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The Dopaminergic Projection System, Basal Forebrain Macrosystems, and Conditioned Stimuli

Published online by Cambridge University Press:  07 November 2014

Daniel S. Zahm  and
Michael Trimble
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Abstract

This review begins with a description of some problems that recently have beset an influential circuit model of fear conditioning and goes on to look at neuroanatomy that may subserve conditioning viewed in a broader perspective, including not only fear but also appetitive conditioning. The column will then focus on basal forebrain functional-anatomical systems, or macrosystems, as they have come to be called. Yet, more specific attention is then given to the relationships of the dorsal and ventral striatopallidal systems and extended amygdala with the dopaminergic mesotelencephalic projection systems, culminating with the hypothesis that all macrosystems contribute to behavioral conditioning.

Type
Brain Regions of Interest
Information
CNS Spectrums , Volume 13 , Issue 1 , January 2008 , pp. 32 - 40
Copyright
Copyright © Cambridge University Press 2008

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References

REFERENCES

1.Kroenke, K, Spitzer, RL, Williams, JB, Monahan, PO, Löwe, B. Anxiety disorders in primary care: prevalence, impairment, comorbidity and detection. Ann Int Med. 2007;146:317–325.CrossRefGoogle ScholarPubMed
2.LeDoux, JE. Emotion circuits in the brain. Ann Rev Neurosci. 2000;23:155–184.Google Scholar
3.Cahill, L, Weinberger, NM, Roozendaal, B, McGaugh, JL. Is the amygdal a locus of “conditioned fear”? Some questions and caveats. Neuron. 1999;23:227–228.Google Scholar
4.Wilensky, AE, Schafe, GE, Kristensen, MP, LeDoux, JE. Rethinking the fear circuit: the central nucleus of the amygdala is required for the acquisition, consolidation, and expression of Pavlovian fear conditioning. J Neurosci. 2006;26:12387–12396.CrossRefGoogle ScholarPubMed
5.Turner, BJ, Zimmer, J. The architecture and some of the interconnections of the rat's amygdala and lateral periallocortex. J Comp Neurol. 1984;227:540–557.CrossRefGoogle ScholarPubMed
6.Quirk, GJ, Repa, C, LeDoux, JE. Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron. 1995;15:1029–1039.CrossRefGoogle ScholarPubMed
7.Rogan, MT, Staubli, UV, LeDoux, JE. Fear conditioning induces associative long-term potentiation in the amygdala. Nature. 1997;390:604–607.CrossRefGoogle ScholarPubMed
8.Collins, DR, Paré, D. Differential fear conditioning induces reciprocal changes in the sensory responses of lateral amygdala neurons to the CS(+) and CS(-). Learn Mem. 2000;7:97–103.CrossRefGoogle Scholar
9.Royer, S, Martina, M, Paré, D. An inhibitory interface gates impulse traffic between the input and output stations of the amygdala. J Neurosci. 1999;19:10575–10583.CrossRefGoogle ScholarPubMed
10.Paré, D, Quirk, GJ, LeDoux, JE. New vistas on amygdala networks in conditioned fear. J Neurophysiol. 2004;92:1–9.Google Scholar
11.Koo, JW, Han, J-S, Kim, JJ. Selective neurotoxic lesions of basolateral and central nuclei of the amygdala produce differential effects on fear conditioning. J Neurosci. 2004;24:7654–7662.CrossRefGoogle ScholarPubMed
12.Weiskrantz, L. Behavioral changes associated with ablations of the amygdaloid complex in monkeys. J Comp Physiol Psychol. 1956;29:381–391.CrossRefGoogle Scholar
