Olfactory relationships of the telencephalon and diencephalon in the rabbit. III. The ipsilateral centrifugal fibers to the olfactory bulbar and retrobulbar formations†
Richard D. Broadwell
Laboratory of Neuropathology and Neuroanatomical Sciences, NINCDS, and Laboratory of Clinical Science, NIMH, National Institutes of Health, Bethesda, Maryland 20014
Search for more papers by this authorDavid M. Jacobowitz
Laboratory of Neuropathology and Neuroanatomical Sciences, NINCDS, and Laboratory of Clinical Science, NIMH, National Institutes of Health, Bethesda, Maryland 20014
Search for more papers by this authorRichard D. Broadwell
Laboratory of Neuropathology and Neuroanatomical Sciences, NINCDS, and Laboratory of Clinical Science, NIMH, National Institutes of Health, Bethesda, Maryland 20014
Search for more papers by this authorDavid M. Jacobowitz
Laboratory of Neuropathology and Neuroanatomical Sciences, NINCDS, and Laboratory of Clinical Science, NIMH, National Institutes of Health, Bethesda, Maryland 20014
Search for more papers by this authorThe results of this study have been presented in part at the eighty-seventh session of the American Association of Anatomists, 1974, and at the fourth and fifth meetings of the Society for Neuroscience, 1974 and 1975.
Abstract
The axoplasmic retrograde transport of horseradish peroxidase (HRP) from axon terminals to their parent cell bodies and histochemical fluorescence microscopy have been used to study the ipsilateral centrifugal fibers to the olfactory bulbs and anterior olfactory nucleus in the rabbit. Focal injections of peroxidase were placed unilaterally into the main or accessory olfactory bulb or into the anterior olfactory nucleus. In animals with injected HRP confined within the main bulb, perikarya retrogradely labeled with the protein in the ipsilateral forebrain were observed in the anterior prepyriform cortex, horizontal limb of the nucleus of the diagonal band, and far lateral preoptic and rostral lateral hypothalamic areas. Brain stem cell groups that contained HRP-positive somata include the locus coeruleus and midbrain dorsal raphe nucleus. Except for the prepyriform cortex, the basal forebrain structures with labeled perikarya correlate well with locations of cell bodies containing acetylcholinesterase and choline acetyltransferase. These somata may represent a cholinergic afferent system to the main olfactory bulb. Peroxidase-labeled cell bodies in the locus coeruleus and midbrain raphe are indicative of noradrenergic and serotonergic innervations respectively of the olfactory bulb. In rabbits in which peroxidase was injected or diffused into the accessory olfactory bulb and anterior olfactory nucleus, HRP-positive somata were identified in the prepyriform cortex bilaterally, the horizontal limb of the diagonal band nucleus, lateral hypothalamic region, nucleus of the lateral olfactory tract, corticomedial complex of the amygdala, mitral and tufted cell layers of the ipsilateral main olfactory bulb, locus coeruleus, and the midbrain raphe. Evidence for centrifugal fibers to the accessory olfactory bulb from the corticomedial complex of the amygdala, locus coeruleus, and possibly the nucleus of the lateral olfactory tract and midbrain raphe is discussed. A similar distribution of labeled perikarya in the forebrain and brain stem was seen in rats in which peroxidase injected into the main olfactory bulb had spread into the accessory bulb and anterior olfactory nucleus.
Histochemical fluorescence microscopy of the main and accessory olfactory bulbs in the rabbit and rat revealed fine caliber, green fluorescent fibers and varicosities predominantly in the granule cell layer and less so among cells in the glomerular layer. In sections through the root of the main olfactory bulb, a similar fluorescence was seen in the deep half of the plexiform layer of the pars externa of the anterior olfactory nucleus. These fluorescent fibers likely represent the noradrenergic innervation of the olfactory bulbar and retrobulbar formations. A fluorescent yellow hue was observed in the glomerular layer of the main bulb and may signify a serotonergic innervation of this lamina.
The results of this study provide continued support for the existence of main and accessory olfactory systems and offer greater insight into the organization of the olfactory brain and the interrelationship of the hypothalamus and olfaction.
Literature Cited
- Allison, A. C. 1953a The structure of the olfactory bulb and its relationship to the olfactory pathways in the rabbit and the rat. J. Comp. Neur., 98: 309–355.
