Advertisement

Brain Structure and Function

, Volume 213, Issue 1–2, pp 3–10 | Cite as

Lennart Heimer: in memoriam (1930–2007)

  • Suzanne N. Haber
  • Jacqueline F. McGinty
  • Enrico Mugnaini
  • Laszlo ZaborszkyEmail author
Original Article
  • 151 Downloads

Keywords

Olfactory Bulb Globus Pallidus Basal Forebrain Ventral Striatum Stria Terminalis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Special thanks are due to all those who have contributed as authors or reviewers, in particular to Daniel S. Zahm, Professor, Department of Pharmacology and Physiological Science, Saint Louis University, St Louis, Missouri who reviewed many of the submissions. The authors thanks to John A. Jane, Sr, Professor and Program Director, Department of Neurological Surgery at the University Virginia, Charlottesville, Virginia and Ms Karen Saulle in helping in the biographical data of LH.

Publications of Lennart Heimer

Books

  1. Heimer L (1961) The human brain and spinal cord. Dissection guide and review of the functional anatomy of the central nervous system. AB Akademiforlaget-Gumperts, Gothenburg. (in Swedish)Google Scholar
  2. Heimer L (1983) The human brain and spinal cord: functional neuroanatomy and dissection guide. Springer, New YorkGoogle Scholar
  3. Heimer L (1995) The human brain and spinal cord: functional neuroanatomy and dissection guide. Springer, New YorkGoogle Scholar
  4. Heimer L, Robards MJ (eds) (1981) Neuroanatomical tract-tracing methods. Plenum Press, New YorkGoogle Scholar
  5. Heimer L, Zaborszky L (eds) (1989) Neuroanatomical tract-tracing methods 2. Recent progress. Plenum Press, New YorkGoogle Scholar
  6. Heimer L, Trimble M, Van Hoesen GW, Zahm DS (2008) Anatomy of neuropsychiatry. The new anatomy of the basal forebrain and its implications for neuropsychiatric illness. Elsevier-Academic Press, AmsterdamGoogle Scholar

Instructional video

  1. Heimer L (1990) Dissection of the human brain: a Videotape Teaching Program. Springer/GmbH & Co KG, Berlin/MainzGoogle Scholar
  2. Heimer L (2007) Dissection of the human brain. Sinauer Associates, Sunderland. (DVD)Google Scholar

