The Basal Forebrain Corticopetal System Revisited
Corresponding Author
L. ZABORSZKY
Center for Molecular and Behavioral Neuroscience, Newark, New Jersey
Address for correspondence: Laszlo Zaborszky, M.D., Ph.D., Center for Molecular and Behavioral Neuroscience, Rutgers Univeristy, 197 University Ave., Newark, NJ 07102, USA. Voice: 973-353-1080 ext. 3181; fax: 973-353-1272; [email protected]Search for more papers by this authorK. PANG
Department of Psychology, Bowling Green State University, Bowling Green, Ohio
Search for more papers by this authorJ. SOMOGYI
Flinders University, Faculty of Health Sciences, Bedford Park, Australia
Search for more papers by this authorZ. NADASDY
Center for Neural Computation, The Hebrew University, Jerusalem, Israel
Search for more papers by this authorI. KALLO
Department of Anatomy, King's College London, United Kingdom
Search for more papers by this authorCorresponding Author
L. ZABORSZKY
Center for Molecular and Behavioral Neuroscience, Newark, New Jersey
Address for correspondence: Laszlo Zaborszky, M.D., Ph.D., Center for Molecular and Behavioral Neuroscience, Rutgers Univeristy, 197 University Ave., Newark, NJ 07102, USA. Voice: 973-353-1080 ext. 3181; fax: 973-353-1272; [email protected]Search for more papers by this authorK. PANG
Department of Psychology, Bowling Green State University, Bowling Green, Ohio
Search for more papers by this authorJ. SOMOGYI
Flinders University, Faculty of Health Sciences, Bedford Park, Australia
Search for more papers by this authorZ. NADASDY
Center for Neural Computation, The Hebrew University, Jerusalem, Israel
Search for more papers by this authorI. KALLO
Department of Anatomy, King's College London, United Kingdom
Search for more papers by this authorAbstract
ABSTRACT: The medial septum, diagonal bands, ventral pallidum, substantia innominata, globus pallidus, and internal capsule contain a heterogeneous population of neurons, including cholinergic and noncholinergic (mostly GABA containing), corticopetal projection neurons, and interneurons. This highly complex brain region, which constitutes a significant part of the basal forebrain has been implicated in attention, motivation, learning, as well as in a number of neuropsychiatric disorders, such as Alzheimer's disease, Parkinson's disease, and schizophrenia. Part of the difficulty in understanding the functions of the basal forebrain, as well as the aberrant information-processing characteristics of these disease states lies in the fact that the organizational principles of this brain area remained largely elusive. On the basis of new anatomical data, it is proposed that a large part of the basal forebrain corticopetal system be organized into longitudinal bands. Considering the topographic organization of cortical afferents to different divisions of the prefrontal cortex and a similar topographic projection of these prefrontal areas to basal forebrain regions, it is suggested that several functionally segregated cortico-prefronto-basal forebrain-cortical circuits exist. It is envisaged that such specific “triangular” circuits could amplify selective attentional processing in posterior sensory cortical areas.
REFERENCES
- 1 Heimer, L. & 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 Proceedings. M. Santini, Ed.: 177-193. Raven Press. New York.
- 2 Heimer, L., R.D. Switzer & G.W. Van Hoesen. 1982. Ventral striatum and ventral pallidum. Components of the motor system?. Trends Neurosci. 5: 83–87.
- 3 Heimer L., G.F. Alheid & L. Zaborszky. 1985. The basal ganglia. In The Rat Nervous System, Vol. 1. Forebrain and Midbrain. G. Paxinos, Ed.: 37-86. Academic Press. Sydney.
- 4 Heimer L., G.F. Alheid & L. Zaborszky. 1989. Substantia innominata and basal forebrain. In Neuroscience Year. G. Adelman, Ed.: 21-24. Birkhauser. Boston.
- 5 Heimer, L, J. de Olmos, G.F. Alheid & L. Zaborszky. 1991. “Perestroika” in the basal forebrain: opening the border between neurology and psychiatry. Prog. Brain Res. 87: 109–165.
- 6 Zaborszky, L., G.F. Alheid, M.C. Beinfeld, L.E. Eiden, L. Heimer & M. Palkovits. 1985. Cholecystokinin innervation of the ventral striatum: a morphological and radioimmunological study. Neuroscience 14: 427–453.
