The Olfactory Cortex and the Ventral Striatum

  • Lennart Heimer


The first part of the paper deals with the relations between the olfactory bulb and the olfactory cortex, represented by the rat and to a lesser extent the rhesus monkey. The second part addresses itself to the olfactory tubercle and its relation to the olfactory system on the one hand, and to the basal ganglia on the other. The discussion related to the second part is to a certain extent supported by recently obtained data, that are either in press or in the process of being prepared for publication. It is also somewhat theoretical. A speculative approach, however, may be justified in a volume commemorating James Papez, especially if it serves to focus attention on a poorly understood area of the basal forebrain. The reference to James Papez is appropriate also from another point of view. Part of our presentation pertains to the concept of the ventral strio-pallidal system, and although this concept is not directly comparable to Papez’s notion of the “motor olfactory striatum” (Papez, 1929), we have no doubt been inspired by his insight and imagination.


Olfactory Bulb Ventral Striatum Olfactory Tubercle Olfactory Cortex Main Olfactory Bulb 


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  1. ADEY, W.R. An experimental study of the central olfactory connections in a marsupial (trichosurus vulpecula). Brain, 1955, 76, 511–550.Google Scholar
  2. ALLEN, W.F. Effects of ablating frontal lobes, hippocampi, and occipito-parieto-temporal (excepting pyriform areas) lobes on positive and negative olfactory conditioned reflexes. American Journal of Physiology, 1940, 128, 754–771.Google Scholar
  3. ALLISON, A.C. The morphology of the olfactory system in the vertebrates, Biological Review, 1955a, 28, 195–244.Google Scholar
  4. ALLISON, A.C. The structure of the olfactory bulb and its relationship to the olfactory pathways in the rabbit and the rat. Journal of Comparative Neurology, 1955, 98, 509–555.Google Scholar
  5. BECCARI, N. II lobo parolfattoro nei mammiferi. Archives of Italian Anatomy and Embryology, 1910, 9, 175–220.Google Scholar
  6. BECCARI, M. La sostanza perforata anteriore e i suoi rapporti colrinencefalo nel cerbello dellfuomo. Archives of Italian Anatomy and Embryology, 1911, 10, 261–528.Google Scholar
  7. BEN J AM IM, RJ, and AKERT, K. Cortical and thalamic areas involved in taste discrimination in the albino rat. Journal of Comparative Neurology, 1959, 111, 251–259.Google Scholar
  8. BENJAMIN, R.M. and JACKSON, J.C, Unit discharges in -mediodorsal nucleus of the squirrel monkey evoked by electrical stimulation of the olfactory bulb. Brain Research, 1974, 75, 181–191.PubMedGoogle Scholar
  9. BIEDENBACH, M.A, and STEVENS, C.F, Synaptic organization of cat olfactory cortex as revealed by intracellular recording, Journal of Neurophysiology, 1969, 52, 204–214.Google Scholar
  10. CALLEJA, C. (Ed.). La region olfatoria del cerebro. Madrid: Moya, 1893.Google Scholar
  11. CLARK, W.E.L. and MEYER, M. The terminal connections of the olfactory tract in the rabbit. Brain, 1947, 70, 504–328.Google Scholar
  12. CONRAD, L.C. and PFAFF, D.W. Efferents from medial basal forebrain and hypothalamus in the rat, I. An autoradiographic study of the medial preoptic area. Journal of Comparative Neurology, 1976, 169, 185–219.PubMedGoogle Scholar
  13. CONRAD, L.C. PFAFF, D.W. Efferents from medial basal forebrain and hypothalamus in the rat. II, An autoradiographic study of the anterior hypothalamus. Journal of Comparative Neurology, 1976, 169, 221–261.PubMedGoogle Scholar
  14. COWAN, W.M. Anterograde and retrograde transneuronal degeneration in the central and peripheral nervous systems. In W.J.H, Nauta and S.O.E. Ebbesson (Eds.) Contemporary Research Methods in Neuroanatomy. New York: Springer, 1970, 217–251.Google Scholar
  15. COWAN, W.M, and POWELL, T.P. A note on terminal degeneration in the hypothalamus, Journal of Anatomy, 1956, 90, 188–192.PubMedGoogle Scholar
  16. COWAN, W.M., RAISMAN, G, and POWELL, T.P.S. The connections of the amygdala. Journal of Neurology, Neurosurgery and Psychiatry, 1965, 28, 137–151.Google Scholar