Journal articles and book chapters

  1. Alheid GF, Heimer L (1996) Theories of basal forebrain organization and the “emotional motor system”. Prog Brain Res 107:461–484PubMedCrossRefGoogle Scholar
  2. Alheid GF, Heimer L (1988) New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27:1–39PubMedCrossRefGoogle Scholar
  3. Alheid GF, Carlsen J, de Olsen J, Heimer L (1984a) Quantitative determination of collateral anterior olfactory nucleus projections using a fluorescent tracer with an algebraic solution to the problem of double retrograde labeling. Brain Res 292:17–22PubMedCrossRefGoogle Scholar
  4. Alheid GF, Carlsen J, Heimer L (1984b) An algebraic approach to the detection of multiple markers in complex neuronal systems. J Neurosci Methods 10:71–77PubMedCrossRefGoogle Scholar
  5. Alheid GF, Van Hoesen GW, Heimer L (1989) Functional neuroanatomy. In: Kaplan HJ, Sadock BJ (eds) Comprehensive textbook of psychiatry, 5th edn. Lippincott Williams and Wilkins, Baltimore, pp 26–95Google Scholar
  6. Alheid GF, Heimer L, Switzer RD (1990) The basal ganglia. In: Paxinos G (ed) The human nervous system. Academic, San Diego, pp 483–581Google Scholar
  7. Alheid GF, Beltramino CA, de Olmos JS, Forbes MS, Swanson DJ, Heimer L (1998) The neuronal organization of the supracapsular part of the stria terminalis in the rat: the dorsal component of the extended amygdala. Neuroscience 84:967–996PubMedCrossRefGoogle Scholar
  8. Beltramino CA, Forbes, Swanson DJ, Alheid GF, Heimer L (1996) Amygdaloid input to transiently tyrosine hydroxylase immunoreactive neurons in the bed nucleus of the stria terminalis of the rat. Brain Res 706:37–46Google Scholar
  9. Beltramino CA, de Olmos JS, Gallyas F, Heimer L, Zaborszky L (1993) Silver staining as a tool for neurotoxic assessment. In: Erinoff L (ed) Methods for assessing neurotoxicity of drugs of abuse. Monograph 136. National Institute of Drug Abuse (NIDA), Rockville, pp 101–132Google Scholar
  10. Blackstad TW, Heimer L, Mugnaini E (1981) Experimental neuroanatomy: general approaches and laboratory procedures. In: Heimer L, Robards MJ (eds) Neuroanatomical tract-tracing methods. Plenum Press, New York, pp 1–54Google Scholar
  11. Brashear HR, Zaborszky L, Heimer L (1986) Distribution of GABAergic and cholinergic neurons in the diagonal band. Neuroscience 17:439–451PubMedCrossRefGoogle Scholar
  12. Bueno A, de Olmos S, Heimer L, de Olmos J (2003) NMDA-antagonist MK-801-induced neuronal degeneration in Wistar rat brain detected by the Amino-Cupric-Silver method. Exp Toxicol Pathol 54:319–334PubMedCrossRefGoogle Scholar
  13. Carlsen J, Heimer L (1986a) A correlated light and electron microscopic immunocytochemical study of cholinergic terminals and neurons in the rat amygdaloid body with special emphasis on the basolateral amygdaloid nucleus. J Comp Neurol 244:121–36PubMedCrossRefGoogle Scholar
  14. Carlsen J, Heimer L (1986b) The projection from the parataenial thalamic nucleus, as demonstrated by the Phaseolus vulgaris leucoagglutinin (PHA-L) method, identifies a subterritorial organization of the ventral striatum. Brain Res 374:375–379PubMedCrossRefGoogle Scholar
  15. Carlsen J, Heimer L (1988) The basolateral amygdaloid complex as a cortical-like structure. Brain Res 441:377–380PubMedCrossRefGoogle Scholar
  16. Carlsen J, de Olmos J, Heimer L (1982) Tracing of two-neuron pathways in the olfactory system by the aid of transneuronal degeneration: projections of the amygdaloid body and hippocampal formation. J Comp Neurol 208:196–208PubMedCrossRefGoogle Scholar
  17. Carlsen J, Zaborszky L, Heimer L (1985) Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: a combined retrograde fluorescent and immunohistochemical study. J Comp Neurol 234:155–167PubMedCrossRefGoogle Scholar