- Allison, A. C. 1953b The morphology of the olfactory system in the vertebrates. Biol. Rev., 28: 195–244.
- Andén, N. E., A., Dahlström, K. Fuxe, K. Larsson, L. Olsson and U. Ungerstedt 1966 Ascending monoamine neurons to the telencephalon and diencephalon. Acta Physiol. Scand., 67: 313–326.
- Barber, P. C., and P. Field 1975 Autoradiographic demonstration of afferent connections of the accessory olfactory bulb in the mouse. Brain Res., 85: 201–203.
- Barber, P. C., and G. Raisman 1974 An autoradiographic investigation of the projection of the vomeronasal organ to the accessory olfactory bulb in the mouse. Brain Res., 81: 21–30.
- Bloom, F. E., E., Costa and G. C. Salmoiragh. 1964 Analysis of individual rabbit olfactory bulb neuron responses to the microelectrophoresis of accetylcholine, norepinepherine, and serotonin synergists and antagonists. J. Pharmacol. Exptl. Therap., 146: 16–23.
- Broadwell, R. D. 1974 Olfactory relationships of the telencephalon in the rabbit as studied by the autoradiographic anterograde and horseradish peroxidase retrograde intraaxonal protein transport tracing techniques. Anat. Rec., 178: 316–317.
- Broadwell, R. D. 1975a Olfactory relationships of the telencephalon and diencephalon in the rabbit. 1. An autoradiographic study of the efferent connections of the main and accessory olfactory bulbs. J. Comp. Neur., 16: 329–346.
- Broadwell, R. D. 1975b Olfactory relationships of the telencephalon and diencephalon in the rabbit. II. An autoradiographic and horseradish peroxidase study of the efferent connections of the anterior olfactory nucleus. J. Comp. Neur., 164: 389–410.
- Broadwell, R. D., and M. W. Brightman 1976 Entry of peroxidase into neurons of the central and peripheral nervous systems from extracerebral and cerebral blood. J. Comp. Neur., 166: 257–284.
- Bunt, A. H., A. E., Hendrickson, J. S. Lund, R. D. Lund and A. F. Fuchs 1975 Monkey retinal ganglion cells: Morpho-metric analysis and of axonal projections with a consideration of the peroxidase technique. J. Comp. Neur., 164: 265–286.
- Cajal, S. R. 1890 Origen y terminación de las fibras nervioosas olfactorias. Gaz. sanit. de Barcelona.
- Cajal, S. R. 1901 La corteza olfactivo del hombre y mamiferos. Trab. d. lab. de invest. biol. Univ. de Madrid, 1 (p. 1).
- Cajal, S. R. 1955 Studies on the Cerebral Cortex. Translated by L. Kraft, Lloyd-Luke, London.
- Carlsson, A., B., Falck and N. A. Hillarp 1962 Cellular localization of brain monoamines. Acta. Physiol. Sand. (Suppl.), 196: 1–28.
- Carreras, M., D., Mancia and M. Mancia 1967 Centrifugal control of the olfactory bulb as revealed by induced DC potential changes. Brain Res., 6: 548–560.
- Conrad, L. C., C. M., Leonard and D. Pfaff 1974 Connections of the median and dorsal raphe nuclei in the rat. An autoradiographic and degeneration study. J. Comp. Neur., 156: 179–206.
- Cragg, B. G. 1962 Centrifugal fibres to the retina and olfactory bulb, and composition of the supraoptic commissures in the rabbit. Exp. Neurol., 5: 406–427.
- Crosby, E. C., and T. Humphrey 1939 Studies on the vertebrate telencephalon. I. The nuclear configuration of the olfactory and accessory olfactory formations and of the nucleus olfactorious anterior of certain reptiles, birds, and mammals. J. Comp. Neur., 71: 121–213.
- Dahlström, A., K., Fuxe, L. Olsson and U. Ungerstedt 1965 On the distribution and possible function of monoamine nerve terminals in the olfactory bulb of the rabbit. Life Sci., 4: 2071–2074.
- Daval, G., and J. Leveteau 1974 Electrophysiological studies of centrifugal and centripetal connections of the anterior olfactory nucleus. Brain Res., 78: 345–410.
- Dennis, B. J., and D. I. B. Kerr 1968 An evoked potential study of centripetal and centrifugal connections of the olfactory bulb in the cat. Brain Res., 11: 373–346.