- 7 Reil, J.C. 1809. Untersuchungen uber den Bau des grossen Gehirn in Menschen. Arch. Psysiol. (Halle) 9: 136–208.
- 8 Brauer, K., A. Schober, J.R. Wolff, E. Winkelman, H. Luppa, H.-J. Luth & H. Bottcher. 1991. Morphology of neurons in the rat basal forebrain nuclei: comparison between NADPH-diaphorase histochemistry and immunohistochemistry of glutamic acid decarboxylase, choline acetyltransferase, somatostatin and parvalbumin. J. Hirnforsch. 32: 1–17.
- 9 Dinopoulos, A., J.G. Parnavelas, H.B.M. Uylings & C.G. Van Eden. 1988. Morphology of neurons in the basal forebrain nuclei of the rat: a Golgi study. J. Comp. Neurol. 272: 461–474.
- 10 Gritti, L., L. Mainville, & B.E. Jones. 1993. Codistribution of GABA-with acetylcholine-synthesizing neurons in the basal forebrain of the rat. J. Comp. Neurol. 329: 438–457.
- 11 Walker, L. C., V.E. Koliatsos, C.A. Kitt, R.T. Richardson, A. Rokaeus &. D.L. Price. 1989. Peptidergic neurons in the basal forebrain magnocellular complex of the rhesus monkey. J. Comp. Neurol. 280: 272–282.
- 12 Zaborszky, L., J. Carlsen, H.R. Brashear & L. Heimer. 1986. 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.
- 13 Price, D.L., P.J. Whitehouse & R.G Struble. 1986. Cellular pathology in Alzheimer's and Parkinson's diseases. Trends Neurosci. 9: 29–33.
- 14 Mesulam, M.M., E.J. Mufson, B.H. Wainer & A.I. Levey. 1983. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10: 1185–1201.
- 15 Vogels, O.J.M., C.A.J. Broere, H.J. ter Laak, H.J. ten Donkelaar, R. Nieuwenhuys & B.P.M. Schulte. 1990. Cell loss and shrinkage in the nucleus basalis Meynert complex in Alzheimer's disease. Neurobiol. Aging 11: 3–13.
- 16 Arendt, T., V. Bigl., A. Tennstedt & A. Arendt. 1985. Neuronal loss in different parts of the nucleus basalis is related to neuritic plaque formation in cortical target areas in Alzheimer's disease. Neuroscience 14: 1–14.
- 17 Mesulam, M.M., E.J. Mufson, A.I. Levey & B.H. Wainer. 1983. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J. Comp. Neurol. 214: 170–197.
- 18 Sofroniew, M.V., F. Eckenstein, H. Thoenen & A.C. Cuello. 1982. Topography of choline acetyltransferase-containing neurons in the forebrain of the rat. Neurosci. Lett. 33: 7–12.
- 19 Armstrong, D.M., C.B. Saper, A.I. Levey, B.H. Wainer & R.D. TERRY. 1983. Distribution of cholinergic neurons in the rat brain demonstrated by immunohistochemical localization of choline acetyltransferase. J. Comp. Neurol. 216: 53–68.
- 20 Rye, D.B., B.H. Weiner, M.-M. Mesulam, E.J. Mufson & C.B. Saper. 1984. Cortical projections arising from the basal forebrain: a study of cholinergic and noncholinergic components combining retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience 13: 627–643.
- 21 Woolf, N.J., F. Eckenstein & L.L. Butcher. 1984. Cholinergic systems in the rat brain. I. Projections to the limbic telencephalon. Brain Res. Bull. 13: 751–784.
- 22 Amaral, D.G. & J. Kurz. 1985. An analysis of the origins of the cholinergic and non- cholinergic septal projections to the hippocampal formation in the rat. J. Comp. Neurol. 240: 37–59.
- 23 Carlsen, J., L. Zaborszky & L. Heimer. 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.
- 24 Luiten, P.G.M., R.P.A. Gaykema, J. Traber & D.G. Spencer. 1987. Cortical projection patterns of magnocellular basal nucleus subdivisions as revealed by anterogradely transported Phaseolus vulgaris leucoaagglutinin. Brain Res. 413: 229–250.