  17. CRAGG, B.G. Responses of the hippocampus to stimulation of the olfactory bulb and of various afferent nerves in five mammals. Experimental Neurology, 1960, 2, 547–572.PubMedGoogle Scholar
  18. CRAGG, B.G. Olfactory and other afferent connections of the hippocampus in the rabbit, rat, and cat. Experimental Neurology, 1961, 3, 588–600.PubMedGoogle Scholar
  19. CRAGG, B.G. Centrifugal fibers to the retina and olfactory bulb, and composition of the supraoptic commissures in the rabbit. Experimental Neurology, 1962, 5, 406–427.Google Scholar
  20. CREPS, E.S. Time of neuron origin in preoptic and septal areas of the mouse; an autoradiographic study. Journal of Comparative Neurology, 1974, 157, 161–243.PubMedGoogle Scholar
  21. CROSBY, E.C, and HUMPHREY, T. Studies of the vertebrate telencephalon: II. The nuclear pattern of the anterior olfactor nucleus, tuberculum olfactorium, and the amygdaloid complex m adult man. Journal of Comparative Neurology, 1941, 74, 340–352.Google Scholar
  22. DAVAL, G. and LEVETEAU, J. Electrophysiological studies of centrifugal and centropetal connections of the anterior olfactory nucleus. Brain Research, 1974, 78, 595–410.Google Scholar
  23. DEJERINE, J.J. Anatomie des centres nerveux, 2 vols. Paris: Rueff, 1895–1901.Google Scholar
  24. DENNIS, B.J, KERR, D.I. An evoked potential study of the centripetal and centrifugal connections of the olfactory bulb in the cat. Brain Research, 1968, 11, 575–596.Google Scholar
  25. DENNIS, B.J. and KERR, D.I. Origins of olfactory bulb centrifugal fibers in the cat, Brain Research, 1976, 110, 595–600.Google Scholar
  26. DE OLMOS, J.S. A cupric-silver method for impregnation of terminal axon degeneration and its further use in staining granular argyrophillc neurons. Brain, Behavior and Evolution, 1969, 1, 215–257.Google Scholar
  27. DE OLMOS, J.S, The amygdaloid projection field in the rat as studied with the cupric-silver method. In B. E. Eleftheriou (Ed.), The Neurobiology of the Amygdala. New York-London: Plenum Press, 1972, 145–204.Google Scholar
  28. DE OLMOS, J.S. An improved HRP method for the study of central nervous connections. Experimental Brain Research. 1977, in press.Google Scholar
  29. DE OLMOS, J.S. and HEIMER, L. The efferent projections of the posterior (temporal) part of the primary olfactory cortex of the guinea pig. 1977, in preparation.Google Scholar
  30. DE OLMOS, J.S., HEIMER, L, and HARDY, H. Centrifugal pathways to the olfactory bulb of the rat: An experimental HRP-study. 1977, in preparation.Google Scholar
  31. DE OLMOS, J.S., INGRAM, W.R. The projection field of the stria terminalis in the rat brain. An experimental study. Journal of Comparative Neurology, 1972, 146, 503–554.Google Scholar
  32. DEVOR, M, Fiber trajectories of olfactory bulb efferents in the hamster. Journal of Comparative Neurology, 1976, 166, 51–47.Google Scholar
  33. DiFIGLIA, M., PASIK, P. and PASIK, T. A Golgi study of the neuronal types in the neostriatum of monkeys. Brain Research, 1976, 114, 245–256.Google Scholar
  34. DIVAC, I. Magnocellular nuclei of the basal forebrain project to neocortex, brain stem, and olfactory bulb. Review of some functional correlates. Brain Research, 1975, 95, 585–598Google Scholar
  35. DOGIEL, A.S. Die Retina der Vogel. Archiv für mikroskopische Anatomie und Entwicklungsmechanik, 1895, 44, 622–648.Google Scholar
  36. DUSSER DE BARENNE, J. G, Selektive Abtotung der Nervenzell schichten der Grosshirnrinde. Die Methode der laminaren Thermokoagula- tion der Rinde. Zeitschrift ges. Neurologie und Psychiatrie, 1935, 147, 280–290.Google Scholar
  37. ELDRED, E., GRANIT, R. MERTON, P.A. Supraspinal control of the muscle spindles and its significance. Journal of Physiology, 1955, 122, 498–523.Google Scholar
  38. FERRER, N.G. Secondary olfactory projections in the galago (Galago crassicaudatus) and the tree shrew (Tupaia glis). Journal of Comparative Neurology, 1969, 136, 337–347PubMedGoogle Scholar
  39. FXLXMONOFF, I.N, On the so-called rhinencephalon in the dolphin. Journal fur Hirnforschung, 1965, 8, 1–23Google Scholar
