Abstract
The basal forebrain (BF) is comprised of a neurochemically heterogeneous population of neurons, including cholinergic, GABA-ergic, peptidergic, and possibly glutamatergic neurons, that project to the cerebral cortex, thalamus, amygdala, posterior hypothalamus and brain stem. This multitude of ascending and descending pathways participate in a similarly bewildering number of functions, including cognition, motivation, emotion, and autonomic regulation. Traditional anatomical methods failed to grasp the basic organizational principles of this brain area and likened it at best to the organization of the brain stem reticular formation. Our studies, using various computational methods for analyzing the spatial distribution and numerical relations of different chemically and hodologically characterized neuronal populations, as well as fully reconstructed electrophysiologically identified single neurons, began to unravel the organizational principles of the BF. According to our model, the different cell types form large-scale cell sheets that are aligned to each other in a specific manner Within each cell system, the neurons display characteristic discontinuous distributions, including high density clusters. As a result of nonhomogeneity within individual cell populations and partial overlapping between different cell types, the space containing the bulk of cholinergic neurons comprises a mosaic of various size cell clusters. The composition, dendritic orientation, and input—output relationships of these high density cell clusters show regional differences. It is proposed that these clusters represent specific sites (modules) where information processed in separate streams can be integrated. Via this BF mechanism a topographically organized prefrontal input could allocate attentional resources to cortical associational areas in a selective self-regulatory fashion.
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References
Dunnett SB, Fibiger HC. Role of forebrain cholinergic system in learning and memory: relevance to the cognitive deficits of aging and Alzheimer’s dementia. Progr Brain Res 1993; 98: 413–420.
Everitt BJ., Robbins TW. Central cholinergic systems and cognition. Annu Rev Psychol 1997; 48: 649–684.
Heimer L, de Olmos J, Alheid GF, Zaborszky L. “Perestroika” in the basal forebrain; opening the border between neurology and psychiatry. Progr Brain Res 1991; 87: 109–165.
Zaborszky L, Pang K, Somogyi J, Nadasdy Z, Kallo I. The basal forebrain corticopetal system revisited. Ann NY Acad Sci 1999; 877: 339–367.
Jones BE, Muhlethaler M. Cholinergic and GABAergic neurons of the basal forebrain: role in cortical activation. In: Handbook of Behavioral State Control—Cellular and Molecular Mechanisms ( Lydic R, Baghdoyan HA, eds.) CRC Press, New York, 1999, pp. 213–234.
de Lacalle S, Saper CB. The cholinergic system in the primate brain: Basal forebrain and pontine-tegmental cell groups. In: Handbook of Chemical Neuroanatomy. The Primate Nervous System, Part I ( Bloom FE, Bjorklund A, Hokfelt T, eds.) Elsevier, New York, 1997, pp. 217–252.
Geula C, Mesulam MM. Cholinergic systems and related neuropathological predilection patterns in Alzheimer disease. In: Alzheimer Disease ( Terry RD, Katzman R, Bick KL, eds.) Raven Press, New York, 1994, pp. 263–291.
Swaab DF. Neurobiology and neuropathology of the human hypothalamus. In: The Primate Nervous System, Part I. Handbook of Chemical Neuroanatomy, Vol. 13 ( Bloom FE, Bjorklund A, Hokfelt T, eds.) Elsevier, New York, 1997, pp. 39–118.
Whitehouse PJ, Price DL, Struble RG, Clark AW, Coyle JT, Delong MR. Alzheimer’s disease and senile dementia: loss of neurons in the basal forebrain. Science 1982; 215: 1237–1239.
Gritti I, Mainville L, Mancia M, Jones B. GABAergic and other noncholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat. J Comp Neurol 1997; 383: 163–177.
Zaborszky L. Afferent connections of the forebrain cholinergic projection neurons, with special reference to monoaminergic and peptidergic fibers. In: Central Cholinergic Synaptic Transmission (Frotscher M, Misgeld U, eds.) Birkhauser, Basel, 1989, pp. 12–32
Heilman KH, Watson RT, Valenstein E. Neglect and related disorders. In: Clinical Neuropsychology ( Heilman KM, Valenstein E, eds.) Oxford University Press, New York, 1993, pp. 279–336.
Mesulam MM. Attentional networks, confusional states, and neglect syndromes. In: Principles of Behavioral and Cognitive Neurology ( Mesulam, M.M., ed.), Oxford University Press, New York, 2000, pp. 174–293.
McGaughy J, Everitt BJ, Robbins TW, Sarter M. The role of cortical cholinergic afferent projections in cognition: impact of new selective immunotoxins. Behav Brain Res 2000; 115: 251–263.