- 25 Gaykema, R.P.A., P.G.M. Luiten, C. Nyakas & J. Traber. 1990. Cortical projection patterns of the medial septum-diagonal band complex. J. Comp. Neurol. 293: 103–124.
- 26 Mesulam, M.M., E.J. Mufson & B.H. Wwiner. 1986. Three-dimensional representation and cortical projection topography of the nucleus basalis (Ch4) in the macaque: concurrent demonstration of choline acetyltransferase and retrograde transport with a stabilized tetramethylbenzidine method for HRP. Brain Res. 367: 301–308.
- 27
Pang, K., J.M. Tepper & L. Zaborszky.
1998. Morphological and electrophysiological characteristics of non-cholinergic basal forebrain neurons.
J. Comp. Neurol.
394: 186–204.
10.1002/(SICI)1096-9861(19980504)394:2<186::AID-CNE4>3.0.CO;2-Z CASPubMedWeb of Science®Google Scholar
- 28 Lynch, B., D. Orosz & L. Zaborszky. 1996. Basal forebrain corticopetal system: 3-D computer graphic reconstruction. Soc. Neurosci. Abstr. 22: 1256.
- 29
Gritti, I., L. Mainville, M. Mancia & B. Jones.
1997. GABAergic and other noncholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat.
J. Comp. Neurol.
383: 163–177.
10.1002/(SICI)1096-9861(19970630)383:2<163::AID-CNE4>3.0.CO;2-Z CASPubMedWeb of Science®Google Scholar
- 30 Poobalasingham, S., K. Pang & L. Zaborszky. 1996. Distribution of neurons containing different type of calcium binding proteins in the cholinergic basal forebrain. Soc. Neurosci. Absrt. 22: 1255.
- 31 Kiss, J., Z. Magloczky, J. Somogyi & T.F. Freund. 1997. Distribution of calretinin containing neurons relative to other neurochemically identified cell types in the medial septum of the rat. Neuroscience 78: 399–410.
- 32 Cullinan, W.E. & L. Zaborszky. 1991. Organization of ascending hypothalamic projections to the rostral forebrain with special reference to the innervation of cholinergic projection neurons. J. Comp. Neurol. 306: 631–667.
- 33 Pearson, R.C.A., K.C. Gatter, P. Brodal & T.P.S. Powell. 1983. The projection of the basal nucleus of Meynert upon the neocortex in the monkey. Brain Res. 259: 132–136.
- 34 Nieuwenhuys, R., L.M.G. Geeraedts & J.G. Veening. 1982. The medial forebrain bundle of the rat. I. General information. J. Comp. Neurol. 206: 49–81.
- 35 Mesulam, M.-M., L.B. Hersh, D.C. Mash & C. Geula. 1992. Differential cholinergic innervation within functional subdivisions of the human cerebral cortex: a choline acetyltransferase study. J. Comp. Neurol. 318: 316–328.
- 36 Mesulam, M.M., L., Volicer, J.K. Marquis, E.J. Mufson & R.C. Green. 1986. Systematic regional differences in the cholinergic innervation of the primate cerebral cortex: distribution of enzyme activities and some behavioral implications. Ann. Neurol. 19: 144–151.
- 37 Lysakowski, A., B.H. Wainer, G.C. Bruce & L.B. Hersh. 1988. An atlas of the regional and laminar distribution of choline acetyltransferase immunoreactivity in rat cerebral cortex. Neuroscience 28: 291–336.
- 38 Houser, C.R., G.D. Crawford, P.M. Salvaterra & J.E. Vaughn. 1985. Immunocytochemical localization of choline acetyltransferase in rat cerebral cortex: a study of cholinergic neurons and synapses. J. Comp. Neurol. 234: 17–34.
- 39 Umbriaco, D., K.C. Watkins, L. Descarries, C. Cozzari & B.K. Hartman. 1994. Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: An electron microscopic study in serial sections. J. Comp. Neurol. 348: 351–373.
- 40 Mrzljak, L., M. Pappy, C. Leranth & P.S. Goldman-Rakic. 1995. Cholinergic synaptic circuitry in the macaque prefrontal cortex. J. Comp. Neurol. 357: 603–617.
