Piecing together the Puzzle of Basal Forebrain Anatomy

Heimer, Lennart; Alheid, George F.

doi:10.1007/978-1-4757-0145-6_1

Cited by 310Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchMedical and Biological Sciences

Piecing together the Puzzle of Basal Forebrain Anatomy

Heimer, Lennart, Alheid, George F.·1991·Advances in Experimental Medicine and Biology

DOI 10.1007/978-1-4757-0145-6_1

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The extended amygdala comprises several basal forebrain structures, including the bed nucleus of the stria terminalis (BNST), central nucleus of the amygdala (CeA), sublenticular substantia innominata, and a transition zone in the shell of the NAc.
“The extended amygdala comprises several basal forebrain structures, including the bed nucleus of the stria terminalis (BNST), central nucleus of the amygdala (CeA), sublenticular substantia innominata, and a transition zone in the shell of the NAc (Heimer and Alheid, 1991).”
From Drug Addiction: Hyperkatifeia/Negative Reinforcement as a Framework for Medications Development (2021) · cites this paper as Heimer and Alheid, 1991
The regions that comprise the extended amygdala have cytoarchitectural and circuitry similarities with each other.
“The regions that comprise the extended amygdala have cytoarchitectural and circuitry similarities with each other (Heimer and Alheid, 1991).”
From Drug Addiction: Hyperkatifeia/Negative Reinforcement as a Framework for Medications Development (2021) · cites this paper as Heimer and Alheid, 1991

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Neurocircuitry of Addiction
Koob, G. F., & Volkow, N. D. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.110 · Cited by 5,340 · see citing works
“Each of these regions has cytoarchitectural and circuitry similarities (Heimer and Alheid, 1991).”
Background
The reward circuit: linking primate anatomy and human imaging
Haber, S. N., & Knutson, B. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.129 · Cited by 3,718 · see citing works
“The VS contains cell islands, including the islands of Calleja, which are thought to contain quiescent immature cells that remain in the adult brain (Bayer, 1985; Chronister et al , 1981; Meyer et al , 1989).”
Background
Autoradiographic localization of dopamine D1 and D2 receptors in rat nucleus accumbens: Resistance to differential rearing conditions
Bardo, M. T., & Hammer, R. P. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90226-e · Cited by 3,229 · see citing works
Drug abuse: hedonic homeostatic dysregulation
Koob, G. F., & Moal, M. L. (1997) · Science · doi:10.1126/science.278.5335.52 · Cited by 2,535 · see citing works
Neurobiology of emotion perception I: the neural basis of normal emotion perception
Phillips, M. L., Drevets, W. C., Rauch, S. L., & Lane, R. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00168-9 · Cited by 2,173 · see citing works
“…as the nucleus accumbens, which lacks distinct microscopic and macroscopic borders with the anteroventral putamen and ventromedial caudate (Heimer and Alheid 1991), other areas of the ventral putamen, and the medial portion of the caudate head, which receive projections from the amygdala…”
Background
Addiction and the brain antireward system
Koob, G. F., & Le Moal, M. (2008) · Annual Review of Psychology · doi:10.1146/annurev.psych.59.103006.093548 · Cited by 1,457 · see citing works
“…nucleus of the amygdala (CeA), but also the bed nucleus of the stria terminalis (BNST) and a transition zone in the medial subregion of the nucleus accumbens (shell of the nucleus accumbens), and these regions share certain cytoarchitectural and circuitry similarities (Heimer & Alheid 1991).”