Szentagothai J. The modular architectonic principle of neural centers. Rev Physiol Biochem Pharmacol 1983; 98: 11–61.
Gerfen CR. The neostriatal mosaic. I. Compartmental organization of projections from the striatum to the substantia nigra in the rat. J Comp Neurology 1985; 236: 454–476.
Bjaalie JG, Diggle PJ, Nikundiwe A, Karagulle T, Brodal P. Spatial segregation between populations of ponto-cerebellar neurons: statistical analysis of multivariate interactions. Anat Rec 1991; 231: 510–523.
Graybiel AM, Penney JB. Chemical architecture of the basal ganglia. In: The Primate Nervous System, Part III, Handbook of Chemical Neuroanatomy, Vol. 15 ( Bloom FE, Bjorklund A, Hokfelt T, eds.) Elsevier, Amsterdam, 1999, pp. 227–284.
Mountcastle VB. Perceptual Neuroscience. The Cerebral Cortex. Harvard University Press, Cambridge, MA, 1998.
Malach R. Dendritic sampling across processing streams in monkey striate cortex. J Comp Neurol 1992; 31: 303–312.
He S-Q, Dum RP, Strick PL. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J Neurosci 1993; 13: 952–980.
Malach R. Cortical columns as devices for maximizing neuronal diversity. Trends Neurosci 1994; 17: 101–104.
Malmierca MS, Blackstad TW, Osen KK, Karagulle T, Molowny RL. The central nucleus of the inferior colliculus in rat: a Golgi and computer reconstruction study of neuronal and laminar structure. J Comp Neurol 1993; 333: 1–27.
Malmierca MS, Leergard TB, Bajo VM, Bjaalie JG, Merchan MA. Anatomic evidence of a three-dimensional mosaic pattern of tonotopic organization in the ventral complex of the lateral lemniscus in cat. J Neurosci 1998; 18: 10603–10618.
Leergaard BT, Alloway KD, Mutic JJ, Bjaalie JG. Three-dimensional topography of corticopontine projections from rat barrel cortex: correlations with corticostriatal organization. J Neurosci 2000; 20: 8474–8484.
Jacobs GA, Theunissen FE. Extraction of sensory parameters from a neural map by primary sensory interneurons. J Neurosci 2000; 20: 2934–2943.
Sofroniew MV, Eckenstein F, Thoenen H, Cuello AC. Topography of choline acetyltransferase-containing neurons in the forebrain of the rat. Neurosci Lett 1982; 33: 7–12.
Armstrong DM, Saper CB, Levey AI, Wainer BH, Terry RD. Distribution of cholinergic neurons in the rat brain demonstrated by immunohistochemical localization of choline acetyltransferase. J Comp Neurol 1983; 216: 53–68.
Mesulam MM, Mufson EJ, Wainer BH, Levey AI. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Chl-Ch6). Neuroscience 1983; 10: 1185–1201.
Rye DB, Wainer BH, Mesulam M-M, Mufson EJ, Saper CB. Cortical projections arising from the basal forebrain: a study of cholinergic and noncholinergic components combining retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience 1984; 13: 627–643.
Amaral DG, Kurz J. An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation in the rat. J Comp Neurol 1985; 240: 37–59.
Carlsen J, Zaborszky L, Heimer L. Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: a combined retrograde fluorescent and immunohistochemical study. J Comp Neurol 1985; 234: 155–167.
Zaborszky L, Carlsen J, Brashear HR, Heimer L. 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 1986; 243: 488–509.
Woolf NJ. Cholinergic system in mammalian brain and spinal cord. Progr Neurobiol 1991; 37: 475–524.
Wainer BH, Steininger TL, Roback JD, Burke-Watson MA, Mufson EJ, Kordower J. Ascending cholinergic pathways: functional organization and implications for disease models. Progr Brain Res 1993; 98: 9–30.
Mesulam MM, Geula C. Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain: observations based on the distribution of acetylcholinesterase and choline acetyltransferase. J Comp Neurol 1988; 275: 216–240.
Baskerville KA, Chang HT, Herron P. Topography of cholinergic afferents from the nucleus basalis of Meynert to representational areas of sensorimotor cortices in the rat. J Comp Neurol 1993; 335: 552–562.
Zaborszky L, Duque A. Local synaptic connections of basal forebrain neurons. Behav Brain Res 2000; 15: 143–158.
Felleman DJ, Van Essen DC. Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex 1991; 1: 1–47.