- 41 Smiley, J.F., F. Morrell & M.M. Mesulam. 1997. Cholinergic synapses in human cerebral cortex: an ultrastructural study in serial sections. Exp. Neurol. 144: 361–368.
- 42 Beaulieu, C. & P. Somogyi. 1991. Enrichment of cholinergic synaptic terminals on GABAergic neurons and coexistence of immunoreactive GABA and choline acetyltransferase in the same synaptic terminals in the striate cortex of the cat. J. Comp. Neurol. 304: 666–680.
- 43 Xiang, Z., J.R. Huguenard & D.A. Prince. 1998. Cholinergic switching within neocortical inhibitory networks. Science 281: 985–988.
- 44 McCormick, D.A. 1993. Action of acetylcholine in the cerebral cortex and thalamus and implications for function. Prog. Brain Res. 98: 303–308.
- 45 Livingston, M.S. & D.H. Hubel. 1981. Effects of sleep and arousal on the processing of visual information in the cat. Nature 291: 554–561.
- 46 Lewandowski, M.H., C.M. Muller & W. Singer. 1993. Reticular facilitation of cat visual cortical responses is mediated by nicotinic and muscarinic cholinergic mechanisms. Exp. Brain Res. 96: 1–7.
- 47 Muller, C.M., M.H. Lewandowski & W. Singer. 1993. Structures mediating cholinergic reticular facilitation of cortical responses in the cat: effects of lesions in immunocytochemically characterized projections. Exp. Brain Res. 96: 8–18.
- 48 Munk, M.H.J., P.R. Roelsema, P. Konig, A.K. Engel & W. Singer. 1996. Role of reticular activation in the modulation of intracortical synchronization. Science 272: 271–274.
- 49 Sillito, A.M. 1993. The cholinergic modulatory system: an evaluation of its functional roles. Prog. Brain Res. 98: 371–378.
- 50 Freund, T.F. & A.I. Gulyas. 1991. GABAergic interneurons containing calbindin D28k or somatostatin are major targets of GABAergic basal forebrain afferents in the rat neocortex. J. Comp. Neurol. 314: 187–199.
- 51
Jimenez-Capdeville, M.E., R.W. Dykes & A.A. Myasnikov.
1997. Differential control of cortical activity by the basal forebrain in rats: a role for both cholinergic and inhibitory influences.
J. Comp. Neurol.
381: 53–67.
10.1002/(SICI)1096-9861(19970428)381:1<53::AID-CNE5>3.0.CO;2-J CASPubMedWeb of Science®Google Scholar
- 52 Jones, E.G., H. Burton, C.B. Ssper & L. Swanson. 1976. Midbrain, diencephalic and cortical relationships of the basal nucleus of Meynert and associated structures in primates. J. Comp. Neurol. 167: 385–420.
- 53 Mesulam, M.M. & E.J. Mufson. 1984. Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. Brain 107: 253–274.
- 54 Russchen, F.T., D.G. Amaral & J.L. Price. 1985. The afferent connections of the substantia innominata in the monkey, Macaca fascicularis. J. Comp. Neurol. 242: 1–27.
- 55 Irle, E.H. & J. Markowitsch. 1986. Afferent connections of the substantia innominata/ basal nucleus of Meynert in carnivores and primates. J. Hirnforsch. 27: 343–367.
- 56 Grove, E.A., V.B. Domesick & W.J.H. Nauta. 1986. Light microscopic evidence of striatal input to intrapallidal neurons of cholinergic cell group Ch4 in the rat: a study employing the anterograde tracer Phaseolus vulgaris leucoagglutinin (PHAL). Brain Res. 367: 379–384.
- 57 Semba, K., P.B. Reiner, E.G. McGeer & H.C. Fibiger. 1988. Brainstem afferents to the magnocellular basal forebrain studied by axonal transport, immunohistochemistry, and electrophysiology in the rat. J. Comp. Neurol. 267: 433–453.
- 58 Sesack, S. R., A. Y. Deutch, R. H. Roth & B. S. Bunney. 1989. Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 290: 213–242.
- 59 Jones, B.E & A.C. Cuello. 1989. Afferents to the basal forebrain cholinergic cell area from the pontomesencephalic-catecholamine, serotonin, and acetylcholine-neurons. Neuroscience 31: 37–61.