  18. Churchill L, Cross RS, Pazdernik TL, Nelson SR, Zahm DS, Heimer L, Kalivas PW (1992) Patterns of glucose use after bicuculline-induced convulsions in relationship to gamma-aminobutyric acid and mu-opioid receptors in the ventral pallidum—functional markers for the ventral palidum. Brain Res 581:39–45PubMedCrossRefGoogle Scholar
  19. de Olmos JS, Heimer L (1978) Mapping of collateral projections with the HRP-method. Neurosci Lett 6:107–114CrossRefGoogle Scholar
  20. de Olmos JS, Heimer L (1980) Double and triple labeling of neurons with fluorescent substances; the study of collateral pathways in the ascending raphe system. Neurosci Lett 19:7–12PubMedCrossRefGoogle Scholar
  21. de Olmos JS, Heimer L (1999) The concepts of the ventral striatopallidal system and extended amygdala. Ann N Y Acad Sci 877:1–32PubMedCrossRefGoogle Scholar
  22. de Olmos J, Hardy H, Heimer L (1978) The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP-study. J Comp Neurol 181:213–244PubMedCrossRefGoogle Scholar
  23. de Olmos JS, Ebbesson SOE, Heimer L (1981) Silver methods for the impregnation of degenerating axoplasma. In: Heimer L, Robards MJ (eds) Neuroanatomical tract-tracing methods. Plenum Press, New York, pp 117–170Google Scholar
  24. Ebbesson SOE, Heimer L (1970) Projections of the olfactory tract fibers in the nurse shark (Ginglymostoma cirratum). Brain Res 17:47–55PubMedCrossRefGoogle Scholar
  25. Fink RP, Heimer L (1967) Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system. Brain Res 4:369–374PubMedCrossRefGoogle Scholar
  26. Hardy H, Heimer L (1977) A safer and more sensitive substitute for diamino-benzidine in the light microscopic demonstration of retrograde and anterograde axonal transport of HRP. Neurosci Lett 5:235–240CrossRefPubMedGoogle Scholar
  27. Hardy H, Heimer L, Switzer R, Watkins D (1976) Simultaneous demonstration of horseradish peroxidase and acetylcholinesterase. Brain Res Newsl 3:1–5Google Scholar
  28. Heimer L (1967) Silver impregnation of terminal degeneration in some forebrain fiber systems: a comparative evaluation of current methods. Brain Res 5:86–108CrossRefGoogle Scholar
  29. Heimer L (1968a) Synaptic distribution of centripetal and centrifugal nerve fibers in the olfactory system of the rat. An experimental anatomical study. J Anat 103:413–432PubMedGoogle Scholar
  30. Heimer L (1968b) The tracing of pathways in the central nervous system. Proc IEEE 56:950–959CrossRefGoogle Scholar
  31. Heimer L (1969a) Silver impregnation of degenerating axons and their terminals on Epon-Araldite sections. Brain Res 12:246–249PubMedCrossRefGoogle Scholar
  32. Heimer L (1969b) The secondary olfactory connections in mammals, reptiles and shark. (In: Comparative and evolutionary aspects of the vertebrate central nervous System.) Ann N Y Acad Sci 167:129–146Google Scholar
  33. Heimer L (1970a) Bridging the gap between light and electron microscopy in the experimental tracing of fiber connections. In: Nauta WJH, Ebbesson SOE (eds) Contemporary research methods in neuroanatomy. Springer, New York, pp 162–172Google Scholar
  34. Heimer L (1970b) Selective silver impregnation of degenerating axoplasm. In: Nauta WJH, Ebbesson SOE (eds) Contemporary research methods in neuroanatomy. Springer, New York, pp 106–131Google Scholar
  35. Heimer L (1971) Pathways of the brain. Sci Am 225:48–60CrossRefGoogle Scholar
  36. Heimer L (1972) The olfactory connections of the diencephalons in the rat. An experimental light- and electron-microscopic study with special emphasis on the problem of terminal degeneration. Brain Behav Evol 6:484–523PubMedCrossRefGoogle Scholar
