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Lennart Heimer: in memoriam (1930–2007)

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Notes

  1. Schimert 1936; Szentagothai-Schimert 1941.

  2. Nauta and Gygax 1954; Nauta 1957.

  3. Bob Switzer, one of Lennart’s coworkers in the late 1970s founded one of the most successful biotech company (NeuroScience Associates) in part in response to this need.

  4. He was especially fond of the various combined techniques that facilitate direct rather than indirect identification of a nerve element or chains of connections in their natural environment (Hardy et al. 1976; de Olmos and Heimer 1980; Alheid et al. 1984a, b; Zaborszky et al. 1985b; Zaborszky and Heimer 1989; Schmued et al. 1990). The chapters, including his own with his coworkers, in the two editions of ‘Neuroanatomical Tract-tracing’ (Heimer and Robards 1981; Heimer and Zaborszky 1989) had a tremendous impact on neuroscience and are still among the most frequently consulted laboratory textbooks. Although he was not able to participate in the preparation of the third edition (Zaborszky, Wouterlood, Lanciego, editors, Springer 2006), he was keenly interested and summarized his thoughts in a ‘Short Retrospection’ as an introduction to the original contributions of this volume (Heimer 2006).

  5. The olfactory tubercle is located on the base of the brain and using dorsal approach, the accidental damage to structures that are penetrated by the electrode would complicate the interpretation of the results due to the ‘fibers of passage’ problem caused by lesions, therefore Lennart used a heat lesion apparatus (Heimer and Lohman 1976) to produce superficial lesion and a ventral approach aided by his stereotaxic apparatus, he developed with Knut Larsson (Heimer et al. 1971).

  6. DeLong and Georgopoulos 1981; Alexander et al. 1986.

  7. See recent discussion in Voorn et al., TINS, 27 (8) 2004.

  8. See in more detail the Introduction and the relevant chapters in the Advancing from the Ventral Striatum to the Extended Amygdala. Implications for neuropsychiatry and drug abuse. A NYAS conference in honor of Lennart Heimer. vol 877, Ann N Y Acad Sci 1999 (edited by McGinty). Also, see the paper of Walker and Davis and Smith and Aston-Jones in this volume.

  9. Using the cupric-silver technique of de Olmos (1969), the gray matter located in the subpallidal (sublenticular) substantia innominata shows similar staining pattern as the bed nucleus of the stria terminalis and the centromedial amygdala (de Olmos 1972). Jose de Olmos passed away in January 2008, just a few days after he submitted his paper for this special issue as a tribute to his friend, Lennart Heimer.

  10. He argued that the term substantia innominata was too vague and should be abandoned since parts of it belongs to better characterized nearby systems, such as the ventral striato-pallidal system, the nucleus basalis and the extended amygdala.

Publications of Lennart Heimer

Books

  • 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)

  • Heimer L (1983) The human brain and spinal cord: functional neuroanatomy and dissection guide. Springer, New York

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  • Heimer L (1995) The human brain and spinal cord: functional neuroanatomy and dissection guide. Springer, New York

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  • Heimer L, Robards MJ (eds) (1981) Neuroanatomical tract-tracing methods. Plenum Press, New York

  • Heimer L, Zaborszky L (eds) (1989) Neuroanatomical tract-tracing methods 2. Recent progress. Plenum Press, New York

  • 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, Amsterdam

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Instructional video

  • Heimer L (1990) Dissection of the human brain: a Videotape Teaching Program. Springer/GmbH & Co KG, Berlin/Mainz

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  • Heimer L (2007) Dissection of the human brain. Sinauer Associates, Sunderland. (DVD)

Journal articles and book chapters

  • Alheid GF, Heimer L (1996) Theories of basal forebrain organization and the “emotional motor system”. Prog Brain Res 107:461–484

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  • 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 27:1–39

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  • 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 292:17–22

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  • Alheid GF, Carlsen J, Heimer L (1984b) An algebraic approach to the detection of multiple markers in complex neuronal systems. J Neurosci Methods 10:71–77

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  • 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 26–95

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  • Alheid GF, Heimer L, Switzer RD (1990) The basal ganglia. In: Paxinos G (ed) The human nervous system. Academic, San Diego, pp 483–581

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  • 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 84:967–996

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  • 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 706:37–46

  • 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 101–132

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  • 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 1–54

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  • Brashear HR, Zaborszky L, Heimer L (1986) Distribution of GABAergic and cholinergic neurons in the diagonal band. Neuroscience 17:439–451

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  • 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 54:319–334

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  • 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 244:121–36

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  • 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 374:375–379

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  • Carlsen J, Heimer L (1988) The basolateral amygdaloid complex as a cortical-like structure. Brain Res 441:377–380