Background
Regional cerebral blood flow throughout the sleep-wake cycle. An H2(15)O PET study
Braun, A. (1997) · Brain · doi:10.1093/brain/120.7.1173 · Cited by 1,268 · see citing works
Specificity in the projection patterns of accumbal core and shell in the rat
Heimer, L., Zahm, D. S., Churchill, L., Kalivas, P. W., & Wohltmann, C. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90202-y · Cited by 1,219 · see citing works
Self-citation
Neuroimaging and neuropathological studies of depression: implications for the cognitive-emotional features of mood disorders
Drevets, W. C. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00203-8 · Cited by 1,146 · see citing works
Functional connectivity of human striatum: a resting state FMRI study
Di Martino, A., Scheres, A., Margulies, D. S., Kelly, A. M. C., Uddin, L. Q., Shehzad, Z., Biswal, B., Walters, J. R., Castellanos, F. X., & Milham, M. P. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn041 · Cited by 1,090 · see citing works
The patterns of afferent innervation of the core and shell in the “Accumbens” part of the rat ventral striatum: Immunohistochemical detection of retrogradely transported fluoro‐gold
Brog, J. S., Salyapongse, A., Deutch, A. Y., & Zahm, D. S. (1993) · Journal of Comparative Neurology · doi:10.1002/cne.903380209 · Cited by 1,102 · see citing works
A Role for Brain Stress Systems in Addiction
Koob, G. F. (2008) · Neuron · doi:10.1016/j.neuron.2008.06.012 · Cited by 1,056 · see citing works
“…is composed of several basal forebrain structures: the bed nucleus of the stria Neuron 59, July 10, 2008 ª2008 Elsevier Inc. 13 terminalis, the central medial amygdala, and a transition zone in the posterior part of the medial nucleus accumbens (i.e., posterior shell) (Heimer and Alheid, 1991).”
Influential
On the significance of subterritories in the “accumbens” part of the rat ventral striatum
Zahm, D. S., & Brog, J. S. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90202-d · Cited by 1,040 · see citing works
Neuroscience of addiction
Koob, G. F., Sanna, P. P., & Bloom, F. E. (1998) · Neuron · doi:10.1016/s0896-6273(00)80557-7 · Cited by 1,026 · see citing works
The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior
McFarland, K., & Kalivas, P. W. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-21-08655.2001 · Cited by 905 · see citing works
“Motor versus limbic subcircuits Figure 8 illustrates the circuit containing the nuclei examined in this study and highlights topographic organization according to associations with limbic or motor subcircuits (Heimer and Alheid, 1991; Mogenson et al., 1993).”
Background
Neurobiological similarities in depression and drug dependence: a self-medication hypothesis
Markou, A. (1998) · Neuropsychopharmacology · doi:10.1016/s0893-133x(97)00113-9 · Cited by 767 · see citing works
Alcoholism: Allostasis and Beyond
Koob, G. F. (2003) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000057122.36127.c2 · Cited by 737 · see citing works
“…and connectivity and is composed of several basal forebrain structures: the BNST, the central and medial amygdala, the area termed the sublenticular substantia innominata, and a transition zone in the posterior medial part of the nucleus accumbens (e.g., shell) (Heimer and Alheid, 1991).”
Background
Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria
Drevets, W. C., Gautier, C., Price, J. C., Kupfer, D. J., Kinahan, P. E., Grace, A. A., Price, J. L., & Mathis, C. A. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01038-6 · Cited by 706 · see citing works
“In primates, these cells are scattered through the ventromedial caudate and anteroventral putamen (Gerfen et al 1985; Heimer et al 1991; Heimer and Alheid 1991).”
BackgroundMethod
Neurobiological mechanisms for opponent motivational processes in addiction
Koob, G. F., & Moal, M. L. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0094 · Cited by 702 · see citing works
Drug dependence: stress and dysregulation of brain reward pathways
Kreek, M. J., & Koob, G. F. (1998) · Drug and Alcohol Dependence · doi:10.1016/s0376-8716(98)00064-7 · Cited by 696 · see citing works
Cognitive functions of cortical acetylcholine: toward a unifying hypothesis
Sarter, M. F., & Bruno, J. P. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(96)00009-4 · Cited by 662 · see citing works
Alcoholism: A Systems Approach From Molecular Physiology to Addictive Behavior
Spanagel, R. (2009) · Physiological Reviews · doi:10.1152/physrev.00013.2008 · Cited by 636 · see citing works
“The construct of the extended amygdala, which is thought to be a key target of ethanol action (248), relates to brain circuits that share some cytoarchitectural similarities (183) and are involved in mediating positive and negative reinforcement.”
