Functional Magnetic Resonance Imaging of Brain Reward Circuitry in the Human
Corresponding Author
HANS C. BREITER
Nuclear Magnetic Resonance Center, Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02129, USA
Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02114, USA
Address correspondence to Hans C. Breiter, MD, MGH-NMR Center, 2nd Floor, Building #149, Thirteenth Street, Charlestown, MA 02129, USA. Voice: 617-726-5715; fax: 617-726-7422; [email protected]Search for more papers by this authorBRUCE R. ROSEN
Nuclear Magnetic Resonance Center, Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02129, USA
Search for more papers by this authorCorresponding Author
HANS C. BREITER
Nuclear Magnetic Resonance Center, Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02129, USA
Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02114, USA
Address correspondence to Hans C. Breiter, MD, MGH-NMR Center, 2nd Floor, Building #149, Thirteenth Street, Charlestown, MA 02129, USA. Voice: 617-726-5715; fax: 617-726-7422; [email protected]Search for more papers by this authorBRUCE R. ROSEN
Nuclear Magnetic Resonance Center, Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02129, USA
Search for more papers by this authorAbstract
ABSTRACT: To produce behavior, motivational states necessitate at least three fundamental operations, including (1) selection of objectives focused on goal-objects, (2) compilation of goal-object information, and (3) determination of physical plans for securing goal-objects. The second of these general operations has been theorized to involve three subprocesses: (a) feature detection and other perceptual processing of putative goal-object “rewards,” (b) valuation of goal-object worth in the context of potential hedonic deficit states, and (c) extraction of incidence and temporal data regarding the goal-object. A number of subcortical brain regions appear to be involved in these three informational subprocesses, in particular, the amygdala, sublenticular extended amygdala (SLEA) of the basal forebrain, and nucleus accumbens/subcallosal cortex (NAc/SCC). Components of the amygdala, SLEA, and NAc/SCC together constitute the larger anatomic structure of the extended amygdala. Functional magnetic resonance imaging (fMRI) studies of humans have recently begun to localize these subcortical regions within the extended amygdala during specific experimental conditions. In this manuscript, two human cocaine- infusion studies and one cognitive psychology experiment are reviewed in relation to their pattern of fMRI activation within regions of the extended amygdala. Activation in the NAc/SCC, in particular, is evaluated in relation to a hypothesis that one function of the NAc/SCC and associated brain regions is the evaluation of goal-object incidence data for the computation of conditional probabilities regarding goal-object availability. Further work is warranted to test hypothesized functions for all regions within the extended amygdala and integrate them toward an understanding of motivated behavior.
REFERENCES
- 1
Shizgal, P.
1997. Neural basis of utility estimation.
Curr. Opin. Neurobiol.
7: 198–208.
- 2
Shizgal, P. 1999. On the neural computation of utility: implications from studies of brain stimulation reward. In Well-Being: The Foundations of Hedonic Psychology. D. Kahneman, E. Diener & N. Schwarz, Eds.: 502-526. Russell Sage Foundation. New York, NY.
- 3
Pfaffmann, C., R. Norgren & H.J. Grill.
1977. Sensory affect and motivation.
Ann. N. Y. Acad. Sci.
290: 18–34.
- 4
Zajonc, R.B.
1980. Feeling and thinking: preferences need no inference.
Am. Psychol.
35(2): 151–175.
- 5
Kahneman, D. & A. Tversky.
1979. Prospect theory: an analysis of decision under risk.
Econometrica
47: 263–291.
- 6
Gallistel, C.R. 1990. The organization of learning. MIT Press. Cambridge, MA.
- 7
Baum, W.M. & H. Rachlin.
1969. Choice as time allocation.
J. Exp. Anal. Behav.
12: 861–874.
- 8
Mazur, J.E.
1986. Choice between single and multiple delayed reinforcers.
J. Exp. Anal. Behav.
46: 67–78.
- 9
Mazur, J.E., J.R. Stellar & M. Waraczynski.
1987. Self-control choice with electrical stimulation of the brain.
Behav. Processes
15: 143–153.
- 10
Green, L. & H. Rachlin.
1991. Economic substitutability of electrical brain stimulation, food, and water.
J. Exp. Anal. Behav.
55: 133–143.
- 11
Robbins, T.W. & B.J. Everitt.
1996. Neurobehavioral mechanisms of reward and motivation.
Curr. Opin. Neurobiol.
6: 228–236.
- 12
Schultz, W., P. Dayan & P.R. Montague.