  40. FLORES, A. Die Myeloarchitektonik und die Myelogenic des Cortex Cerebri beim Igel (Erinaceus europaeus). Journal fur Psychologie und Neurologie (Leipzig), 1910–11, 215–247.Google Scholar
  41. FOX, C.A., ANDRADE, A.N., LU QUI, J, J. and RAFOLS, J.A. The primate globus pallidas: a Golgi and electron microscopic study. Journal fur Hirnforschung, 1974, 15, 75–93PubMedGoogle Scholar
  42. FOX, C.A., FISHER, R.R. and DESALVA, S.J. The distribution of the anterior commissure in the monkey (Macaca mulatta). Journal of Comparative Neurology, 1948, 89, 245–277.PubMedGoogle Scholar
  43. FOX, C.A. and SCHMITZ, J.I, A march study of the distribution of the anterior commissure in the cat. Journal of Comparative Neurology, 1943, 79, 297–314.Google Scholar
  44. FREEMAN, W.J. Effects of surgical isolation and tetanization on prepyriform cortex in cats. Journal of Neurophysiology, 1968, 31, 349–357.PubMedGoogle Scholar
  45. FREEMAN, W.J. Mass Action in the Nervous System. New York: Academic Press, 1975Google Scholar
  46. FUXE, K. Evidence for the existence of monoamine neurons in the central nervous system. IV. Distribution of monoamine nerve terminals in the central nervous system. Acta Physiologica Scandinavica, 1965, 64 (Suppl. 247), 39–85.Google Scholar
  47. GALAMBOS, R. Suppression of auditory nerve activity by stimulation of efferent fibers to the cochlea. Federation Proceedings, 1955, 14, 53.Google Scholar
  48. GIRGIS, M. and GOLDBY, F. Secondary olfactory connections and the anterior commissure in the coypu, Myocastor coypus. Journal of Anatomy (London), 1967, 101, 33–44.Google Scholar
  49. GOLD, R.M, Aphagia and adipsia following unilateral and bilaterally asymmetrical lesions in rats. Physiology and Behavior, 1967, 2, 211–220.Google Scholar
  50. GORRY, J.D. Studies on the comparative anatomy of the ganglion basale of Meynert, Acta anatomica, 1965, 55, 51–104.Google Scholar
  51. GRANIT, R, Centrifugal and antidromic effects on ganglion cells of retina. Journal of Neurophysiology, 1955, 18, 388–411.PubMedGoogle Scholar
  52. GRANIT, R, and KAADA, B.R, Influence of stimulation of central nervous structures on muscle spindles in cat. Acta Physiologica Scan- dinavica, 1952, 27, 130–160Google Scholar
  53. GRAY, P.A. The cortical lamination pattern of the opossum, didel- phys virginiana. Journal of Comparative Neurology, 1924, 37, 221–263.Google Scholar
  54. GRAYBIEL, A. Wallerian degeneration and anterograde tracer methods. In W.M. Cowan and M. Cuenod (Eds.), The Use of Axonal Transport for Studies of Neuronal Connectivity. Amsterdam: Elsevier, 1975, 175–216.Google Scholar
  55. GURDJIAN, E.S. Olfactory connections in the albino rat, with special reference to the stria medullaris and the anterior commissure. Journal of Comparative Neurology, 1925, 38, 127–165.Google Scholar
  56. HABERLY, L.B. and SHEPHERD, G.M. Current-density analysis of summed evoked potentials in opossum prepyriform cortex. Journal of Neurophysiology, 1973, 36, 789–802.PubMedGoogle Scholar
  57. HAGBARTH, K.E. and KERR, D.I.B. Central influences on spinal afferent conduction. Journal of Neurophysiology, 1954, 17, 295–507.PubMedGoogle Scholar
  58. HARDY, H., HEIMER, L., SWITZER, R. and WATKINS, D. Simultaneous demonstration of horseradish peroxidase and acetylcholinesterase, Neuroscience Letters, 1976, 3, 1–5.PubMedGoogle Scholar
  59. HAUG, F-M. S. Heavy metals in the brain. A light microscopic study of the rat with Tinmifs sulphid silver method. Methodological considerations and cytological and regional stainign patterns. Advances in Anatomy, Embryology and Cell Biology, 1975, 47(4) Verlag, Berlin: Heidelberg: New York.Google Scholar
  60. HAUG, F.M. S. Sulphide silver pattern and cytoarchitectonics of parahippocampal areas in the rat. Advances in Anatomy, Embryology and Cell Biology, 1976, 52 (4), 5–73.Google Scholar
  61. HEDREEN, J.C. and CHALMERS, J,P. Neuronal degeneration in rat brain induced by 6-hydroxydopamine; a histological and biochemical study. Brain Research, 1972, 47, 1–56PubMedGoogle Scholar
  62. HEIMER, L, Synaptic distribution of centripetal and centrifugal nerve fibres in the olfactory system of the rat. An experimental anatomical study. Journal of Anatomy (London), 1968, 103, 415–452.Google Scholar