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  • 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 208:196–208

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  • 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 234:155–167

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  • 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 581:39–45

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  • de Olmos JS, Heimer L (1978) Mapping of collateral projections with the HRP-method. Neurosci Lett 6:107–114

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  • 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 19:7–12

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  • de Olmos JS, Heimer L (1999) The concepts of the ventral striatopallidal system and extended amygdala. Ann N Y Acad Sci 877:1–32

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  • 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 181:213–244

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  • 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 117–170

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  • Ebbesson SOE, Heimer L (1970) Projections of the olfactory tract fibers in the nurse shark (Ginglymostoma cirratum). Brain Res 17:47–55

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  • 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 4:369–374

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  • 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 5:235–240

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  • Hardy H, Heimer L, Switzer R, Watkins D (1976) Simultaneous demonstration of horseradish peroxidase and acetylcholinesterase. Brain Res Newsl 3:1–5

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  • Heimer L (1967) Silver impregnation of terminal degeneration in some forebrain fiber systems: a comparative evaluation of current methods. Brain Res 5:86–108

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  • Heimer L (1968a) Synaptic distribution of centripetal and centrifugal nerve fibers in the olfactory system of the rat. An experimental anatomical study. J Anat 103:413–432

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  • Heimer L (1968b) The tracing of pathways in the central nervous system. Proc IEEE 56:950–959

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  • Heimer L (1969a) Silver impregnation of degenerating axons and their terminals on Epon-Araldite sections. Brain Res 12:246–249

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  • 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 167:129–146

  • 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 162–172

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  • Heimer L (1970b) Selective silver impregnation of degenerating axoplasm. In: Nauta WJH, Ebbesson SOE (eds) Contemporary research methods in neuroanatomy. Springer, New York, pp 106–131

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  • Heimer L (1971) Pathways of the brain. Sci Am 225:48–60

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  • 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 6:484–523

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  • Heimer L (1975) Olfactory projections to the diencephalons. In: Stumpf W, Grant L (eds) Handbook of neuroendocrinology. Karger, Basel, pp 30–39

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  • 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 96–187

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  • Heimer L (1987) Neuroanatomical tract-tracing methods. In: Adelman G (ed) Encyclopedia of neurosciences. Birkhauser, Boston 3:766–769

  • Heimer L (1999) The third quarter of the twentieth century; the golden age of the silver methods. Brain Res Bull 50:399–400

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  • Heimer L (2000) Basal forebrain in the context of schizophrenia. Brain Res Brain Res Rev 31:205–235

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  • Heimer L (2003a) A new anatomical framework for neuropsychiatric disorders and drug abuse. Am J Psychiatry 160:1726–1739

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  • 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 44:189–201

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  • 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 1–5

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  • 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, 295:1–42

  • Heimer L, Alheid GF (1996) Basal forebrain organization; emerging concepts. Encyclopedia of neuroscience, 2nd edn. Elsevier, Amsterdam

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  • Heimer L, Ekholm R (1967) Neuronal argyrophilia in early degenerative states: a light- and electronmicroscopical study of the Glees and Nauta techniques. Experientia 23:237–239

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  • 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 178:559–609

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  • Heimer L, Larsson K (1964) Drastic changes in the mating behavior of male rats following lesions in the junction of diencephalons and mesencephalon. Experientia 20:460–461

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  • Heimer L, Larsson K (1965) Mating behavior in male rats after destruction of the mammillary bodies. Acta Neurol Scand 40:353–360

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  • Heimer L, Larsson K (1966–1967) Impairment of mating behavior in male rats following lesions in the preoptic-anterior hypothalamic continuum. Brain Res 3:248–263

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  • Heimer L, Larsson K (1967) Mating behavior of male rats after olfactory bulb lesions. Physiol Behav 2:207–209

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  • 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 73–106

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  • Heimer L, Nauta WJ (1969) The hypothalamic distribution of the stria terminalis in the rat. Brain Res 13:284–297

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  • Heimer L, Peters A (1968) An electron microscope study of a silver stain for degenerating boutons. Brain Res 8:337–346

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  • Heimer L, van Hoesen G (1979) Ventral striatum. In: Divac J, Oberg RGE (eds) The neostriatum. Pergamon Press, Oxford, NY, pp 147–158

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  • Heimer L, Van Hoesen GW (2006) The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neurosci Biobehav Rev 30:126–147

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  • 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 6:89–99

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  • Heimer L, Wilson RD (1975) The subcortical projections of the allocortex. In: Santini M (ed) Golgi centennial symposium. Raven Press, New York, pp 177–193