1997. A neural substrate of prediction and reward.
Science
275: 1593–1599.
- 13
Breiter H.C., R.L. Gollub, R.M. Weisskoff, D.N. Kennedy, N. Makis, J.D. Berke, J.M. Goodman, H.L. Kantor, D.R. Gastfriend, J.P. Riorden, R.T. Mathew, B.R. Rosen & S.E. Hyan.
1997. Acute effects of cocaine on human brain activity and emotion.
Neuron
19: 591–611.
- 14
Heimer, L., R.E. Harlan, G.F. Alheid, M.M. Garcia & J. de Olmos.
1997. Substantia innominata: a notion which impedes clinical-anatomical correlations in neuropsychiatric disorders.
Neuroscience
76(4): 957–1006.
- 15
Alheid, G.F. & L. Heimer.
1988. New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders; the striatopallidal, amygdaloid, and corticopetal components of substantia innominata.
Neuroscience
27: 1–39.
- 16
Gollub, R., H. Breiter, R. Weisskoff, W. Kennedy, H. Kantor, D. Kennedy, D. Gastfriend, T. Matthew, N. Makris, A. Guimares, J. Riorden, S, Hyman, B. Rosen & R. Weisskoff.
1998. Cocaine decreases cortical blood flow, but does not obscure regional activation in functional magnetic resonance imaging in human subjects.
J. Cereb. Blood Flow Metab.
18(7): 724–34.
- 17
Breiter, H.C., R.L. Gollub, W. Edminster, T. Talavage, N. Makris, J. Melcher, D. Kennedy, H. Kantor, I. Elman, J. Riorden, D. Gastfriend, T. Campbell, M. FOLEY, R.M. Weisskoff & B.R. Rosen.
1998. Cocaine induced brainstem and subcoartical activity observed through fMRI with cardiac gating.
Proc. Int. Soc. Magn. Reson. Med.
1: 499.
- 18
Johanson, C.E. & M.W. Fischman.
1989. The pharmacology of cocaine related to its abuse.
Pharmacol. Rev.
41: 3–52.
- 19
Arvanitogiannis, A., M. Waraczynski & P. Shizgal.
1996. Effects of excitotoxic lesions of the basal forebrain on MFB self-stimulation.
Physiol. & Behav.
59(4/5): 795–806.
- 20
Everitt, B.J., K.A. Morris, A. O'Brien & T.W. Robbins.
1991. The basolateral amygdala-ventral striatal system and conditioned place preference: further evidence of limbic-striatal interactions underlying reward-related processes.
J. Neurosci.
42: 1–18.
- 21
Breiter, H.C., N.L. Etcoff, P.J. Whalen, W.A. Kennedy, S.L. Rauch, R.L. Buckner, M.M. Strauss, S.E. Hyman & B.R. Rosen.
1996a. Response and habituation of the human amygdala during visual processing of facial expression.
Neuron
17: 875–887.
- 22
Breiter, H.C., S.L. Rauch, K.K. Kwong, J.R. Baker, R.M. Weisskoff, D.N. Kennedy, A.D. Kendrick, T.L. Davis, A. Jiang, M.S. Cohen, C.E. Stern, J.W. Belliveau, L. Baer, R.L. O'Sullivan, C.R. Savage, M.A. Jenike & B.R. Rosen.
1996b. Functional magnetic resonance imaging of symptom provocation in obsessive-compulsive disorder.
Arch. Gen. Psychiatry
53: 595–606.
- 23
Carelli, R.M. & S.A. Deadwyler.
1996. Dual factors controlling activity of nucleus accumbens cell-firing during cocaine self-administration.
Synapse
24: 308–311.
- 24
Lynd-Balta, E. & S.N. Haber.
1994. The organization of midbrain projections to the ventral striatium in the primate.
Neuroscience
59: 609–623.
- 25
Heimer, L., G.F. Alheid, J.S. de Olmos, H.J. Groenewegen, S.N. Haber, R.E. Harlan & D.S. Zahm.
1997. The accumbens: beyond the core-shell dichotomy.
J. Neuropsychiatry Clin. Neurosci.
9(3): 354–81.
- 26
Schultz, W., P. Apicella & T. Ljungberg.
1993. Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task.
J. Neurosci.
13(3): 900–913.
- 27
Peoples, L.L. & M.O. West.
1996. Phasic firing of single neurons in the rat nucleus accumbens correlated with the timing of intravenous cocaine self-administration.