- 60 Hurley, K.M., H. Herbert, M.M. Moga & C.B. Saper. 1991. Efferent projections of the infralimbic cortex of the rat. J. Comp. Neurol. 308: 249–276.
- 61 Zaborszky, L., C. Leranth & L. Heimer. 1984. Ultrastructural evidence of amydalofugal axons terminating on cholinergic cells of the rostral forebrain. Neurosci. Lett. 52: 219–225.
- 62 Zaborszky, L. & W.E. Cullinan. 1989. Hypothalamic axons terminate on forebrain cholinergic neurons: an ultrastructural doublelabeling study using PHAL tracing and ChAT immunochemistry. Brain Res. 479: 177–184.
- 63 Cullinan, W.E. & L. Zaborszky. 1991. Organization of ascending hypothalamic projections to the rostral forebrain with special reference to the innervation of cholinergic projection neurons. J. Comp. Neurol. 306: 631–667.
- 64 Zaborszky, L. & W.E Cullinan. 1992. Projections from the nucleus accumbens to cholinergic neurons of the ventral pallidum: a correlated light and electron microscopic double-immunolabeling study in rat. Brain Res. 570: 92–101.
- 65 Zaborszky, L., W.E. Cullinan & V.N. Luine. 1993. Catecholaminergic-cholinergic interaction in the basal forebrain. Prog. Brain Res. 98: 31–49.
- 66
Zaborszky, L. & W. E Cullinan.
1996. Direct catecholaminergic-cholinergic interactions in the basal forebrain.
I. Dopamine-β-hydroxylase- and tyrosine hydroxylase input to cholinergic neurons. J. Comp. Neurol.
374: 535–554.
10.1002/(SICI)1096-9861(19961028)374:4<535::AID-CNE5>3.0.CO;2-2 CASPubMedWeb of Science®Google Scholar
- 67 Gaykema, R.P.A. & L. Zaborszky. 1996. Direct catecholaminergic-cholinergic interactions in the basal forebrain. II. Substantia nigra and ventral tegmental area projections to cholinergic neurons. J. Comp. Neurol. 374: 555–577.
- 68 Rodrigo, J., P. Fernandez, M.L. Bnetura, J.M. de Velasco, J. Serrano, O. Uttenthal & R. Martinez-Murillo. 1998. Distribution of catecholaminergic afferent fibres in the rat globus pallidus and their relations with cholinergic neurons. J. Chem. Neuroanat. 15: 1–20.
- 69 Henderson, Z. 1997. The projection from the striatum to the nucleus basalis in the rat: an electron microscopic study. Neuroscience 78: 943–955.
- 70 Zaborszky, L., L. Heimer, F. Eckennstein & C. Leranth. 1986. GABAergic input to cholinergic forebrain neurons: an ultrastructural study using retrograde tracing of HRP and double immunolabeling. J. Comp. Neurol. 250: 282–295.
- 71 Chang, H.T., G.R. Penny & S.T. Kitai. 1987. Enkephalinergic-cholinergic interaction in the rat globus pallidus: a pre-embedding double-labeling immunocytochemistry study. Brain Res. 426: 197–203.
- 72 Martinez-Murillo, R., Blasco, I. Alavrez, F.J. Villalba, R. Solano, M.L. Montero-Caballero & J. Rodrigo. 1988. Distribution of enkephalin-immunoreactive nerve fibers and terminals in the region of the nucleus basalis magnocellularis of the rat: a light and electron microscopic study. J. Neurocytol. 17: 361–376.
- 73 Zaborszky, L. 1989. Afferent connections of the forebrain cholinergic projection neurons with special reference to monoaminergic and peptidergic fibers. In Central Cholinergic Synaptic Transmission. M. Frotscher & U. Misgeld, Eds.: 12-22. Birkhauser. Basel.
- 74 Bolam, J.P., C.A. Ingham, P.N. Izzo, A.I. Levey, D.B. Rye, A.D. Smith & B.H. Wainer. 1986. Substance P-containing terminals in synaptic contact with cholinergic neurons in the neostriatum and basal forebrain; a double immunocytochemical study in the rat. Brain Res. 397: 279–289.