  63. HEIMER, L. Bridging the gap between light and electron microscopy in the experimental tracing of fiber connections. In WaJ.H. Nauta and Sa0.Ea Ebbesson (Eds.). Contemporary Research Methods in Neuroanatomy, New York: Springer, 1970, 162–172.Google Scholar
  64. HEIMER, L. The olfactory connections of the diencephalon. An experimental light- and electron-microscopic study with special emphasis on the problem of terminal degeneration. Brain, Behavior and Evolution, 1972, 6, 484–523.PubMedGoogle Scholar
  65. HEIMER, L. Olfactory projections to diencephalon. In WE. Stumpf and L.D, Grant (Eds.), Anatomical Neuroendocrinology. Basel: Karger, 1975, 30–39.Google Scholar
  66. HEIMER, L. and DE OLMOS, J.S. The efferent projections of the olfactory tubercle in the rat. 1977, in preparation.Google Scholar
  67. HEIMER, L., DE OLMOS, J.S., HARDY, H. and ROBARDS, M.J. The olfactory tubercle projections in the rat. Neuroscience Abstract, 1975, 1, 680.Google Scholar
  68. HEIMER, L. and KALIL, R. Rapid death of cortical neurons following removal of the olfactory bulb in adult rats. 1977, in preparation.Google Scholar
  69. HEIMER, L. and PETERS, A. An electron microscope study of a silver stain for degenerating boutons. Brain Research, 1968, 8, 337–346.PubMedGoogle Scholar
  70. HEIMER, L., VAN HOESEN, G.W, and ROSENE, D, The olfactory pathways and the anterior perforated substance in the primate brain. International Journal of Neurology, 1977a, in pressGoogle Scholar
  71. HEIMER, L., ROBARDS, M. and SWXTZER, R.C. The olfactory tubercle: A structure of varying stratification. Experimental Brain Research, 1977b, in press.Google Scholar
  72. HEIMER, L., VAN HOESEN, G.W., MESULAM, M-M. and ROSENE, D.L. The origin of the centrifugal ac ethylcho1in esterase positive fiber system to the olfactory bulb in rat and monkey: An experimental HRP and AChE-histochemical study. 1977c, in preparationGoogle Scholar
  73. HEIMER, L. and WILSON, R. D, The subcortical projections of the allocortex: Similarities in the neural associations of the hippocampus, the piriform cortex, and the neocortex. In M. Santin I (Ed.), Golgl Centennial Symposium: Perspective In Neurobiology, New York: Raven Press, 1975, 177–193.Google Scholar
  74. HERKENHAM, M.A. Afferent connections of the habenular nuclei in the rat. Neuroscience Abstract, 1975, 849, 1.Google Scholar
  75. HERKENHAM, M.A. A thalamo-hippocampal connection In the rat. Neuroscience Abstract, 1976, 2, 548.Google Scholar
  76. HERKENHAM, M.A. and NAUTA, W.J.H. Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fiber-of-passage problem. Journal of Comparative Neurology. 1977, in press.Google Scholar
  77. HERNANDEZ-PEON, R. Central mechanisms controlling conduction along central sensory pathways, Acta Neurologica (Latinoamerica), 1955, 1, 256–264.Google Scholar
  78. HERNANDEZ-PEON R. HAGBARTH, K.E, Interaction between afferent and cortically Induced reticular responses. Journal of Neurophysiology, 1955, 18, 44–55.Google Scholar
  79. HERRICK, C.J. The morphology of the for.ebrain in Amphibia and Reptilia. Journal of Comparative Neurology and Psychology, 1910, 20, 413–546.Google Scholar
  80. HIDDEMA, F. De vergindingen van het Intermediaire kemsysteem van de thalamus bij de rat. Proefschrift: Groningen (1968).Google Scholar
  81. HJORTH-SIMONSEN, A. HIppocampal efferents to the ipsilateral ento- rhinal area: an experimental study in the rat. Journal of iomparcitlve Neurology, 1971, 142, 417–457.Google Scholar
  82. HJORTH-SIMONSEN, A, and JEUNE, B. Origin and termination of the hippo- campal perforant path in the rat studied by silver impregnation. Journal of Comparative Neurology, 1972, 144, 215–232.Google Scholar
  83. HUNT, C.C. KUFFLER, Sfi Further study of efferent small-nerve fibers to mammalian muscle spindles. Multiple spindle innervation and activity during contraction. Journal of Physiology. 1951, 113, 283–297.PubMedGoogle Scholar
  84. JACKSON, J.C. and BENJAMIN, R.M. Unit discharges in the irt?dodorsal nucleus of the rabbit evoked by electrical stimulation of the olfactory bulb. Brain Research, 1974, 75, 193–201PubMedGoogle Scholar