  37. Heimer L (1975) Olfactory projections to the diencephalons. In: Stumpf W, Grant L (eds) Handbook of neuroendocrinology. Karger, Basel, pp 30–39Google Scholar
  38. Heimer L (1978) The olfactory cortex and the ventral striatum. In: Livingston K, Hornykiewicz O (eds) Limbic mechanisms. The continuing evolution of the limbic system concept. Plenum Press, New York, pp 96–187Google Scholar
  39. Heimer L (1987) Neuroanatomical tract-tracing methods. In: Adelman G (ed) Encyclopedia of neurosciences. Birkhauser, Boston 3:766–769Google Scholar
  40. Heimer L (1999) The third quarter of the twentieth century; the golden age of the silver methods. Brain Res Bull 50:399–400PubMedCrossRefGoogle Scholar
  41. Heimer L (2000) Basal forebrain in the context of schizophrenia. Brain Res Brain Res Rev 31:205–235PubMedCrossRefGoogle Scholar
  42. Heimer L (2003a) A new anatomical framework for neuropsychiatric disorders and drug abuse. Am J Psychiatry 160:1726–1739PubMedCrossRefGoogle Scholar
  43. Heimer L (2003b) The legacy of the silver methods and the new anatomy of the basal forebrain: implications for neuropsychiatry and drug abuse. Scand J Psychol 44:189–201PubMedCrossRefGoogle Scholar
  44. Heimer L (2006) Short retrospection. In: Zaborszky L, Wouterlood FG, Lanciego JL (eds) Neuroanatomical tract-tracing 3: molecules, neurons, and systems. Springer, New York, pp 1–5CrossRefGoogle Scholar
  45. Heimer L, Alheid G (1991) Piecing together the puzzle of basal forebrain anatomy. In: Napier TC, Kalivas PW, Hanin (eds) The basal forebrain: anatomy to function. Plenum Press, New York, 295:1–42Google Scholar
  46. Heimer L, Alheid GF (1996) Basal forebrain organization; emerging concepts. Encyclopedia of neuroscience, 2nd edn. Elsevier, AmsterdamGoogle Scholar
  47. Heimer L, Ekholm R (1967) Neuronal argyrophilia in early degenerative states: a light- and electronmicroscopical study of the Glees and Nauta techniques. Experientia 23:237–239PubMedCrossRefGoogle Scholar
  48. Heimer L, Kalil R (1978) Rapid transneuronal degeneration and death of cortical neurons following removal of the olfactory bulb in adult rats. J Comp Neurol 178:559–609PubMedCrossRefGoogle Scholar
  49. Heimer L, Larsson K (1964) Drastic changes in the mating behavior of male rats following lesions in the junction of diencephalons and mesencephalon. Experientia 20:460–461PubMedCrossRefGoogle Scholar
  50. Heimer L, Larsson K (1965) Mating behavior in male rats after destruction of the mammillary bodies. Acta Neurol Scand 40:353–360CrossRefGoogle Scholar
  51. Heimer L, Larsson K (1966–1967) Impairment of mating behavior in male rats following lesions in the preoptic-anterior hypothalamic continuum. Brain Res 3:248–263Google Scholar
  52. Heimer L, Larsson K (1967) Mating behavior of male rats after olfactory bulb lesions. Physiol Behav 2:207–209CrossRefGoogle Scholar
  53. Heimer L, Lohman AHM (1976) Anatomical methods for tracing connections in the central olfactory system. In: Gazzaniga MS, Blakemore C (eds) Handbook of psychobiology. Academic, New York, pp 73–106Google Scholar
  54. Heimer L, Nauta WJ (1969) The hypothalamic distribution of the stria terminalis in the rat. Brain Res 13:284–297PubMedCrossRefGoogle Scholar
  55. Heimer L, Peters A (1968) An electron microscope study of a silver stain for degenerating boutons. Brain Res 8:337–346PubMedCrossRefGoogle Scholar
  56. Heimer L, van Hoesen G (1979) Ventral striatum. In: Divac J, Oberg RGE (eds) The neostriatum. Pergamon Press, Oxford, NY, pp 147–158Google Scholar
  57. Heimer L, Van Hoesen GW (2006) The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neurosci Biobehav Rev 30:126–147PubMedCrossRefGoogle Scholar