- Dennis, B. J., and D. I. B. Kerr 1975 Olfactory bulb connections with basal rhinencephalon in the ferret: an evoked potential and neuroanatomical study. J. Comp. Neur., 154: 129–148.
-
De Olmos, J. S.
1972
The amygdaloid projection field in the rat as studied with the cupricsilver method. In:
The Neurobiology of the Amygdala.
Basil E. Eleftheriou, ed.
Plenum Publ. Co.,
New York,
pp. 145–204.
10.1007/978-1-4615-8987-7_7 Google Scholar
- De Olmos, J. S., and W. R. Ingram 1972 The projection field of the stria terminalis in the rat brain. An experimental study. J. Comp. Neur., 146: 303–334.
- Divac, I. 1975 Magnocellular nuclei of the basal forebrain project to neocortex, brain stem, and olfactory bulb. Review of some functional correlates. Brain Res., 93: 385–398.
-
Estes, R. D.
1973
The role of the vomeronasal organ in mammalian reproduction.
Mammalia,
36:
315–341.
10.1515/mamm.1972.36.3.315 Google Scholar
- Falck, B. 1962 Observations on the possibilities for the cellular localization of monoamines with a fiuorescence method. Acta Physiol. Scand. (Suppl. 147). 56: 1–25.
- Getchell, T. V., and G. M. Shepherd 1975 Shortaxon cells in the olfactory bulb: dendrodendritic synaptic interactions. J. Physiol., 251: 523–548.
- Golgi, C. 1875 Sulla fina struttura dei bulbi olfactorii. Reggio-Emilia.
- Graham, R. C., and M. J. Karnovsky 1966 The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J. Histochem. Cytochem., 14: 291–302.
- Haberly, L. B., and J. L. Price 1975 Afferent connections of the olfactory cortex. Soc. Neurosci., 1: 14 (abstract).
- Halperin, M. 1973 Olfactory bulb and accessory bulb projections in the snake, Thranophis sirtalis. Anat. Rec., 175: 337.
- Heimer, L. 1968 Synaptic distribution of centripetal and centrifugal nerve fibers in the olfactory system of the rat. An experimental anatomical study. J. Anat. (London), 103: 413–432.
- Heimer, L. 1969 The secondary olfactory connections in mammals, reptiles and sharks. Ann. N. Y. Acad. Sci., 167: 129–146.
- Heimer, L. 1972 The olfactory connections of the diencephalon in the rat. Brain, Behav. and Evol., 6: 484–523.
- Heimer, L., and R. D. Wilson 1975 The subcortical projections of the allocortex: Similarities in the neural associations of the hippocampus, the piriform cortex, and the neocortex. In: Golgi Centennial Symposium Proc. M. Santini, Raven Press, New York, pp. 177–193.
- Hinds, J. W. 1970 Reciprocal and serial dendrodendritic synapses in the glomerular layer of the rat olfactory bulb. Brain Res., 17: 530–534.
- Hjorth-Simonsen, A. 1972 Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata. J. Comp. Neur., 146: 219–232.
- Hökfelt, T., N., Halász, A. Ljungdahl, O. Johansson, M. Goldstein and D. Park 1975 Histochemical support for a dopaminergic mechanism in the dendrites of certain periglomerular cells in the rat olfactory bulb. Neurosci. Letters, 1: 85–90.
- Jacobowitz, D. M. 1975 Fluorescence microscopic mapping of CNS morepinephrine systems in rat forebrain. In: Anatomical Neuroendocrinology. W. E. Stumpf and L. D. Grant, eds. Karger, Basal, pp. 368–380.
- Jacobowitz, D. M., and M. Palkovits 1974 Topographic atlas of catecholamine and acetylcholinesterase-containing neurons in the rat brain: I. Forebrain (Telencephalon, Diencephalon). J. Comp. Neur., 157: 13–28.
- Kerr, D. I. B., and K. E. Hagbarch 1955 An investigation of olfactory centrifugal system. J. Neurophysiol., 18: 362–374.
- Krettek, J. E., and J. L. Price 1974 Connection of the amygdala with the bed nucleus of the stria terminalis and the hypothalamus in the rat and cat. Soc. Neurosci., 4th Annual Meeting. Abstract book, p. 243.