13.Kellicut, MH, Schwartzbaum, JS. Formation of a conditioned emotional response (CER) following lesions of the amygdaloid complex in rats. Psychol Rev. 1963;12:351–358.Google Scholar
14.Blanchard, DC, Blanchard, RJ. Innate and conditioned reactions to threat in rats with amygdaloid lesions. J Comp Physiol Psychol. 1972;81:281–290.CrossRefGoogle ScholarPubMed
15.Spevack, AA, Campbell, CT, Drake, L. Effect of amygdalectomy on habituation and CER in rats. Physiol Behav. 1975;15:199–207.CrossRefGoogle ScholarPubMed
16.Gallagher, M, Holland, PC. The amygdala complex: multiple roles in associative learning and attention. Proc Natl Acad Sci USA. 1994;91:11771–11776.Google Scholar
17.Everitt, BJ, Morris, KA, O'Brien, A, Robbins, TW. The basolateral amygdala-ventral striatal system and conditioned place preference: further evidence of limbic-striatal interactions underlying reward-related processes. Neuroscience. 1989;42:1–18.CrossRefGoogle Scholar
18.Everitt, BJ, Robbins, TW. Amygdala-ventral striatal interactions and reward-related processes. In: Aggleton, J, ed. The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. New York, NY: Wiley-Liss, Inc: 1992;401–429.Google Scholar
19.Parkinson, JA, Olmstead, MC, Burns, LH, Robbins, TW, Everitt, BJ. Dissociation in effects of lesions of the nucleus accumbens core and shell on appetitive Pavlovian approach behavior and the potentiation of conditioned reinforcement and locomotor activity by D-amphetamine. J Neurosci. 1999;19:2401–2411.Google Scholar
20.Parkinson, JA, Willoughby, , Robbins, TW, Everitt, BJ. Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: further evidence for limbic cortical-ventral striatopallidal systems. Behav Neurosci. 2000;114:42–63.CrossRefGoogle ScholarPubMed
21.Riedel, G, Harrington, NR, Hall, G, Macphail, EM. Nucleus accumbens lesions impair context, but not cue, conditioning in rats. NeuroReport. 1997;8:2477–2481.Google Scholar
22.Parkinson, JA, Robbins, TW, Everitt, BJ. Selective excitotoxic lesions of the nucleus accumbens core and shell differentially affect aversive Pavlovian conditioning to discrete and contextual cues. Psychobiology. 1999;27:256–266.CrossRefGoogle Scholar
23.Haralambous, T, Westbrook, RF. An infusion of bupivacaine into the nucleus accubmens disrupts the acquisition, but not the expression, of contextual fear conditioning. Behav Neurosci. 1999;113:925–940.CrossRefGoogle Scholar
24.Levita, L, Dalley, JW, Robbins, TW. Disruption of Pavlovian contextual conditioning by excitotoxic lesions of the nucleus accumbens core. Behav Neurosci. 2002;116:539–552.CrossRefGoogle ScholarPubMed
25.Gallagher, M, Graham, PW, Holland, PC. The amygdala central nucleus and appetitive Pavlovian conditioning: lesions impair one class of conditioned behavior. J Neurosci. 1990;10:1906–1911.Google Scholar
26.Heimer, L, Alheid, GF. Piecing together the puzzle of basal forebrain anatomy. In: Napier, TC, Kalivas, PW, Hanin, I, eds. The Basal Forebrain: Anatomy to Function. New York, NY: Plenum Press; 1991:1–42.Google Scholar
27.Heimer, L, de Olmos, JS, Alheid, GF, Zaborszky, L. “Perestroika” in the basal forebrain: opening the border between neurology and psychiatry. Prog Brain Res. 1991;87:109–165.CrossRefGoogle ScholarPubMed