  85. JACOBS, M.S., MORGANS, P.G. and MCFARLAND, W.L, The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus). Rhinic lobe (Rhinencephalon). 1. The paleocortex. Journal of Comparative Neurology, 1971, 141, 205–2719PubMedGoogle Scholar
  86. JOHNSON, T.N. Studies on the brain of the guinea pig, II. The olfactory tracts and fornix. Journal of Comparative Neurology, 1959, 112, 121–159.PubMedGoogle Scholar
  87. JONES, E.G., BURTON, H., SAFER, C,B, and SWANSQN, L.W. Mibrain, diencephalic and cortical relationships of the basal nucleus of Meynert and associated structures in primates. Journal of Comparative Neurology, 1976, 167, 385–420.PubMedGoogle Scholar
  88. JONES, E.G. and POWELL, T.P.S. An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain, 1970, 93, 793–820.PubMedGoogle Scholar
  89. KALLEN, B, The nuclear development in the mammalian forebrain with special regard to the subpallidum. A imiversitets Arss- krift, 1952, Avd. 2, Bd9 46, Nr. 9, 11.Google Scholar
  90. KARTEN, H.J. Projections of the parahippocampal gyrus of the cat. Anatomical Record, 1963, 145, 247–248.Google Scholar
  91. KEMP, J. The termination of strio-pallidal and strio-nigral fibers. Brain Research, 1970, 17, 125–128.PubMedGoogle Scholar
  92. KERR, D.I.B. and DENNIS, B.J. Collateral projection of the lateral olfactory tract to entorhinal cortical areas in the cat., Brain Research, 1972, 36, 399–403.PubMedGoogle Scholar
  93. KERR, D.I.B. and HAGBARTH, K.E. An investigation of olfactory centrifugal fiber system. Journal of Neurophysiology, 1955, 18, 362–374.PubMedGoogle Scholar
  94. KIEVIT, J. KuHERS, H.G. Basal forebrain and hypothalamic connections to fijital and parietal cortex in the rhesus monkey. Science, 1975, 187, 660–662.PubMedGoogle Scholar
  95. KOLLIKER, A. VON. Handbuch der Gewebelehre des Menschen. Engelmann: Leipzig, 1896, 2aGoogle Scholar
  96. KREINER, J. Myeloarchitectonics of the lateral olfactory tract and of the piriform cortex of the albino rat, Journal of Comparative Neurology, 1949, 91, 103–127.PubMedGoogle Scholar
  97. KRETTEK, J.E. and PRICE, J.L, Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat. Journal of Comparative Neurology, 1977a (in press).Google Scholar
  98. KRETTEK, J.E. and PRICE, J.L, Projections from the amygdaloid complex and adjacent olfactory structures to the entorhinal cortex and stxbiculum In the rat and cat. Journal of Comparative Neurology, 1977b (In press).Google Scholar
  99. KRETTEK, J.E, and PRICE, J.L. Amygdaloid projections to subcortical structures within the basal forebraln and brainstem in the rat and cat. Journal of Comparative Neurology, 1977c (in press).Google Scholar
  100. KRIEG, W.J.S. Connections of the cerebral cortex, I. The albino rat. A, Topography of the cortical areas. Journal of Comparative Neurology, 1946, 84, 221–275.Google Scholar
  101. KRIEG, W.J.S. Connections of the cerebral cortex. I. The albino rat. B. Structures of the cortical areas. Journal of Comparative Neurology, 1946, 84, 277–323.Google Scholar
  102. LAMMERS, H.J. Experimenteel anatomisch ondersoek van de secundaire olfactorische verbindingen bij de kat, Ned. Tschr. Geneesk, 1959, 103, 702–705.Google Scholar
  103. LEONARD, C.M. The prefrontal cortex of the rat. I. Cortical projection of the medic-dorsal nucleus. II. Efferent connections. Brain Research, 1969, 12, 321–545.PubMedGoogle Scholar
  104. LINDVALL, O. and BJSIKLLJND, A. The organization of the ascending catecholamine neuron systems in the rat brain as revealed by the glyoxylic acid fluorescence method. Acta Physiologica Scandinavica (Suppl.. 412 ), 1974, 1–48.Google Scholar
  105. LOEWENTHAL, S. Ueber das Riechhirn der Saugethiere, Festschr. 69. Vers, dtsch. Naturforsch. u. Arzte, Braunschweiger. Deitr. wiss. Med., 1897, 215–220.Google Scholar
  106. LOHMAN, A.H.M. The anterior olfactory lobe of the guinea pig. A descriptive and experimental anatomical study. Acta anatomica (Basel), 1963, 53 (Suppl. 49), 1–109.Google Scholar
  107. LOHMAN, A.H.M. and MENTINK, G.M. The lateral olfactory tract, the anterior commissure and the cells of the olfactory bulb. Brain Research, 1969, 12, 396–415.PubMedGoogle Scholar