- Kristensson, K., and Y. Olsson 1974 Retrograde transport of horseradish peroxidase in transected axons. 1. Time relationships between transport and induction of chromatolysis. Brain Res., 79: 101–109.
- Land, L. J., and G. M. Shepherd 1974 Autoradiographic analysis of olfactory receptor projections in the rabbit. Brain Res., 70: 506–510.
- Leonard, C. M., and J. W. Scott 1971 Origin and distribution of the amygdalofugal pathways in the rat. An experimental neuroanatomical study. J. Comp. Neur., 141: 313–330.
- Lohman, A. H. M. 1963 The anterior olfactory lobe of the guinea pig. A descriptive and experimental anatomical study. Acta Anat. (suppl. 49), 53: 1–109.
- Lohman, A. H. M., and G. M. Mentink 1969 The lateral olfactory tract, the anterior commissure, and the cells of the olfactory bulb. Brain Res., 12: 396–413.
- Lundberg, P. O. 1960 Cortico-hypothalamic connections in the rabbit. Acta Physiol. Scand. (Suppl. 171), 49: 1–84.
- Mancia, M., J. D., Green and R. Von Baumgarten 1962 Reticular control of single neurons in the olfactory bulb. Arch. Ital. Biol., 100: 463–475.
- McCotter, R. E. 1912 The connexions of the vomeronasal nerves with the accessory olfactory bulb in the opossum and other mammals. Anat. Rec., 6: 299–318.
- McLennan, H. 1971 The pharmacology of inhibition of mitral cells in the olfactory bulb. Brain Res., 24: 177–184.
- Miliaressis, E., N. B., Thoa, Y. Tizabi and D. M. Jacobowitz 1975 Catecholamine concentration of discrete brain areas following self-stimulation in the ventromedial tegmentum of the rat. Brain Res., 100: 142–147.
- Millhouse, O. E. 1969 A Golgi study of the descending medial forebrain bundle. Brain Res., 15: 341–363.
- Nicoll, R. A. 1969 Inhibitory mechanisms in the rabbit olfactory bulb: dendrodendritic mechanisms. Brain Res., 14: 157–172.
- Nicoll, R. A. 1970 Identification of tufted cells in the olfactory bulb. Nature, 227: 623–625.
- Nicoll, R. A. 1971 Pharmacological evidence for GABA as the transmitter in granule cell inhibition in the olfactory bulb. Brain Res., 35: 137–149.
- Palkovits, M., J. M., Saavedra, R. M. Kobayashi and M. B. Brownstein 1974 Choline acetyltransferase content of limbic nuclei of the rat. Brain Res., 79: 443–450.
- Phillips, C. G., T. P. S., Powell and G. M. Shepherd 1963 Responses of mitral cells to stimulation of the lateral olfactory tract in the rabbit. J. Physiol. (London), 168: 65–88.
- Pickel, V. M., M., Segal and F. E. Bloom 1974 A radioautographic study of the efferent pathways of the nucleus locus coeruleus. J. Comp. Neur., 155: 15–42.
- Pinching, A. J., and T. P. S. Powell 1971 The neuropil of the glomeruli of the olfactory bulb. J. Cell Sci., 9: 347–377.
- Pinching, A. J., and T. P. S. Powell 1972 The termination of centrifugal fibers in the glomerular layer of the olfactory bulb. J. Cell Sci., 10: 621–635.
- Powell, T. P. S., W. M., Cowan and G. Raisman 1965 The central olfactory connections. J. Anat., 99: 791–813.
- Powers, J. B., and S. Winans 1975 Vomeronasal organ: critical role in mediating sexual behavior of the male hamster. Sci., 187: 961–963.
- Price, J. L. 1968 The termination of centrifugal fibers in the olfactory bulb. Brain Res., 7: 483–486.
-
Price, J. L.
1969
The origin of the centrifugal fibers to the olfactory bulb.
Brain Res.,
14:
542–545.
10.1016/0006-8993(69)90135-8 Google Scholar
- Price, J. L. 1973 An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex. J. Comp. Neur., 150: 87–108.
- Price, J. L., and T. P. S. Powell 1970a An electron microscopic study of the termination of the afferent fibres to the olfactory bulb from the cerebral hemisphere. J. Cell. Sci., 7: 157–187.