- 75 Martinez-Murillo, R., R.M. Villalba & J. Rodrigo. 1990. Immunocytochemical localization of cholinergic terminals in the region of the nucleus basalis magnocellularis of the rat: a correlated light and electron microscopic study. Neuroscience 36: 361–376.
- 76 Csillik, B., P. Rakic & E. Knyihar-Csillik. 1998. Peptidergic innervation and the nicotinic acetylcholine receptor in the primate basal nucleus. Eur. J. Neurosci. 10: 573–585.
- 77 Smiley, J.F. & M.-M. Mesulam. 1998. Cholinergic neurons of the nucleus basalis of Meynert receive cholinergic, catecholaminergic and GABAergic synapses: an electron microscopic investigation in the monkey. Neuroscience 88: 241–254.
- 78 Zaborszky, L., R.P. Gaykema, D.J. Swanson & W.E. Cullinan. 1997. Cortical input to the basal forebrain. Neuroscience 79: 1051–1078.
- 79 Gaykema, R.P.A. & L. Zaborszky. 1997. Parvalbumin-containing neurons in the basal forebrain receive direct input from the substantia nigra-ventral tegmental area. Brain Res. 478: 375–381.
- 80 Zaborszky, L., W.E. Cullinan & A. Braun. 1991. Afferents to basal forebrain cholinergic projection neurons: an update. In Basal Forebrain: Anatomy to Function. T. C. Napier, P.W. Kaliwas & I. Hanin, Eds.: 43-100. Plenum Press. New York.
- 81 Zaborszky, L. 1992. Synaptic organization of basal forebrain cholinergic projection neurons. In Neurotransmitter Interactions and Cognitive Functions. E.D. Levin, M. Decker & L. Butcher, Eds.: 27-65. Birkhauser. Boston.
- 82 Benzing, W.C., J.H. Kordower & E.J. Mufson. 1993. Galanin immunoreactivity within the primate basal forebrain: evolutionary change between monkeys and apes. J. Comp. Neurol. 336: 31–39.
- 83 Burgunder, J.M. & W.S. Young III. 1989. Neurons with neurokinin B mRNA in the rat magnocellular basal nucleus: distribution, projection and colocalization studies. J. Chem. Neuroanat. 2: 239–251.
- 84
Ding, Y.Q., R. Shigemoto, M. Takada, H. Ohishi, S. NAKANISHI & N. MIZUNO.
1996. Localization of the neuromedin K receptor (NK3) in the central nervous system of the rat.
J. Comp. Neurol.
364: 290–310.
10.1002/(SICI)1096-9861(19960108)364:2<290::AID-CNE8>3.0.CO;2-0 CASPubMedWeb of Science®Google Scholar
- 85 Geula, C., C.R. Schatz & M.-M. Mesulam. 1993. Differential localization of NADH-diaphorase and calbindin-D28k within the cholinergic neurons of the basal forebrain, striatum and brainstem in the rat, monkey, baboon and human. Neuroscience 54: 461–476.
- 86 Planas, B., P.E. Kolb, M.A. Raskind & M.A. Miller. 1995. Vasopressin and galanin mRNAs coexist in the nucleus of the horizontal diagonal band: a novel site of vasopressin gene expression. J. Comp. Neurol. 361: 48–56.
- 87 Rance, N.E., W.S. Young III & N.T. McMullen. 1994. Topography of neurons expressing luteinizing hormone-releasing hormone gene transcripts in the human hypothalamus and basal forebrain. J. Comp. Neurol. 339: 573–586.
- 88 Sobreviela, T., S. Jaffar & E.J. Mufson. 1998. Tyrosine kinase A, galanin and nitric oxide synthase within basal forebrain neurons in the rat. Neuroscience 87: 447–461.
- 89 Sugaya, K. & M. McKinney. 1994. Nitric oxide synthase gene expression in cholinergic neurons in the rat brain examined by combined immunocytochemistry and in situ hybridization histochemistry. Mol. Brain Res. 23: 111–125.
- 90 Everitt, B.J. & T.W. Robbins. 1997. Central cholinergic systems and cognition. Annu. Rev. Psychol. 48: 649–684.
- 91 Dunnett, S.B., B.J. Everitt & T.W. Robbins. 1991. The basal forebrain-cortical cholinergic system: interpreting the functional consequences of excitotoxic lesions. Trends Neurosci. 14: 494–501.