28.Heimer, L. The olfactory connections of the diencephalon in the rat. An experimental light- and electron-microscopic study with special emphasis on the problem of terminal degeneration. Brain Behav Evol. 1972;6:484–523.Google Scholar
29.Heimer, L, Wilson, RD. The subcortical projections of allocortex: similarities in the neuronal associations of the hippocampus, the piriform cortex and the neocortex. In: Santini, M, ed. Golgi Centennial Symposium Proceedings. New York, NY: Raven Press; 1975;173–193.Google Scholar
30.Alheid, GF, Heimer, L. New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience. 1988;27:1–39.CrossRefGoogle ScholarPubMed
31.Carlsen, J, Heimer, L. The basolateral amygdaloid nucleus as a cortical-like structure. Brain Res. 1988;441:377–380.Google Scholar
32.Heimer, L, Van Hoesen, GW. The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neurosci Biobehav Rev. 2006;30:126–147.Google Scholar
33.Heimer, L, Van Hoesen, GW, Trimble, MR, Zahm, DS. Anatomy of Neuropsychiatry. Amsterdam, Netherlands: Elsevier Press; 2008.Google Scholar
34.Alheid, GF. Extended amygdala and basal forebrain. In: Shinnick-Gallagher, P, Pitkänen, A, Shekhar, A, Cahill, L, eds. The Amygdala in Brain Function. New York, NY: New York Academy of Sciences; 2003;185–205.Google Scholar
35.Zahm, DS, Grosu, S, Irving, JC, Williams, EA. Discrimination of striatopallidum and extended amygdala in the rat: a role for parvalbumin immunoreactive neurons? Brain Res. 2003;978:141–154.CrossRefGoogle Scholar
36.Zahm, DS. The evolving theory of basal forebrain functional-anatomical “macrosystems.” Neurosci Biobehav Rev. 2006;30:148–172.CrossRefGoogle ScholarPubMed
37.Dahlström, A, Fuxe, K. Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol Scan Suppl. 1964;62(suppl 232):1–55.Google Scholar
38.Andén, NE, Carlsson, A, Dahlström, A, Fuxe, K, Hillarp, NÅ, Larsson, K. Demonstration and mapping out of nigro-neostriatal dopaminergic neurons. Life Sci. 1964;3:523–530.CrossRefGoogle Scholar
39.Andén, NE, Dahlström, A, Fuxe, K, Larsson, K. Mapping out of catecholaminergic and 5-hydroxtryptamine neurons innervating the telencephalon and diencephalon. Life Sci. 1965;4:1275–1279.CrossRefGoogle Scholar
40.Andén, NE, Dahlström, A, Fuxe, K, Larsson, K, Olson, L, Ungerstedt, U. Ascending monoamine neurons to the telencephalon and diencephalon. Acta Physiol Scand. 1965;67:313–326.CrossRefGoogle Scholar
41.Andén, NE, Fuxe, K, Hamberger, B, Hökfelt, T. A quantitative study on the nigro-striatal dopamine neuron system in the rat. Acta Physiol Scand. 1966;67:306–312.CrossRefGoogle Scholar
42.Björklund, A, Lindvall, O. Dopamine-containing systems in the CNS. In: Björklund, A, Hökfelt, T, eds. Classical Transmitters in the CNS. Handbook of Chemical Neuroanatomy, Volume 2, Part 1. Amsterdam, Netherlands: Elsevier Press; 1984;55–122.Google Scholar
43.Fallon, JH, Koziell, DA, Moore, RY. Catecholamine innervation of the basal forebrain. II. Amygdala, suprarhinal cortex and entorhinal cortex. J Comp Neurol. 1978;180:509–532.CrossRefGoogle ScholarPubMed
44.Fallon, JH, Moore, RY. Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J Comp Neurol. 1978;180:545–580.CrossRefGoogle Scholar
45.Swanson, LW. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunoflourescence study in the rat. Brain Res Bull. 1982;9:321–353.Google Scholar