Background
Opioid use disorder
Strang, J., Volkow, N. D., Degenhardt, L., Hickman, M., Johnson, K., Koob, G. F., Marshall, B. D. L., Tyndall, M., & Walsh, S. L. (2020) · Nature Reviews Disease Primers · doi:10.1038/s41572-019-0137-5 · Cited by 639 · see citing works
Neurobiological mechanisms in the transition from drug use to drug dependence
Koob, G. F., Ahmed, S. H., Boutrel, B., Chen, S. A., Kenny, P. J., Markou, A., O’Dell, L. E., Parsons, L. H., & Sanna, P. P. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2003.11.007 · Cited by 576 · see citing works
The neurobiology of drug addiction
Koob, G. F., & Nestler, E. J. (1997) · Journal of Neuropsychiatry · doi:10.1176/jnp.9.3.482 · Cited by 572 · see citing works
The nucleus accumbens: a comprehensive review
Salgado, S., & Kaplitt, M. G. (2015) · Stereotactic and Functional Neurosurgery · doi:10.1159/000368279 · Cited by 489 · see citing works
Addiction as a stress surfeit disorder
Koob, G. F., Buck, C. L., Cohen, A., Edwards, S., Park, P. E., Schlosburg, J. E., Schmeichel, B., Vendruscolo, L. F., Wade, C. L., Whitfield, T. W., et al. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.05.024 · Cited by 483 · see citing works
“The neuroanatomical entity termed the extended amygdala (Heimer and Alheid, 1991) may represent a common anatomical substrate that integrates brain arousal-stress systems with hedonic processing systems to produce the between-system opponent process elaborated above.”
BackgroundInfluential
An integrative neuroanatomical perspective on some subcortical substrates of adaptive responding with emphasis on the nucleus accumbens
Zahm, D. S. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00065-2 · Cited by 487 · see citing works
Neurobiology of opioid addiction: Opponent process, hyperkatifeia, and negative reinforcement
Koob, G. F. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.05.023 · Cited by 477 · see citing works
Neurobiological substrates for the dark side of compulsivity in addiction
Koob, G. F. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.043 · Cited by 458 · see citing works
“The neuroanatomical entity termed the extended amygdala (Heimer and Alheid, 1991) may represent a common anatomical substrate integrating brain arousal-stress systems with hedonic processing systems to produce the between-system opponent process elaborated above.”
The dark side of emotion: the addiction perspective
Koob, G. F. (2015) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2014.11.044 · Cited by 433 · see citing works
“…conceptualized to be composed of several basal forebrain structures, including the bed nucleus of the stria terminalis, central nucleus of the amygdala, sublenticular substantia innominata, and a transition zone in the medial part of the nucleus accumbens (e.g., shell; Heimer and Alheid, 1991).”
BackgroundInfluential
Addictive and non‐addictive drugs induce distinct and specific patterns of ERK activation in mouse brain
Valjent, E., Pagès, C., Hervé, D., Girault, J., & Caboche, J. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03278.x · Cited by 434 · see citing works
Theoretical Frameworks and Mechanistic Aspects of Alcohol Addiction: Alcohol Addiction as a Reward Deficit Disorder
Koob, G. F. (2011) · Current topics in behavioral neurosciences · doi:10.1007/7854_2011_129 · Cited by 428 · see citing works
Active Music Therapy in Parkinson’s Disease: An Integrative Method for Motor and Emotional Rehabilitation
Pacchetti, C., Mancini, F., Aglieri, R., Fundarò, C., Martignoni, E., & Nappi, G. (2000) · Psychosomatic Medicine · doi:10.1097/00006842-200005000-00012 · Cited by 421 · see citing works
The neurobiology of addiction: a neuroadaptational view relevant for diagnosis
Koob, G. F. (2006) · Addiction · doi:10.1111/j.1360-0443.2006.01586.x · Cited by 397 · see citing works
“The neuroanatomical entity termed the extended amygdala [6] may thus represent a common anatomical substrate for acute drug reward and a common neuroanatomical substrate for the negative effects on reward function produced by stress that help drive compulsive drug administration.”