Alloway D, Crist J, Mutic JJ, Roy SA. Corticostriatal projections from rat barrel cortex have an anisotropic organization that correlates with vibrissal whisking behavior. J Neurosci 1999; 19: 10908–10922.
Nadasdy Z, Zaborszky L. Computational analysis of spatial organization of large scale neural networks. Anat Embryol 2001; 204: 303–317.
Valverde F. Reticular formation of the pons and medulla oblongata. A Golgi study. J Comp Neurol 1961; 116: 71–99.
Leontovich TA, Zhukova GP. The specificity of the neuronal structure and topography of the reticular formation in the brain and spinal cord of carnivora. J Comp Neurol 1963; 121: 347–381.
Ramon-Moliner E, Nauta WJH. The isodendritic core of the brain stem. J Comp Neurol 1966; 126: 311–336.
Das GD, Kreutzberg GW. Evaluation of interstitial nerve cells in the central nervous system. Adv Anat Embryol 1968; 41: 1–58.
Zaborszky L. Synaptic organization of basal forebrain cholinergic projection neurons. In: Neurotransmitter Interactions and Cognitive Functions ( Levin E, Decker M, Butcher L, eds.) Birkhauser, Boston, 1992, pp. 27–65.
McMullen NT, Goldberger B, Suter CM, Glaser EM. Neonatal deafening alters nonpyramidal dendrite orientation in auditory cortex: a computer microscope study in the rabbit. J Comp Neurol 1988; 267: 92–106.
Csillik B, Rakic P, Knyihar-Csillik E. Peptidergic innervation and the nicotinic acetylcholine receptor in the primate basal nucleus. Eur J Neurosci 1998; 10: 573–585.
Braitenberg V, Schutz A. Cortex: Statistics and Geometry of Neuronal Connectivity. Springer, Berlin, 1998.
Szentagothai J. “Specificity versus (quasi-) randomness” revisited. Acta Morph Hung 1990; 38:159–167.
Zaborszky L, Cullinan WE, Luine VN. Catecholaminergic-cholinergic interaction in the basal forebrain. Prog Brain Res 1993; 98: 31–49.
Zaborszky L, Cullinan WE, Braun A. Afferents to basal forebrain cholinergic projection neurons: an update. In: Basal Forebrain: Anatomy to Function ( Napier TC, Kaliwas PW, Hanin I, eds.) Plenum Press, New York, 1991, pp. 43–100.
Zaborszky L, Gaykema RP, Swanson DJ, Cullinan WE. Cortical input to the basal forebrain. Neuroscience 1997; 79: 1051–1078.
Pang K, Tepper JM, Zaborszky L. Morphological and electrophysiological characteristics of non-cholinergic basal forebrain neurons. J Comp Neurol 1998; 394: 186–204.
Duque A, Balatoni B, Detari L, Zaborszky L. EEG correlation of the discharge properties of identified neurons in the basal forebrain. J Neurophysiol 2000; 84: 1627–1635.
Schwaber JS, Rogers WT, Satoh K, Fibiger HC. Distribution and organization of cholinergic neurons in the rat forebrain demonstrated by computer-aided data acquisition and three-dimensional reconstruction. J Comp Neurol 1987; 263: 309–325.
Cullinan WE, Zaborszky L. Organization of ascending hypothalamic projections to the rostral forebrain with special reference to the innervation of cholinergic projection neurons. J Comp Neurol 1991; 306: 631–667.
Gaykema RPA, Zaborszky L. Direct catecholaminergic-cholinergic interactions in the basal forebrain: II. Substantia nigra and ventral tegmental area projections to cholinergic neurons. J Comp Neurol. 1996; 374: 555–577.
Glaser JR, Glaser EM. Neuron imaging with Neurolucida-a PC-based system for image combining microscopy. Comput Med Imaging Graph 1990; 14: 307–317.
Vassbo K, Nicotra G, Wiberg M, Bjaalie JG. Monkey somatosensory cerebrocerebellar pathways: Uneven densities of corticopontine neurons in different body representations of areas 3b, 1, and 2. J Comp Neurol 1999; 406: 109–128
Heimer L, Zaborszky L. (eds.) Neuroanatomical Tract-Tracing Methods 2. Recent Progress. Plenum Press, New York, 1989.
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Zaborszky, L., Csordas, A., Buhl, D.L., Duque, A., Somogyi, J., Nadasdy, Z. (2002). Computational Anatomical Analysis of the Basal Forebrain Corticopetal System. In: Ascoli, G.A. (eds) Computational Neuroanatomy. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-59259-275-3_9
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DOI: https://doi.org/10.1007/978-1-59259-275-3_9
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