  108. LUNDBERG, P.O. Cortlco-hypothalamic connections in the rabbit: a experimental neuroanatomical study. Acta Physiologica Scandinavica, 1960, 49 (Suppl. 171), 1–80.Google Scholar
  109. MACCHI, G. The ontogenetic development of the olfactory telencephalon in man, Journal of Comparative Neurology, 1951, 95, 245–305.PubMedGoogle Scholar
  110. MCLEAN, P.D, Psychosomatic disease and. the visceral brainf recent developments bearing on Papez theory of emotion. Psychosomatic Medicine, 1949, II, 338–355.Google Scholar
  111. MMN, G, Bulbusoi. fact or ins accessorius in Chiroptera. Journal of Comparative Neurology, 1961, 116, 135–144.Google Scholar
  112. MESULAM, M-M. The blue reaction product in horseradish peroxidase neuro histochemistry: Incubation parameters and visibility, The Journal of Histochemistry and Cytochemistry, 1976, 24 (12), 1273–1280.PubMedGoogle Scholar
  113. MESULAM, M-M. and VAN HOESEN, G.W. Acetylcholinesterase-rich projections from the basal forebrain of the rhesus monkey to neocortex. Brain Research, 1976, 109, 152–157.PubMedGoogle Scholar
  114. METTLER, F.A. Extracortical connections of the primate frontal cerebral cortex. II. Corticifugal connections. Journal of Comparative Neurology, 1947, 86, 119–166.Google Scholar
  115. MEYER, M. and ALLISON, A.C. An experimental investigation of the connections of the olfactory tracts in the monkey. Journal of Neurology, Neurosurgery and Psychiatry, 1949, 12, 274–286.PubMedGoogle Scholar
  116. MEYNERT, T. Vom Gehirne der Saugethiere. In S. Stricker (Ed.), Handbuch der Lehre von den Geweben des Menschen und Thiere. Leipzig: Engelmann, 1872, 2, 694–808.Google Scholar
  117. MILLHOUSE, O.E. A Golgi study of the descending medial forebrain bundle. Brain Research, 1969, 15, 341–363.PubMedGoogle Scholar
  118. MIODONSKI, R. Myeloarchitectonics and connections of substantia innominata in the dog brain. Acta Biologiae Experimentalis (Warszawa), 1967, 27, 61–84.Google Scholar
  119. MONAKOW, C. VON. Experimentelle und pathalogisch-anatomische Untersuchungen über die Optishchen Centren und Bahnen (Neue Folge). Archiv für Psychiatrica Nervenkr., 1889, 20, 714–787.Google Scholar
  120. NAUTA, W.J.H. HAYMAKER, W. Hypothalamic nuclei and fiber connections. In W. Haymaker and E, Anderson (Eds.), The Hypothalamus. Springfield: C.C. Thomas, 1969Google Scholar
  121. NORGREN, R. Gustatory afferents to ventral forebrain. Brain Research, 1974, 81, 285–295.PubMedGoogle Scholar
  122. NORGREN, R. Taste pathways to hypothalamus and amygdala. Journal of Comparative Neurology, 1976, 166, 17–50PubMedGoogle Scholar
  123. NORGREN, R. and LEONARD, C.M. Ascending central gustatory pathways. Journal of Comparative Neurology, 1975, 150, 217–257.Google Scholar
  124. OLLEARY, J.L. Structure of the primary olfactory cortex of the mouse. Journal of Comparative Neurology, 1975, 150, 217–258.Google Scholar
  125. PANDYA, D.N., KAROL, E.A. and LELE, P.P. The distribution of the anterior commissure in the squirrel monkey. Brain Research, 1975, 49, 177–180.Google Scholar
  126. PAPEZ, J.W., ARONSON, L.R. Thalamic nuclei of pithecus (macacus) rhesus, 1. Ventral thalamus. Archives of Neurology and Psychiatry, 1954, 52, 1–26.Google Scholar
  127. PIGACHE, R.M. The anatomy of “paleocortex.” A critical review. Ergebnisse der Anatomie und Entwicklungsgeschichte, 1970, 45, 5–62.Google Scholar
  128. POPOFF, I. and POPOFF, N. Allocortex bei der Ratte (Mus decumanus). Journal fur Psychologie und Neurologie, 1929, 59, 257–522.Google Scholar
  129. POWELL, T.P.S., COWAN, W.M. and RAISMAN, G. Olfactory relationships of the diencephalon. Nature (London), 1965, 199, 710–712.Google Scholar
  130. POWELL, T.P.S., COWAN, W.M. and RAISMAN, G. The central olfactory connections. Journal of Anatomy (London), 1965, 99, 791–815.Google Scholar
  131. PRICE, J.L. An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex. Journal of Comparative Neurology, 1975, 150, 87–108.Google Scholar
  132. ROSENE, D.L., VAN HOESEN, G.W. and MESULAM, M-M. Hippocampal projections to entorhinal cortex of the rhesus monkey. The Anatomical Record, 1976, 184, 517.Google Scholar