Background
Addiction is a Reward Deficit and Stress Surfeit Disorder
Koob, G. F. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00072 · Cited by 397 · see citing works
Brain stress systems in the amygdala and addiction
Koob, G. F. (2009) · Brain Research · doi:10.1016/j.brainres.2009.03.038 · Cited by 388 · see citing works
“…efferent connections from this complex include the posterior medial (sublenticular) ventral pallidum, ventral tegmental area, various brainstem projections, and perhaps most intriguing from a functional point of view, a considerable projection to the lateral hypothalamus (Heimer and Alheid, 1991).”
Background
Functional–anatomical implications of the nucleus accumbens core and shell subterritories
ZAHM, D. S. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09264.x · Cited by 384 · see citing works
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
Zahm, D. S., & Heimer, L. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903270205 · Cited by 385 · see citing works
Self-citation
Allostasis, amygdala, and anticipatory angst
Schulkin, J., McEwen, B. S., & Gold, P. W. (1994) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(94)90051-5 · Cited by 380 · see citing works
Brain Morphology and Schizophrenia: A Magnetic Resonance Imaging Study of Limbic, Prefrontal Cortex, and Caudate Structures
Breier, A. (1992) · Archives of General Psychiatry · doi:10.1001/archpsyc.1992.01820120009003 · Cited by 513 · see citing works
The human BNST: functional role in anxiety and addiction
Avery, S. N., Clauss, J. A., & Blackford, J. U. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.185 · Cited by 331 · see citing works
Drug Addiction: The Yin and Yang of Hedonic Homeostasis
Koob, G. F. (1996) · Neuron · doi:10.1016/s0896-6273(00)80109-9 · Cited by 347 · see citing works
Chapter 29 The nucleus accumbens: gateway for limbic structures to reach the motor system?
Groenewegen, H. J., Wright, C. I., & Beijer, A. V. J. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)61883-x · Cited by 344 · see citing works
Drug Addiction: Hyperkatifeia/Negative Reinforcement as a Framework for Medications Development
Koob, G. F. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000083 · Cited by 337 · see citing works
“The regions that comprise the extended amygdala have cytoarchitectural and circuitry similarities with each other (Heimer and Alheid, 1991).”
BackgroundInfluential
Extended Amygdala and Basal Forebrain
Alheid, G. F. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07082.x · Cited by 334 · see citing works
Self-citation
Heterogeneity of Alcohol Use Disorder: Understanding Mechanisms to Advance Personalized Treatment
Litten, R. Z., Ryan, M. L., Falk, D. E., Reilly, M., Fertig, J. B., & Koob, G. F. (2015) · Alcoholism: Clinical and Experimental Research · doi:10.1111/acer.12669 · Cited by 330 · see citing works
The Role of the Striatopallidal and Extended Amygdala Systems in Drug Addiction
Koob, G. F. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09282.x · Cited by 322 · see citing works
Neurobiology of Addiction: Toward the Development of New Therapies
Koob, G. F. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06682.x · Cited by 314 · see citing works
GABAA receptor antagonism in the extended amygdala decreases ethanol self-administration in rats
Hyytiä, P., & Koob, G. F. (1995) · European Journal of Pharmacology · doi:10.1016/0014-2999(95)00314-b · Cited by 302 · see citing works
The role of mesolimbic dopamine in the development and maintenance of ethanol reinforcement
Gonzales, R. A., Job, M. O., & Doyon, W. M. (2004) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2004.06.002 · Cited by 297 · see citing works
The amygdala complex: multiple roles in associative learning and attention.