- 92 Voytko, M.L., D.S. Olton, R.T. Richardson, L.K. Gorman, J.R. Tobin & D.L. Price. 1994. Basal forebrain lesions in monkeys disrupt attention but not learning and memory. J. Neurosci. 14: 167–186.
- 93 Parasuraman, R., P.M. Greenwood, J.V. Haxby & C.L. Grady. 1992. Visuospatial attention in dementia of the Alzheimer type. Brain 115: 711–733.
- 94 Stoehr, J.D., S.L. Mobley, D. Roice, R. Brooks, L.M. Baker, R.G. Wiley & G.L. Wenk. 1997. The effects of selective cholinergic basal forebrain lesions and aging upon expectancy in the rat. Neurobiol. Learn. Mem. 67: 214–227.
- 95 Turchi, J. & M. Sarter. 1997. Cortical acetylcholine and processing capacity: effects of cortical cholinergic deafferentation on crossmodal divided attention in rats. Cogn. Brain Res. 6: 147–158.
- 96 Pang, K., M.J. Williams, H. Egeth & D.S. Olton. 1993. Nucleus basalis magnocellularis and attention: effects of muscimol infusions. Behav. Neurosci. 107: 1031–1038.
- 97 Muir, J.L., B.J. Everitt & T.W. Robbins. 1994. AMPA-induced excitotoxic lesions of the basal forebrain: a significant role for the cortical cholinergic system in attentional function. J. Neurosci. 4: 12313–2326.
- 98 Baxter, G.M & M. Gallagher. 1997. Cognitive effects of selective loss of basal forebrain cholinergic neurons: implications for cholinergic therapies of Alzheimer's disease. In Pharmacological Treatment of Alzheimer's Disease: Molecular and Neurobiological Foundations. J.E. Brioni & M.W. Decker, Eds.: 87-103. Wiley-Liss, Inc. New York.
- 99 Paus, T., R.J. Zatorre, N. Hofle, Z. Caramanos, J. Gotman, M. Petrides & A.C. Evans. 1997. Time-related changes in neural systems underlying attention and arousal during the performance of an auditory vigilance task. J. Cogn. Neurosci 9: 392–408.
- 100 Bakin, J.S. & N.W. Weinberger. 1996. Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc. Natl. Acad. Sci. USA 93: 11219–11224.
- 101 Edeline, J.-M., B. Hars et al. 1994. Transient and prolonged facilitation of tone-evoked responses induced by basal forebrain stimulations in the rat auditory cortex. Exp. Brain Res. 97: 373–386.
- 102 Metherate, R. & J.H. Ashe. 1991. Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors. Brain Res. 559: 163–167.
- 103 Tremblay, N., R.A. Warren & R.W. Dykes. 1990. Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. II. Cortical neurons excited by somatic stimuli. J. Neurophysiol. 64: 1212–1222.
- 104 Maalouf, M., A.A. Miasnikov & R.W. Dykes. 1998. Blockade of cholinergic receptors in rat barrel cortex prevents long-term changes in the evoked potential during sensory preconditioning. J. Neurophysiol. 80: 529–545.
- 105 Sachdev, R.N.S., S.M. Lu, R.G. Wiley & F.F. Ebner. 1998. Role of the basal forebrain cholinergic projection in somatosensory cortical plasticity. J. Neurophysiol. 79: 3216–3228.
- 106 Baskerville, K.A., J.B. Schweitzer & P. Herron. 1997. Effects of cholinergic depletion on experience-dependent plasticity in the cortex of the rat. Neuroscience 80: 1159–1169.
- 107 Juliano, S.L., W. MA M.F. Bear & D. Eslin. 1990. Cholinergic manipulation alters stimulus-evoked metabolic activity in cat somatosensory cortex. J. Comp. Neurol. 297: 106–120.
- 108 Kilgard, M.P. & M.M. Merzenich. 1998. Cortical map reorganization enabled by nucleus basalis activity. Science 279: 1714–1718.
- 109 Morris, J.S., K.J. Friston & R.J. Dolan. 1998. Experience-dependent modulation of tonotopic neural responses in human auditor cortex. Proc. R. Soc. Lond. B. 265: 649–657.