  58. Heimer L, Wall PD (1968) The dorsal root distribution to the substantia gelatinosa of the rat with a note on the distribution in the cat. Exp Brain Res 6:89–99PubMedCrossRefGoogle Scholar
  59. Heimer L, Wilson RD (1975) The subcortical projections of the allocortex. In: Santini M (ed) Golgi centennial symposium. Raven Press, New York, pp 177–193Google Scholar
  60. Heimer L, Ebner FF, Nauta WJH (1967) A note on the termination of commissural fibers in neocortex. Brain Res 5:171–177PubMedCrossRefGoogle Scholar
  61. Heimer L, Kuikka V, Larsson K, Nordstrom E (1971) A headholder for stereotaxic operations of small laboratory animals. Physiol Behav 7:263–264PubMedCrossRefGoogle Scholar
  62. Heimer L, Robards M, Switzer RC III (1976) The olfactory tubercle: a structure of varying stratification. Exp Brain Res (Suppl 1):141–147Google Scholar
  63. Heimer L, Van Hoesen GW, Rosene DL (1977) The olfactory pathways and the anterior perforated substance in the primate brain. Int J Neurol 12:42–52Google Scholar
  64. Heimer L, Switzer RD, van Hoesen GW (1982) Ventral striatum and ventral pallidum: additional components of the motor system? Trends Neurosci 5:83–87CrossRefGoogle Scholar
  65. Heimer L, Alheid G, Zaborszky L (1985) The basal ganglia. In: Paxinos G (ed) The rat nervous system. Academic, San DiegoGoogle Scholar
  66. Heimer L, Zaborszky L, Zahm DS, Alheid GF (1987) The ventral striatopallidothalamic projection. I. The striatopallidal link originating in the superficial layers of the olfactory tubercle. J Comp Neurol 255:571–591PubMedCrossRefGoogle Scholar
  67. Heimer L, Alheid GF, Zaborszky L (1989) Substantia innominata and basal forebrain. In: Edelman G (ed) Neuroscience year. Birkhauser, Boston, pp 21–24Google Scholar
  68. Heimer L, Zahm DS, Schmued L (1990) The basal forebrain projection to the region of the nuclei Gemini in the rat: a combined light and electron microscopic study employing horseradish peroxidase, fluorescent tracers and Phaseolus vulgaris-leucoagglutinin. Neuroscience 34:707–731PubMedCrossRefGoogle Scholar
  69. Heimer L, de Olmos J, Alheid GF, Zaborszky L (1991a) “Perestroika” in the basal forebrain: opening the border between neurology and psychiatry. Prog Brain Res 87:109–165PubMedCrossRefGoogle Scholar
  70. Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C (1991b) Specificity in the projection patterns of accumbal core and shell. Neuroscience 41:89–125PubMedCrossRefGoogle Scholar
  71. Heimer L, Alheid GF, Zahm (1993) Basal forebrain organization: an anatomical framework for motor aspects of drive and motivation. In: Kalivas PW, Barnes CD (eds) The mesolimbic motor circuit and its role in neuropsychiatric disorders. CRC, Boca Raton, pp 1–43Google Scholar
  72. Heimer L, Zahm DS, Alheid GF (1995) Basal ganglia. In: Paxinos (ed) The rat nervous system, 2nd edn. Academic, San Diego, pp 579–628Google Scholar
  73. Heimer L, Alheid GF, de Olmos JS, Groenewegen HJ, Haber SN, Harlan RE, Zahm DS (1997a) The accumbens: beyond the core-shell dichotomy. J Neuropsychiatry Clin Neurosci 9:354–381PubMedGoogle Scholar
  74. Heimer L, Harlan RE, Alheid GF, Garcia MM, de Olmos J (1997b) Substantia innominata: a notion which impedes clinical-anatomical correlations in neuropsychiatric disorders. Neuroscience 76:957–1006PubMedCrossRefGoogle Scholar
  75. Heimer L, de Olmos JS, Alheid GF, Pearson J, Sakamaoto N, Shinoda K, Marksteiner J, Switzer III RC (1999) The human basal forebrain. Part II. In: Bloom FE, Bjorklund A, Hokfelt T (eds) The primate nervous system, Part III. Handbook of chemical neuroanatomy, vol 15. Elsevier, Amsterdam, pp 57–226CrossRefGoogle Scholar