Gallagher, M., & Holland, P. C. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.25.11771 · Cited by 300 · see citing works
L-dopa modulates functional connectivity in striatal cognitive and motor networks: A double-blind placebo-controlled study
Kelly, C., de Zubicaray, G., Di Martino, A., Copland, D. A., Reiss, P. T., Klein, D. F., Castellanos, F. X., Milham, M. P., & McMahon, K. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0810-09.2009 · Cited by 292 · see citing works
“As outlined in detail by Di Martino et al. (2008), these seed locations are consistent with both anatomical and functional subdivisions of the striatum (Heimer and Alheid, 1991; Drevets et al., 1999; Postuma and Dagher, 2006).”
Background
The role of CRF and CRF-related peptides in the dark side of addiction
Koob, G. F. (2009) · Brain Research · doi:10.1016/j.brainres.2009.11.008 · Cited by 290 · see citing works
“CRF drives the orticotropic hormone (ACTH) in the portal system of the brainstem and mediates arousal and behavioral responses ions, and ventral midbrain such as the ventral tegmental medial nucleus accumbens (i.e., posterior shell) (Johnston, 1923; Heimer and Alheid, 1991).”
Substantia innominata: a notion which impedes clinical–anatomical correlations in neuropsychiatric disorders
Heimer, L., Harlan, R. E., Alheid, G. F., Garcia, M. M., & de Olmos, J. S. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00405-8 · Cited by 286 · see citing works
Self-citation
Neuroadaptive mechanisms of addiction: studies on the extended amygdala
Koob, G. F. (2003) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2003.08.005 · Cited by 278 · see citing works
“A neuroanatomical entity termed the extended amygdala (Heimer and Alheid, 1991) may represent a common anatomical substrate for acute drug reward and the negative effects of compulsive drug administration on reward function.”
BackgroundInfluential
Sex differences in the neurobiology of drug addiction
Bobzean, S. A. M., Nobrega, A. K. D., & Perrotti, L. I. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.01.022 · Cited by 261 · see citing works
“…is the key anatomical substrate that comprises the so called “anti-reward pathway” which includes the central nucleus of the amygdala (CeA), bed nucleus of stria terminalis (BNST), and a transition zone in the medial (shell) of the nucleus accumbens (NAc Shell) (Heimer and Alheid, 1991) Figure 3.”
Influential
Cannabis use is quantitatively associated with nucleus accumbens and amygdala abnormalities in young adult recreational users
Gilman, J. M., Kuster, J. K., Lee, S., Lee, M. J., Kim, B. W., Makris, N., van der Kouwe, A., Blood, A. J., & Breiter, H. C. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.4745-13.2014 · Cited by 250 · see citing works
“The density increase was localized to a large area, which clearly represents the extended amygdala as defined by Heimer and Alheid (1991), a neuroanatomical entity implicated in addiction (Koob, 2003).”
Background
Stress, Corticotropin‐releasing Factor, and Drug Addiction
Koob, G. F. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb07876.x · Cited by 231 · see citing works
Striatum-Based Circuitry of Adolescent Depression and Anhedonia
Gabbay, V., Ely, B. A., Li, Q., Bangaru, S. D., Panzer, A. M., Alonso, C. M., Castellanos, F. X., & Milham, M. P. (2013) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2013.04.003 · Cited by 222 · see citing works
Neurocircuitry of alcohol addiction
Koob, G. F. (2014) · Handbook of clinical neurology · doi:10.1016/b978-0-444-62619-6.00003-3 · Cited by 227 · see citing works
A role for GABA mechanisms in the motivational effects of alcohol
Koob, G. F. (2004) · Biochemical Pharmacology · doi:10.1016/j.bcp.2004.07.031 · Cited by 224 · see citing works
Drugs of Abuse and the Brain
Leshner, A. I., & Koob, G. F. (1999) · Proceedings of the Association of American Physicians · doi:10.1046/j.1525-1381.1999.09218.x · Cited by 220 · see citing works
Candidate genes, pathways and mechanisms for bipolar (manic-depressive) and related disorders: an expanded convergent functional genomics approach
Ogden, C. A., Rich, M. E., Schork, N. J., Paulus, M. P., Geyer, M. A., Lohr, J. B., Kuczenski, R., & Niculescu, A. B. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001547 · Cited by 221 · see citing works
Development and organization of ocular dominance bands in primary visual cortex of the sable ferret
Ruthazer, E. S., Baker, G. E., & Stryker, M. P. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990503)407:2 · Cited by 46 · see citing works
Identifying a series of candidate genes for mania and psychosis: a convergent functional genomics approach
Niculescu, A. B., Segal, D. S., Kuczenski, R. T., Barrett, T. B., Hauger, R. L., & Kelsoe, J. R. (2000) · Physiological Genomics · doi:10.1152/physiolgenomics.2000.4.1.83 · Cited by 206 · see citing works
“These brain regions were chosen based on the extensive literature demonstrating their central role in cognition and emotion (24, 36).”