  133. ROSENE, D.L., MESULAM, M-M. and VAN HOESEN, G.W. Afferents to area FL of the medial frontal cortex from the amygdala and hippocampus of the rhesus monkey. Neuroscience Abstracts, 1976b, 2, 141.Google Scholar
  134. SANDERS-WOUDSTRA, J.A.R. Experimental anatomisch onderzoek over de verbindingen van enkele basale telencefale hersengebieden bij de albinorat. Thesis, University of Groningen, Groningen: Van Denderen, 1961.Google Scholar
  135. SMIDES, F. Die Insulae terminales des Erwachsenengehirns des Menschen. Journal fur Hirnforschung, 1957, 5, 245–275.Google Scholar
  136. SANIDES, F. Representation in the cerebral cortex and its areal lamination patterns. In GJ, Bourne (Ed.), Structure and Function of Nervous Tissue, New York-London: Academic Press, 1972, 5, 529–455.Google Scholar
  137. SCALIA, F. Some olfactory pathways in the rabbit brain. Journal of Comparative Neurology, 1966, 126, 285–310.PubMedGoogle Scholar
  138. SCALIA, F. A review of recent experimental studies on the distribution of the olfactory tracts in mammals. Brain, Behavior and Evolution, 1968, 1, 101–125.Google Scholar
  139. SCALIA, F. and WINANS, S.S. The differential projections of the olfactory bulb and the accessory olfactory bulb in mammals. Journal of Comparative Neurology, 1975, 161, 31–55.PubMedGoogle Scholar
  140. SCOTT, J.W. CHAFIN, B.R. Origin of olfactory projections to lateral hypothalamus and nuclei gemini of the rat. Brain Research, 1975, 88, 64–68.PubMedGoogle Scholar
  141. SCOTT, J.W. and LEONARD, C.M. The olfactory connections of the lateral hypothalamus in the rat, mouse and hamster. Journal of Comparative Neurology, 1971, 141, 551–544.Google Scholar
  142. SCOTT, J.W. and PFAFFMANN, C. Olfactory input to the hypothalamus. Electrophysiological evidence. Science, 1967, 158, 1592–1594.PubMedGoogle Scholar
  143. SELTZER, B, and PANDYA, D.N. Some cortical projections to the para- hippocampal area in the rhesus monkey. Experimental Neurology, 1976, 50, 146–160.PubMedGoogle Scholar
  144. SHEPHERD, M.G. The synaptic organization of the brain. An introduction. New York: Oxford University Press, 1974.Google Scholar
  145. SHEPHERD, G.M. and HABERLY, L.B. Partial activation of olfactory bulb: Analysis of field potentials and topographic relation between bulb and lateral olfactory tract. Journal of Neurophysiology, 1970, 53, 643–655.Google Scholar
  146. SHIPLEY, M.T. The topographical and laminar organization of the presubiculum1s projection to the ipsi- and contralateral entorhinal cortex in the guinea pig. Journal of Comparative Neurology, 1975, 160, 127–145.PubMedGoogle Scholar
  147. SHOWERS, M.J.C. Correlation of medial thalamic nuclear activity with cortical and subcortical neuronal arcs. Journal of Comparative Neurology, 1958, 109, 261–315.PubMedGoogle Scholar
  148. SHUTE, C.C.D, and LEWIS, P.R. Cholinergic nervous pathways in the forebrain. Nature (London), 1961, 189, 532–553.Google Scholar
  149. SHUTE, C.C.D, LEWIS P. R. Cholinergic nervous pathways in the brain. Nature (London), 1965, 199, 1160–1164Google Scholar
  150. SHUTE, C.C.D. and LEWIS, P.R. The ascending cholinergic reticular system: Neocortical, olfactory and subcortical projections. Brain, 1967, 50, 497–520.Google Scholar
  151. S1EGEL, A., FUKUSHIMA, T. and EDJNGER, H. Origins of the mediodorsal nucleus in the rat. Neuroscience Abstract, 1976, II, 597.Google Scholar
  152. SIEGEL, A, and TASSONI, J.P. Differential efferent projections of lateral and medial septal nuclei to the hippocampus in the cat. Brain Behavior and Evolution, 1971, 4, 201–219.Google Scholar
  153. SKEEN, L.C. Sources of olfactory projections to the dorsal thalamus in the tree shrew (tupaia glis). Neuroscience Abstracts, 1976, 2, 165.Google Scholar
  154. SMITH, G.E. A new topographical survey of the human cerebral cortex, being an account of the distribution of the anatomically distinct cortical areas and their relationship to the cerebral sulci. Journal of Anatomy (London), 1907, 41, 257–254.Google Scholar
  155. STEP MAN, H. Allocortex, Handbuch der mikroskopischen Anatomy des Menschen, IV /9. 1 Berlin: Springer Verlag, 1975.Google Scholar
  156. STEVENS, C.F. Structure of cat frontal olfactory cortex. Journal of Neurophysiology, 1969, 52, 184–192.Google Scholar