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  • Heimer L, Ebner FF, Nauta WJH (1967) A note on the termination of commissural fibers in neocortex. Brain Res 5:171–177

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  • Heimer L, Kuikka V, Larsson K, Nordstrom E (1971) A headholder for stereotaxic operations of small laboratory animals. Physiol Behav 7:263–264

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  • Heimer L, Robards M, Switzer RC III (1976) The olfactory tubercle: a structure of varying stratification. Exp Brain Res (Suppl 1):141–147

  • Heimer L, Van Hoesen GW, Rosene DL (1977) The olfactory pathways and the anterior perforated substance in the primate brain. Int J Neurol 12:42–52

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  • Heimer L, Switzer RD, van Hoesen GW (1982) Ventral striatum and ventral pallidum: additional components of the motor system? Trends Neurosci 5:83–87

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  • Heimer L, Alheid G, Zaborszky L (1985) The basal ganglia. In: Paxinos G (ed) The rat nervous system. Academic, San Diego

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  • 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 255:571–591

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  • Heimer L, Alheid GF, Zaborszky L (1989) Substantia innominata and basal forebrain. In: Edelman G (ed) Neuroscience year. Birkhauser, Boston, pp 21–24

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  • 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 34:707–731

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  • 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 87:109–165

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  • Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C (1991b) Specificity in the projection patterns of accumbal core and shell. Neuroscience 41:89–125

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  • 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 1–43

  • Heimer L, Zahm DS, Alheid GF (1995) Basal ganglia. In: Paxinos (ed) The rat nervous system, 2nd edn. Academic, San Diego, pp 579–628

  • 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 9:354–381

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  • 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 76:957–1006

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  • 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 57–226

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  • Keefer DA, Chung JW, Heimer L (1980) Morphology and ultrastructure of anterior thalamic neurons solidly labeled with horseradish peroxidase. Brain Res 191:301–311

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  • Larsson K, Heimer L (1964) Mating behavior of the male rat after lesions in the preoptic area. Nature 202:413–414

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  • Millhouse OE, Heimer L (1984) Cell configuration in the olfactory tubercle of the rat. J Comp Neurol 227:571–597

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  • Pohorecky LA, Zigmond MJ, Heimer L, Wurtman RJ (1969) Olfactory bulb removal: effects on brain norepinephrine. Proc Natl Acad Sci USA 62:1052–1055

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  • 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 1–55

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  • Schmued L, Heimer L (1990) Iontophoretic injection of fluoro-gold and other fluorescent tracers. J Histochem Cytochem 38:721–723

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  • Schmued LC, Kyrihidis K, Heimer L (1990) In vivo anterograde and retrograde axonal transport of fluorescent rhodamine-dextran-amines within the CNS. Brain Res 526:127–134

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  • Shammah-Lagnado SJ, Alheid GF, Heimer L (1996) Efferent connections of the caudal part of the globus pallidus in the rat. J Comp Neurol 376:489–507

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  • 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 94:1097–1123

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  • 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 422:533–555

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  • 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 439:104–126

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  • 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 7:1891–1904

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  • 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 207–262

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  • 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 4:1626–1638

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  • 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 49–96

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  • 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 303:225–231

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  • Zaborszky L, Leranth C, Heimer L (1984b) Ultrastructural evidence of amygdalofugal axons terminating on cholinergic cells of the rostral forebrain. Neurosci Lett 52:219–225

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  • 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 243:488–509

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  • 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 250:282–295

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  • 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 404:327–331

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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.

Author information

Authors and Affiliations

  1. Department of Pharmacology and Physiology, University of Rochester School of Medicine and Dentistry, 601 Elmwood Avenue, Rochester, NY, 14642, USA

    Suzanne N. Haber

  2. Department of Neurosciences, Psychiatry and Behavioral Sciences, Medical University of South Carolina, 173 Ashley Avenue BSB 403, Charleston, SC, 29425, USA

    Jacqueline F. McGinty

  3. Institute for Neuroscience, Northwestern University, 303 East Chicago Avenue, Chicago, IL, 60611-3008, USA

    Enrico Mugnaini

  4. Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, 197 University Avenue, Newark, NJ, 07102, USA

    Laszlo Zaborszky

Authors
  1. Suzanne N. Haber
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  2. Jacqueline F. McGinty
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  3. Enrico Mugnaini
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  4. Laszlo Zaborszky
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Correspondence to Laszlo Zaborszky.

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Haber, S.N., McGinty, J.F., Mugnaini, E. et al. Lennart Heimer: in memoriam (1930–2007). Brain Struct Funct 213, 3–10 (2008). https://doi.org/10.1007/s00429-008-0194-0

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