Regional and Cellular Mapping of cAMP Response Element-Mediated Transcription during Naltrexone-Precipitated Morphine Withdrawal
Shaw-Lutchman, T. Z., Barrot, M., Wallace, T. L., Gilden, L., Zachariou, V., Impey, S., Duman, R. S., Storm, D. R., & Nestler, E. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03663.2002 · Cited by 205 · see citing works
The structural basis for mapping behavior onto the ventral striatum and its subdivisions
Meredith, G. E., Baldo, B. A., Andrezjewski, M. E., & Kelley, A. E. (2008) · Brain Structure and Function · doi:10.1007/s00429-008-0175-3 · Cited by 202 · see citing works
“Heimer and colleagues carried the concept further in a series of seminal works defining and refining major basal forebrain systems that included the ventrostriatopallidal system (Alheid and Heimer 1988, 1996; Heimer and Alheid 1991; Heimer et al. 1991b, 1993, 1997).”
BackgroundMethod
Modulation of Cell Firing in the Nucleus Accumbens
O’Donnell, P., GREENE, J., Pabello, N. G., LEWIS, B. L., & Grace, A. A. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09267.x · Cited by 204 · see citing works
Central nucleus of the amygdala and the effects of alcohol and alcohol-drinking behavior in rodents
McBride, W. J. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00680-3 · Cited by 197 · see citing works
Chemical anatomy of primate basal ganglia
Parent, A., Côté, P., & Lavoie, B. A. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(95)80010-6 · Cited by 186 · see citing works
Differential Effects of Caffeine on Dopamine and Acetylcholine Transmission in Brain Areas of Drug-naive and Caffeine-pretreated Rats
Acquas, E. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(02)00290-7 · Cited by 186 · see citing works
“With these premises we studied with microdialysis in freely-moving rats the effect of caffeine on extracellular DA and ACh levels in the shell and in the core of the NAc (Heimer et al. 1991; Heimer and Alheid 1991) and in the prefrontal cortex (PFCX).”
Background
Molecular mechanisms underlying alcohol-drinking behaviours
Ron, D., & Barak, S. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.85 · Cited by 165 · see citing works
Amygdala and Extended Amygdala of the Rat: A Cytoarchitectonical, Fibroarchitectonical, and Chemoarchitectonical Survey
de Olmos, J. S., Beltramino, C. A., & Alheid, G. F. (2004) · Elsevier eBooks · doi:10.1016/b978-012547638-6/50020-1 · Cited by 160 · see citing works
Self-citation
Afferents to basal forebrain cholinergic projection neurons: an update.
Záborszky, L., Cullinan, W., & Braun, A. (1991) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4757-0145-6_2 · Cited by 173 · see citing works
Neurobiology of dysregulated motivational systems in drug addiction
Edwards, S., & Koob, G. F. (2010) · Future Neurology · doi:10.2217/fnl.10.14 · Cited by 157 · see citing works
“, posterior shell) [133,134].”