  157. STEWARD, O. Topographic organization of the projections from the entorhinal area to the hippocampus formation of the rat. Journal of Comparative Neurology, 1976, 167, 285–514.PubMedGoogle Scholar
  158. SLLWLFD, O. and SCOVLLLE, S.A. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. Journal of Comparative Neurology, 1976, 169, 547–570.Google Scholar
  159. SWANSON, LJ. An autoradiographic study of the efferent connections of the preoptic region in the rat. Journal of Comparative Neurology, 1976, 167, 227–256.PubMedGoogle Scholar
  160. SWANSGN, L.W. and COWAN, W.M. A note on the connections and development of the nucleus accumbens. Brain Research, 1975, 92, 524–550.Google Scholar
  161. SWANSON, L.W. and HARTMAN, B.K, The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta- hydroxylase as a marker. Journal of Comparative Neurology, 1975, 165, 467–505.Google Scholar
  162. SWITZER, R.C. and HEIMER, L. A direct olfactory projection to area frontalis in the opossum, Neuroscience Abstract, 1976, II, 259.Google Scholar
  163. SWITZER, R.C. and HEIMER, L. An olfactory projection to the frontal neocortex In the opossum and the rat. 1977, In preparation.Google Scholar
  164. TANABE, T., YARITA, H., UNO, M., OOSHIMA, Y. and TAKAGI, S.F. An olfactory projection area in orbitofrontal cortex in the monkey. Journal of Neurophysiology, 1975, 58, 1269–1285.Google Scholar
  165. UNGERSTEDT, U. Stereotaxic mapping of the monoamine pathways in the rat brain. Acta Physiologica Scandinavica, 1971, Suppl. 567, 1–48.Google Scholar
  166. VALVERDE-GARCIA, F. Studies on the piriform lobe. Cambridge: Harvard University Press, 1965.Google Scholar
  167. VAN ALPHEN, H.A.M. The anterior commissure of the rabbit. Acta Anatomica (Basel), 1969, 74 (Suppl. 57), 1–112.Google Scholar
  168. VAN GEHUCHTEN, A. Contribution a lfetude des voles olfactives. Le Nevraxe, 1904–04, 6, 191–200.Google Scholar
  169. VAN HOESEN, G.W., MESULAM, M-M. and HAAXMA, R. Temporal cortical projections to the olfactory tubercle in the rhesus monkey. Brain Research, 1976, 109, 375–581.PubMedGoogle Scholar
  170. VAN HOESEN, G.W., PANDYA, D.N. and BUTTERS, N. Cortical afferents to the entorhinal cortex of the rhesus monkey. Science, 1972, 175, 1471–1473.PubMedGoogle Scholar
  171. VAN HOESEN, G.W. and PANDYA, D.N. Afferent and efferent connections of the perirhinal cortex (area 55) In the rhesus monkey. Anatomical Record, 1973, 175, 460.Google Scholar
  172. VAN HOESEN, G.W. and PANDYA, D.N. Some connections of the entorhinal (area 28) and perirhinal (area 55) cortices of the rhesus monkey. I. Temporal lobe afferents. Brain Research, 1975, 95, 1–24.PubMedGoogle Scholar
  173. VAN HOESEN, G.W. and PANDYA, D.N. Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections. Brain Research, 1975, 95, 35–59.Google Scholar
  174. VAZFERREIRA, A. The cortical areas of the albino rat studied by silver Impregnation. Journal of Comparative Neurology, 1951, 95, 177–245.Google Scholar
  175. VONECONOMO, C. Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen, Wien-Berlin: Springer, 1925.Google Scholar
  176. WALLENBERG, A. Das sensibel System (Anatomy, physiology, and pathology of the sensory systems). Abstracted in Archives of Neurology and Psychiatry (Chicago), 1928, 20, 1109–1120Google Scholar
  177. WHITE, L.E., Jr. Olfactory bulb projections of the rat. Anatomical Record, 1965, 152, 465–479.Google Scholar
  178. W1NANS, S.S. and SCALIA, F. Amygdaloid nucleus: New afferent input from the vomeronasal organ. Science, 1970, 170, 550–552.Google Scholar
  179. YOUNG, M.W. The nuclear pattern and fiber connections of the non- cortical centers of the telencephalon in the rabbit (lepus cuniculus). Journal of Comparative Neurology, 1956, 65, 295–401.Google Scholar
  180. YOUNG, M.W. Degeneration of the fiber tracts following experimental transection of the olfactory bulb. Anatomical Record, 1941, 79 (Suppl.), 65–66.Google Scholar

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© Springer Science+Business Media New York 1978

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  • Lennart Heimer

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