  76. Keefer DA, Chung JW, Heimer L (1980) Morphology and ultrastructure of anterior thalamic neurons solidly labeled with horseradish peroxidase. Brain Res 191:301–311PubMedCrossRefGoogle Scholar
  77. Larsson K, Heimer L (1964) Mating behavior of the male rat after lesions in the preoptic area. Nature 202:413–414PubMedCrossRefGoogle Scholar
  78. Millhouse OE, Heimer L (1984) Cell configuration in the olfactory tubercle of the rat. J Comp Neurol 227:571–597CrossRefGoogle Scholar
  79. Pohorecky LA, Zigmond MJ, Heimer L, Wurtman RJ (1969) Olfactory bulb removal: effects on brain norepinephrine. Proc Natl Acad Sci USA 62:1052–1055PubMedCrossRefGoogle Scholar
  80. Sakamoto N, Pearson J, Shinoda K, Alheid GF, de Olmos JS, Heimer L (1999) The human basal forebrain. Part I. An overview. In: Bloom FE, Bjorklund A, Hokfelt T (eds) The primate nervous system, Part III. Handbook of chemical neuroanatomy, vol 15. Elsevier, Amsterdam, pp 1–55CrossRefGoogle Scholar
  81. Schmued L, Heimer L (1990) Iontophoretic injection of fluoro-gold and other fluorescent tracers. J Histochem Cytochem 38:721–723PubMedGoogle Scholar
  82. Schmued LC, Kyrihidis K, Heimer L (1990) In vivo anterograde and retrograde axonal transport of fluorescent rhodamine-dextran-amines within the CNS. Brain Res 526:127–134PubMedCrossRefGoogle Scholar
  83. Shammah-Lagnado SJ, Alheid GF, Heimer L (1996) Efferent connections of the caudal part of the globus pallidus in the rat. J Comp Neurol 376:489–507PubMedCrossRefGoogle Scholar
  84. Shammah-Lagnado SJ, Alheid GF, Heimer L (1999) Afferent connections of the interstitial nucleus of the posterior limb of the anterior commissure and adjacent amygdalostriatal transition area in the rat. Neuroscience 94:1097–1123PubMedCrossRefGoogle Scholar
  85. Shammah-Lagnado SJ, Beltramino CA, McDonald AJ, Miselis RR, Yang M, de Olmos J, Heimer L, Alheid GF (2000) Supracapsular bed nucleus of the stria terminalis contains central and medial extended amygdala elements: evidence from anterograde and retrograde tracing experiments in the rat. J Comp Neurol 422:533–555PubMedCrossRefGoogle Scholar
  86. Shammah-Lagnado SJ, Alheid GF, Heimer L (2001) Striatal and central extended amygdala parts of the interstitial nucleus of the posterior limb of the anterior commissure: evidence from tract-tracing techniques in the rat. J Comp Neurol 439:104–126PubMedCrossRefGoogle Scholar
  87. Switzer RC, Hill J, Heimer L (1982) The globus pallidus and its rostroventral extension into the olfactory tubercle of the rat: A cyto- and chemoarchitectural study. Neuroscience 7:1891–1904PubMedCrossRefGoogle Scholar
  88. Switzer R, de Olmos J, Heimer L (1985) The olfactory system. In: Paxinos G (ed) The rat nervous system. Academic, San DiegoGoogle Scholar
  89. Van Hoesen GW, Alheid GF, Heimer L (1989) A survey of major brain structures. In: Kaplan HJ, Sadock BJ (eds) Comprehensive textbook of psychiatry, 5th edn. Lippincott Williams and Wilkins, Baltimore, pp 5–25Google Scholar
  90. Warr WB, de Olmos JS, Heimer L (1981) Horseradish peroxidase: the basic procedure. In: Heimer L, Robards MJ (eds) Neuroanatomical tract-tracing methods. Plenum Press, New York, pp 207–262Google Scholar
  91. Young WS, Alheid GF, Heimer L (1984) The ventral pallidal projection to the mediodorsal thalamus: a study with fluorescent retrograde tracers and immunohistofluorescence. J Neurosci 4:1626–1638PubMedGoogle Scholar
  92. Zaborszky L, Heimer L (1989) Combinations of tracer techniques, especially HRP, with transmitter identification for correlated light and electron microscopic studies. In: Heimer L, Zaborszky L (eds) Tract-tracing methods II. Plenum Press, New York, pp 49–96Google Scholar