Dopamine receptor mRNA expression patterns by opioid peptide cells in the nucleus accumbens of the rat: A double in situ hybridization study
Curran, E. J., & Watson, S. J. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903610106 · Cited by 148 · see citing works
Distribution of dopaminergic fibers in the central division of the extended amygdala of the rat
Freedman, L. J., & Cassell, M. D. (1994) · Brain Research · doi:10.1016/0006-8993(94)91545-8 · Cited by 145 · see citing works
The Paraventricular Nucleus of the Thalamus as an Integrating and Relay Node in the Brain Anxiety Network
Kirouac, G. J. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.627633 · Cited by 136 · see citing works
“The BSTDL and CeL are part of a larger macrostructure called the central extended amygdala (cEA) (Heimer and Alheid, 1991; Alheid et al., 1995; de Olmos et al., 2004).”
Background
Individual differences in the neuropsychopathology of addiction
George, O., & Koob, G. F. (2017) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2017.19.3/gkoob · Cited by 140 · see citing works
Hypothalamo‐preoptic Histaminergic Projections in Sleep‐Wake Control in the Cat
Lin, J., Sakai, K., & Jouvet, M. (1994) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1994.tb00306.x · Cited by 139 · see citing works
Neurobiological mechanisms of addiction: focus on corticotropin-releasing factor.
Koob, G. F., & Zorrilla, E. P. (2010) · PubMed · Cited by 138 · see citing works
The Central Amygdala and Alcohol: Role of -Aminobutyric Acid, Glutamate, and NeuropeptidesPreprint
Roberto, M., Gilpin, N. W., & Siggins, G. R. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a012195 · Cited by 136 · see citing works
“In the context of drug addiction, the major constituents of the extended amygdala are the CeA, the lateral portion of the bed nucleus of stria terminalis (BNST), and nucleus accumbens (NAc) shell (Heimer and Alheid 1991).”
Background
The dopamine D-1 receptor antagonist SCH 23390 injected into the dorsolateral bed nucleus of the stria terminalis decreased cocaine reinforcement in the rat
Epping-Jordan, M. P., Markou, A., & Koob, G. F. (1998) · Brain Research · doi:10.1016/s0006-8993(97)01190-6 · Cited by 131 · see citing works
Lateral Preoptic Control of the Lateral Habenula through Convergent Glutamate and GABA Transmission
Barker, D. J., Miranda-Barrientos, J. A., Zhang, S., Root, D. H., Wang, H.-L., Liu, B., Calipari, E. S., & Morales, M. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.066 · Cited by 125 · see citing works
“, 2015), and anatomical and electrophysiological findings from over forty years of research have led to the suggestion that LPO/LHb inputs are GABAergic (Araki et al., 1984; Garland and Mogenson, 1983; Heimer and Alheid, 1991; Meye et al., 2013; Mok andMogenson, 1972a, 1972b).”
Background
Sex Differences and the Role of Estradiol in Mesolimbic Reward Circuits and Vulnerability to Cocaine and Opiate Addiction
Kokane, S. S., & Perrotti, L. I. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.00074 · Cited by 123 · see citing works
“…associated with motor circuitry, thus coordinating behavioral output, while the shell interacts with limbic and autonomic brain regions, indicating significant regulation of reward, emotional, and visceral responses to stimuli (Heimer and Alheid, 1991; Zahm and Brog, 1992; Everitt et al., 1999).”
Background
The evolving theory of basal forebrain functional—anatomical ‘macrosystems’
Zahm, D. S. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.06.003 · Cited by 128 · see citing works
Two discrete nucleus accumbens projection areas differentially mediate cocaine self-administration in the rat
Robledo, P., & Koob, G. F. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90112-4 · Cited by 127 · see citing works
Brain aromatase: Roles in reproduction and neuroprotection
Roselli, C. E. (2007) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2007.05.014 · Cited by 127 · see citing works
“Heimer, L.; Alheid, G. Piecing together the puzzle of basal forebrain anatomy.”
Background
Sensorimotor gating in rats is regulated by different dopamine-glutamate interactions in the nucleus accumbens core and shell subregions
Wan, F.-J., & Swerdlow, N. R. (1996) · Brain Research · doi:10.1016/0006-8993(96)00209-0 · Cited by 124 · see citing works
Existing and future drugs for the treatment of the dark side of addiction
Koob, G. F., & Mason, B. J. (2016) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010715-103143 · Cited by 121 · see citing works
PET measures of amphetamine-induced dopamine release in ventral versus dorsal striatum
Drevets, W. (1999) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00079-2 · Cited by 122 · see citing works
“In primates, the accumbens cells blend with those of the anteroventral putamen and the ventral caudate, so that a distinct border of the accumbens shell is not microscopically or macroscopically evident (Heimer and Alheid 1991).”
