main olfactory bulb , 1984, The Journal of comparative neurology.

[60]  W. Oertel,et al.  Immunocytochemical localization of GABA neurons and dopamine neurons in the rat main and accessory olfactory bulbs , 1984, Neuroscience Letters.

[61]  J M Bower,et al.  Analysis of association fiber system in piriform cortex with intracellular recording and staining techniques. , 1984, Journal of neurophysiology.

[62]  E Orona,et al.  Dendritic and axonal organization of mitral and tufted cells in the rat olfactory bulb , 1984, The Journal of comparative neurology.

[63]  F. Macrides,et al.  Evidence for morphologically, neurochemically and functionally heterogeneous classes of mitral and tufted cells in the olfactory bulb , 1985 .