- 110 Posner, M.I. & M.E. Raichle. 1997. Images of Mind. Scientific American Library. New York.
- 111 Laberge, D. 1995. Attentional Processing. Harvard University Press. Cambridge, MA. p. 262.
- 112 Heilman, K.H., R.T. Watson & E. Valenstein. 1993. Neglect and related disorders. In Clinical Neuropsychology. K.M. Heilman & E. Valenstein, Eds.: 279-336. Oxford University Press. New York.
- 113 Roland, P.E. 1994. Brain Activation. Wiley-Liss. New York. p. 589.
- 114 Mesulam, M-M. 1990. Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann. Neurol. 28: 597–613.
- 115 Detari, L., K. Semba & D.D. Rasmusson. 1997. Responses of cortical EEG-related basal forebrain neurons to brainstem and sensory stimulation in urethane-anaesthetized rats. Eur. J. Neurosci. 9: 1153–1161.
- 116 Jones, B.E. & M. Muhlataler. 1999. Cholinergic and GABAergic neurons of the basal forebrain: Role in cortical activation. In Handbook of Behavioral State Control. R. Lydic & A.A. Baghdoyan, Eds.: 213-233. CRC Press. Boca Raton, FL.
- 117 Steriade, M., E.G. Jones & D.A. McCormick. 1997. Thalamus. Vol. 1. Organization and Function. Elsevier. Amsterdam. p. 959.
- 118 Sarter, M. & J.P. Bruno. 1997. Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res. Rev. 23: 28–46.
- 119 Aston-Jones, G., J. Rajkowski, P. Kubiak & T. Alexinsky. 1994. Locus coeruleus neurons in monkey are selectively activated by attended cues in a vigilance task. J. Neurosci. 14: 4467–4480.
- 120 Faiers, A.A. & G.J. Mogenson. 1976. Electrophysiological identification of neurons in locus coeruleus. Exp. Neurol. 53: 254–266.
- 121 Maho, C., B. Hars, J-M. Edeline & E. Hennevin. 1995. Conditioned changes in the basal forebrain: relations with learning-induced cortical plasticity. Psychobiology 23: 10–25.
- 122 Woods, D.L. 1990. The physiological basis of selective attention: implications of event-related potential studies. In Event-Related Brain Potentials: Issues and Interdisciplinary Vantages. J. W. Rohrbaugh, R. Johnson & R. Parasuraman, Eds.: 178-209. Oxford University Press. New York.
- 123 VanEden, C.G., V.A.F. Lamme & H.B.M. Uylings. 1991. Heterotopic cortical afferents to the medial prefrontal cortex in the rat. A combined retrograde and anterograde tracer study. Eur. J. Neurosci. 4: 77–97.
- 124 Felleman, D.J. & D.C. Van Essen. 1991. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1: 1–47.
- 125 Pandya, D.N. & E.H. Yeterian. 1985. Architecture and connections of cortical association areas. In Cerebral Cortex. Vol. 4. A. Peters & E.G. Jones, Eds.: 3-61. Plenum Press. New York.
- 126 Alexzander, G.E., &M.D. Crutcher. 1990. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 13: 266–271.
- 127 Momiyama, T. & J.A. Sim. 1996. Modulation of inhibitory transmission by dopamine in rat basal forebrain nuclei: activation of presynaptic D1-like dopaminergic receptors. J. Neurosci. 16: 7505–7512.
- 128 Alonso, A. 1999. Intrinsic electroresponsiveness of basal forebrain cholinergic and non-cholinergic neurons. In Handbook of Behavioral State Control. R. Lydic & A.A. Baghdoyan, Eds.: 297-309. CRC Press. Boca Raton, FL.
- 129 Paxinos, G. & C. Watson. 1998. The Rat Brain in Stereotaxic Coordinates. Academic Press. San Diego, CA.
- 130
Henderson, Z. & N. Morris.
1997. Galanin-immunoreactive synaptic terminals on basal forefrain neurons in the rat.
J. Comp. Neurol.
383: 82–93.
10.1002/(SICI)1096-9861(19970623)383:1<82::AID-CNE7>3.0.CO;2-H CASPubMedWeb of Science®Google Scholar