BackgroundMethodInfluential
Integration of chemosensory and hormonal cues is essential for mating in the male Syrian hamster
Wood, R., & Newman, S. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-11-07261.1995 · Cited by 122 · see citing works
Direct comparison of projections from the central amygdaloid region and nucleus accumbens shell
Zahm, D. S., Jensen, S. L., Williams, E. S., & Martin, J. R. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00524.x · Cited by 121 · see citing works
The Role of the Central Amygdala in Alcohol Dependence
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Neuropeptide Y opposes alcohol effects on gamma-aminobutyric acid release in amygdala and blocks the transition to alcohol dependence
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“Brain stress systems in the “extended amygdala” (4) appear to be especially important in mediating motivational deficits associated with alcohol withdrawal and excessive alcohol drinking.”
Chapter 28 Theories of basal forebrain organization and the “emotional motor system”
Alheid, G. F., & Heimer, L. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)61882-8 · Cited by 115 · see citing works
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“Each of these regions has cytoarchitectural and circuitry similarities [30].”
Background
Effects of dopamine depletion on the morphology of medium spiny neurons in the shell and core of the rat nucleus accumbens
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THE ANATOMY OF THE BASAL FOREBRAIN
Heimer, L., Hoesen, G. W. V., Trimble, M., & Zahm, D. S. (2008) · Elsevier eBooks · doi:10.1016/b978-012374239-1.50006-3 · Cited by 28 · see citing works
Self-citation
Basal Forebrain
Binder, M. D., Hirokawa, N., & Windhorst, U. (2008) · Springer eBooks · doi:10.1007/978-3-540-29678-2_558
Chapter 28 Theories of basal forebrain organization and the “emotional motor system”
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Self-citation
Basal Forebrain Anatomical Systems in MRI Space
Záborszky, L., Amunts, K., Palomero‐Gallagher, N., & Zilles, K. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-397025-1.00238-4 · Cited by 7 · see citing works
The human basal forebrain. Part I. An overview
Sakamoto, N., Pearson, J., Shinoda, K., Alheid, G. F., de Olmos, J. S., & Heimer, L. (1999) · Handbook of chemical neuroanatomy · doi:10.1016/s0924-8196(99)80023-2 · Cited by 39 · see citing works
Self-citation

Authors: Heimer, L., & Alheid, G. F.
Affiliations: University of Virginia Health System (US)
University of Virginia (US)
Venue: Advances in Experimental Medicine and Biology
Publisher: Springer US
Published: 1991
Volume: 295
Pages: 1-42
ISSN: 0065-2598 (ISSN-L)
DOI: 10.1007/978-1-4757-0145-6_1
OpenAlex: W2230876051
Cited by: 310
References: 208
Citations by year: 2026: 1 · 2025: 3 · 2024: 5 · 2023: 7 · 2022: 7 · 2021: 10 · 2020: 14 · 2019: 4 · 2018: 5 · 2017: 6 · 2016: 7 · 2015: 12 · 2014: 11 · 2013: 10 · 2012: 13
FWCI: 13.12
Type: book chapter
Language: en
Open access: closed
Locations: Advances in experimental medicine and biology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
U.S. Public Health Service (17743)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Health Sciences › Medicine › Anatomy › Medical and Biological Sciences
Keywords: basal forebrain, hypothalamus, limbic system, nucleus accumbens, olfactory tubercle, septum, diagonal band of Broca, bed nucleus of the stria terminalis, substantia innominata, olfactory cortex, hippocampus, amygdala, fornix, stria terminalis, medial forebrain bundle, fiber tracts
MeSH terms: Animals, Brain, Humans, Prosencephalon

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