  93. Zaborszky L, Beinfeld M, Palkovits M, Heimer L (1984a) Brainstem projection to the hypothalamic ventromedial nucleus in the rat: a CCK-containing long ascending pathway. Brain Res 303:225–231PubMedCrossRefGoogle Scholar
  94. Zaborszky L, Leranth C, Heimer L (1984b) Ultrastructural evidence of amygdalofugal axons terminating on cholinergic cells of the rostral forebrain. Neurosci Lett 52:219–225PubMedCrossRefGoogle Scholar
  95. Zaborszky L, Alheid GF, Beinfeld MC, Eiden LE, Heimer L, Palkovits M (1985a) Cholecystokinin innervation of the ventral striatum: a morphological and radioimmunological study. Neuroscience 14:427–453PubMedCrossRefGoogle Scholar
  96. Zaborszky L, Alheid GF, Heimer L (1985b) Mapping of transmitter specific connections: simultaneous demonstration of anterograde degeneration and changes in the immunostaining pattern induced by lesions. J Neurosci Methods 14:255–266PubMedCrossRefGoogle Scholar
  97. Zaborszky L, Carlsen J, Brashear HR, Heimer L (1986a) Cholinergic and GABAergic afferents to the olfactory bulb in the rat with special emphasis on the projection neurons in the nucleus of the horizontal limb of the diagonal band. J Comp Neurol 243:488–509PubMedCrossRefGoogle Scholar
  98. Zaborszky L, Heimer L, Eckenstein F, Leranth C (1986b) GABA-ergic input to cholinergic forebrain neurons: an ultrastructural study using retrograde tracing of HRP and double immunolabeling. J Comp Neurol 250:282–295PubMedCrossRefGoogle Scholar
  99. Zahm DS, Heimer L (1985) Synaptic contacts of ventral striatal cells in the olfactory tubercle of the rat: correlated light microscopy and EM of anterogradely transported Phaseolus vulgaris-leucoagglutinin (PHA-L). Neurosci Lett 60:169–175PubMedCrossRefGoogle Scholar
  100. Zahm DS, Heimer L (1987) The ventral striatopallidothalamic projection. III. Striatal cells of the olfactory tubercle establish direct synaptic contract with ventral pallidal cells projecting to mediodorsal thalamus. Brain Res 404:327–331PubMedCrossRefGoogle Scholar
  101. Zahm DS, Heimer L (1988) Ventral striatopallidal parts of the basal ganglia in the rat. I. Neurochemical compartmentations reflected by the distribution of neurotensin and substance P immunoreactivity. J Comp Neurol 272:516–535PubMedCrossRefGoogle Scholar
  102. Zahm DS, Heimer L (1990) Two transpallidal pathways originating in rat nucleus accumbens. J Comp Neurol 302:437–446PubMedCrossRefGoogle Scholar
  103. Zahm DS, Heimer L (1993) Specificity in the efferent projections of the nucleus accumbens in the rat: comparison of the rostral pole projection patterns with those of the core and shell. J Comp Neurol 327:220–232PubMedCrossRefGoogle Scholar
  104. Zahm DS, Zaborszky L, Alones VE, Heimer L (1985) Evidence for the coexistence of glutamate decarboxylase and met-enkephalin immunoreactivities in axon terminals of rat ventral pallidum. Brain Res 325:317–321PubMedCrossRefGoogle Scholar
  105. Zahm DS, Zaborszky L, Alheid GF, Heimer L (1987) The ventral striatopallidothalamic projection. II. The ventral pallido-thalamic link. J Comp Neurol 255:592–605PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Suzanne N. Haber
    • 1
  • Jacqueline F. McGinty
    • 2
  • Enrico Mugnaini
    • 3
  • Laszlo Zaborszky
    • 4
    Email author
  1. 1.Department of Pharmacology and PhysiologyUniversity of Rochester School of Medicine and DentistryRochesterUSA
  2. 2.Department of Neurosciences, Psychiatry and Behavioral SciencesMedical University of South CarolinaCharlestonUSA
  3. 3.Institute for NeuroscienceNorthwestern UniversityChicagoUSA
  4. 4.Center for Molecular and Behavioral NeuroscienceRutgers, The State University of New JerseyNewarkUSA

Personalised recommendations