46.Lindvall, O, Björkland, A. Dopamine- and norepinephrine-containing neuron systems: their anatomy in the rat brain. In: Emson, PC, ed. Chemical Neuroanatomy. New York, NY: Raven Press; 1983;229–256.Google Scholar
47.Fallon, JH, Loughlin, SE. Monoamine innervation of cerebral cortex and a theory of the role of monoamines in cerebral cortex and basal ganglia. In: Jones, EG, Peters, A, eds. Cerebral Cortex: Further Aspects of Cortical Function, Including Hippocampus. New York, NY: Plenum Press; 1985;41–127.Google Scholar
48.Fallon, JH, Loughlin, SE. Substantia nigra. In: Paxinos, G, ed. The Rat Nervous System, Volume 1, Forebrain and Midbrain, 2nd Edition. Sydney, Australia: Academic Press; 1995;215–237.Google Scholar
49.Deutch, AY, Goldstein, M, Baldino, F Jr, Roth, RH. Telencephalic projections of the A8 dopamine cell group. Ann N Y Acad Sci. 1988;537:27–50.CrossRefGoogle ScholarPubMed
50.Fallon, JH. Topographic association of ascending dopaminergic projections. Ann N Y Acad Sci. 1988;537:1–9.CrossRefGoogle Scholar
51.Hökfelt, T, Mårtensson, R, Björklund, A, Kleinau, S, Goldstein, M. Distribution maps of tyrosine-hydroxylase-immunoreactive neurons in the rat brain. In: Björklund, A, Hokfelt, T, eds. Classical Transmitters in the CNS. Handbook of Chemical Neuroanatomy, Volume2, Part 1. Amsterdam, Netherlands: Elsevier Press; 1984;277–379.Google Scholar
52.Houk, JC, Davis, JL, Beiser, DG, eds. Models of Information Processing in the Basal Ganglia. Cambridge, Mass: MIT Press; 1995.Google Scholar
53.Phillipson, OT. Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: a horseradish peroxidase study in the rat. J Comp Neurol. 1979;187:85–98.CrossRefGoogle Scholar
54.Geisler, S, Zahm, DS. Afferents of the ventral tegmental area in the rat - anatomical substratum for integrative functions. J Comp Neurol. 2005;490:270–294.CrossRefGoogle ScholarPubMed
55.Geisler, S, Zahm, DS. Neurotensin afferents of the ventral tegmental area in the rat: [1] re-examination of their origins and [2] responses to acute psychostimulant drug administration. Eur J Neurosci. 2006;24:116–134.CrossRefGoogle ScholarPubMed
56.Geisler, S, Derst, C, Veh, RW, Zahm, DS. Glutamatergic afferents of the ventral tegmental area in the rat. J Neurosci. 2007;27:5730–5743.CrossRefGoogle ScholarPubMed
57.Kelly, PH, Seviour, PW, Iversen, SD. Amphetamine and apomorphine responses in the rat following 6-OHDA lesions of the nucleus accumbens septi and corpus striatum. Brain Res. 1975;94:507–522.CrossRefGoogle ScholarPubMed
58.Wise, RA. Action of drugs of abuse on brain reward systems. Pharmacol Biochem Behav. 1980;13(suppl 1):213–223.CrossRefGoogle ScholarPubMed
59.Salamone, JD, Cousins, MS, Bucher, S. Anhedonia or anergia: effects of haloperidol and nucleus accumbens dopamine depletion on instrumental response selection in a T-maze cost/benefit procedure. Behav Brain Res. 1994;65:221–229.CrossRefGoogle ScholarPubMed
60.Rebec, GV, Grabner, CP, Johnson, M, Pierce, RC, Bardo, MT. Transient increases in catecholaminergic activity in medial prefrontal cortex and nucleus accumbens shell during novelty. Neuroscience. 1997;76:707–714.CrossRefGoogle ScholarPubMed
61.Schultz, W, Dayan, P, Montague, PR. A neural substrate of prediction and reward. Science. 1997;275:1593–1599.CrossRefGoogle ScholarPubMed
62.Wise, RA. Dopamine, learning and motivation. Nat Rev Neurosci. 2004;5:483–494.CrossRefGoogle ScholarPubMed