- Price, J. L., and T. P. S. Powell 1970b An experimental study of the origin and the course of the centrifugal fibres to the olfactory bulb in the rat. J. Anat. (London), 107: 215–237.
- Price, J. L., and T. P. S. Powell 1970c The afferent connections of the nucleus of the horizontal limb of the diagonal band. J. Anat. (London), 107: 239–256.
- Raisman, G. 1972 An experimental study of the projection of the amygdala to the accessory olfactory bulb and its relationship to the concept of a dual olfactory system. Exp. Brain Res., 14: 395–408.
- Rall, W., and G. M. Shepherd 1968 Theoretical reconstruction of field potential and dendrodendritic synaptic interactions in olfactory bulb. J. Neurophysiol., 31: 884–915.
- Rall, W., G. M., Shepherd, T. S. Reese and M. W. Brightman 1966 Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exptl. Neurol., 14: 44–56.
- Reese, T. S., and M. W. Brightman 1970 Olfactory surface and central olfactory connections in some vertebrates. In: Ciba Found. Symp. Taste and Smell in Vertebrates. G. E. W. Wolstenholme and J. Knight, eds. Churchill, London, pp. 115–149.
- Reese, T. S., and G. M. Shepherd 1972 Dendrodendritic synapses in the central nervous system. In: Structure and function of synapses. G. D. Pappas and D. P. Purpura, eds. Raven, New York, pp. 121–136.
- Scalia, F. 1972 The projection of the accessory olfactory bulb in the frog. Brain Res., 36: 409–411.
- Scalia, F., and S. Winans 1975 The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J. Comp. Neur., 161: 31–55.
- Scott, J. W., and B. R. Chafin 1975 Origin of olfactory projections to lateral hypothalamus and nuclei gemini of the rat. Brain Res., 88: 64–68.
- Scott, J. W., and C. M. Leonard 1971 The olfactory connections of the lateral hypothalamus in the rat, mouse and hamster. J. Comp. Neur., 141: 331–344.
- Shepherd, G. M. 1963a Responses of mitral cells to olfactory nerve volleys in the rabbit. J. Physiol. (London), 168: 89–100.
- Shepherd, G. M. 1963a Neuronal systems controlling mitral cell excitability. J. Physiol. (London), 168: 101–117.
- Sherlock, D. A., P. M., Field and G. Raisman 1974 Retrograde transport of horseradish peroxidase in the magnocellular neurosecretory system of the rat. Brain Res., 88: 403–414.
- Shute, C. C. D., and P. R. Lewis 1967 The ascending cholinergic reticular system: Neocortical, olfactory and subcortical projections. Brain, 90: 497–522.
- Swanson, L. W., and B. K. Hartman 1975 The central adrenergic system. An immunofluorescence of the location of cell bodies and their efferent connections in the rat utilizing dopamine-B-hydroxylase as a marker. J. Comp. Neur., 163: 467–506.
- Ungerstedt, U. 1971 Sterotaxic mapping of the monoamine pathways in the rat brain. Acta Physiol. Scand., (Suppl.) 367: 1–48.
-
Valverde, F.
1965
Studies on the Piriform Lobe.
Harvard Univ. Press,
Cambridge, Mass.
10.4159/harvard.9780674864559 Google Scholar
- Valverde, H. P. M. 1969 The anterior commissure of the rabbit. Acta Anatomica, (Suppl. 74), 57: 1–112.
- Van Gehuchten, A., and I. Martin 1891 Le bulbe olfactif chez quelques mammifères. La Cellule, 7: 205–237.
- White, E. L. 1972 Synaptic organization in the olfactory glomerulus of the mouse. Brain Res., 37: 69–80.
- White, E. L. 1973 Synaptic organization of the mammalian olfactory glomerulus: new findings including an intraspecific variation. Brain Res., 60: 299–313.
- Winans, S. S., and F. Scalia 1970 Amygdaloid nucleus: new afferent input from the vomeronasal organ. Science, 170: 330–332.
- Willey, T. J. 1973 The ultrastructure of the cat olfactory bulb. J. Comp. Neur., 152: 211–232.
- Winkler, C. 1918 On the olfactory tract in the rabbit. Opera omnia Haarlem: F. Bohm, 5: 397–413.
- Young, M. W. 1936 The nuclear pattern and fiber connections of the non-cortical centers of the telencephalon in the rabbit. J. Comp. Neur., 65: 295–401.