63.Wise, RA. The role of reward pathways in the development of drug dependence. Pharmacol Ther. 1987;35:227–263.CrossRefGoogle ScholarPubMed
64.Nestler, EJ. Is there a common molecular pathway for addiction? Nat Neurosci. 2005;8:1445–1449.CrossRefGoogle Scholar
65.Beckstead, RM, Domesick, VB, Nauta, WJ. Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res. 1979;175:191–217.Google Scholar
66.Davis, M, Walker, DL, Lee, Y. Roles of the amygdala and bed nucleus of the stria terminalis in fear and anxiety measured with the acoustic startle reflex. Possible relevance to PTSD. Ann N Y Acad Sci. 1997;821:305–331.Google Scholar
67.Walker, DL, Davis, M. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci. 1997;17:9375–9383.CrossRefGoogle ScholarPubMed
68.Davis, M, Shi, C. The extended amygdala: are the central nucleus of the amygdala and the bed nucleus of the stria terminalis differentially involved in fear versus anxiety? Ann N Y Acad Sci. 1999;877:292–308.CrossRefGoogle ScholarPubMed
69.Krettek, JF, Price, JL. Amygdaloid projections to subcortical structures within the forebrain and brainstem in the rat and cat. J Comp Neurol. 1978;178:225–254.Google Scholar
70.Zahm, DS, Jensen, S, Williams, EA, Martin, JR III. Direct comparison of projections from the central nucleus of the amygdala and nucleus accumbens shell. Eur J Neurosci. 1999;11:1119–1126.CrossRefGoogle ScholarPubMed
71.Dong, H-W, Petrovich, GD, Watts, AG, Swanson, LW. Basic organization of projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis in adult rat brain. J Comp Neurol. 2001;436:430–455.CrossRefGoogle ScholarPubMed
72.Misu, Y, Goshima, Y, Ueda, H, Okamura, H. Neurobiology of L-DOPA systems. Prog Neurobiol. 1996;49:415–454.CrossRefGoogle Scholar
73.Hasue, RH, Shammah-Lagnado, SJ. Origin of the dopaminergic innervation of the central extended amygdala and accumbens shell: a combined retrograde tracing and immunohistochemical study in the rat. J Comp Neurol. 2002;454:15–33.Google Scholar
74.White, NM, Carr, GD. The conditioned place preference is affected by two independent reinforcement processes. Phamacol Biochem Behav. 1985;23:591–618.CrossRefGoogle ScholarPubMed
75.White, NM, Messier, C, Carr, GD. Operationalizing and measuring the organizing influence of drugs on behaviour. In: Bozarth, MA, ed. Methods of Assessing the Reinforcing Properties of Abused Drugs. New York, NY: Springer Verlag; 1985;275–290.Google Scholar
76.Phillips, AG, Fibiger, HC. Anatomical and neurochemical substrates of drug reward. In: Bozarth, MA, ed. Methods of Assessing the Reinforcing Properties of Abused Drugs. New York, NY: Springer Verlag; 1987:275–290.CrossRefGoogle Scholar
77.Lamont, EW, Kokkinidis, L. Infusion of the dopamine D1 receptor antagonist SCH23390 into the amygdala blocks fear expression in a potentiated startle paradigm. Brain Res. 1998;795:128–136.CrossRefGoogle Scholar
78.Guarraci, FA, Frohardt, RJ, Kapp, BS. Amygdaloid D1 dopamine receptor involvement in Pavlovian fear conditioning. Brain Res. 1999;827:28–40.CrossRefGoogle ScholarPubMed
79.Guarraci, FA, Frohardt, RJ, Falls, WA, Kapp, BS. The effects of intra-amygdaloid infusions of a D2 dopamine receptor antagonist on Pavlovian fear conditioning. Behav Neurosci. 2000;114:647–651.CrossRefGoogle ScholarPubMed
80.Swanson, LW. Cerebral hemisphere regulation of motivated behavior. Brain Res. 2000;886:113–164.CrossRefGoogle ScholarPubMed