J. Neurosci.
16(10): 3459–3473.
- 28
Guimares, A.R., J.R. Melcher, T.M. Talavage, J.R. Baker, B.R. Rosen & R.M. Weisskoff.
1996. Detection of inferior colliculus activity during auditory stimulation usingcardiac gated functional MRI with T1 correction.
NeuroImage
3(3): S9.
- 29
Edminster, W.B., T.M. Talavage, P.J. LEDDEN & R.M. Weisskoff.
1999. Improved auditory cortex imaging using clustered volume acquisitions.
Hum. Brain Map
7(2): 89–97.
- 30
Seidman, L.J., H.C. Breiter, J.M. Goldstein, J.M. Goddman, M. Ward,.W.R. Woodruff, S.V. Faraone, D.N. Kennedy, R.M. Weisskoff, B.R. Rosen & M.T. Tsuang.
1997. Functional MRI of attention in relatives of schizophrenic patients.
Schizophr. Res.
24: 172.
- 31
Goldstein, J.M., L.J. Seidman, R. Anagnoson, J.M. Goodman, R. Weisskoff, M.F. Ward, M.R. PATTI, S.V. Faraone, M.T. Tsuang, B.R. Rosen & H. Breiter.
1998. An fMRI study of sex differences in auditory verbal working memory in normals.
NeuroImage
7(4): S854.
- 32
Breiter, H.C., L.J. Seidman, J.M. Goodman, J.M. Goldstein, K.M. O'Craven, R.M. Weisskoff, P.W.R. Woodruff, R. Savoy, A. Jiang, D. Kennedy, W. Kennedy, M.T. Tsuang & B.R. Rosen.
1995a. fMRI of effortful attention using Talairach averaging across subjects.
Proc. Soc. Magn. Reson./Eur. Soc. Magn. Reson. Med. Biol. Joint Meeting
3: 1348.
- 33
Breiter, H.C., L.J. Seidman, J.M. Goodman, J.M. Goldstein, K.M. O'Craven, R.M. Weisskoff, P.W.R. Woodruff, R. Savoy, A. Jiang, D. Kennedy, W. Kennedy, M.T. Tsuang & B.R. Rosen
1995b. Functional MRI of auditory effortful attention in humans.
Proc. Soc. Neurosci.
3: 1988.
- 34
Seidman, L.J., H.C. Breiter, J.M. Goodman, J.M. Goldstein, P.W.R., K. O'Craven, R. Savoy, D. Kennedy, J. Baker, K. Kwong, M.T. Tsuang & B.R. Rosen.
1996. Development of auditory continuous performance tests for functional MRI.
Biol. Psychiatry
39: 636.
- 35
Seidman, L.J., H.C. Breiter, J.M. Goldstein, P.W.R. Woodruff, K. O'Craven, R. Savoy, M.T. Tsuang & B.R. Rosen.
1998. A functional magnetic resonance imagining study of auditory vigilance with low and high information processing demands.
Neuropsychology
12(4): 505–518.
- 36
Berns, G.S., J.D. Cohen & M.A. Mintun.
1997. Brain regions responsive to novelty in the absence of awareness.
Science
276: 1272–1275.
- 37
Taghzouti, K., A. Louilot, J.P. Herman, M. Le Moal & H. Simon.
1985. Alternative behavioral, spatial discrimination, and 6-hydroxydopamine lesions in the nucleus accumbens of the rat.
Behav. Neural Biol.
44(3): 354–363.
- 38
Mogenson, G.J., D.L. Jones & C.Y. Yim.
1980. From motivation to action: functional iterface between the limbic system and the motor system.
Prog. Neurobiol.
14(2-3): 69–97.
- 39
Stern, C.E. & R.E. Passingham.
1995. The nucleus accumbens in monkeys (Macaca fascicularis): III.
Reversal learning. Exp. Brain Res.
106: 239–247.
- 40
Kahneman, D. 1973. Attention and effort. Prentice Hall. Englewood Cliffs, NJ.
- 41
Gibbon, J.
1977. Scalar expectancy theory and Weber's law in animal timing.
Psychol. Rev.
84: 279–325.
- 42
Gibbon, J., R.M. Church, S. Fairhurst & A. Kacelnik.
1988. Scalar expectancy theory and choice between delayed rewards.
Psychol. Rev.
95: 102–114.
- 43
Gallagher, M. & A.A. Chiba.
1996. The amygdala and emotion.
Curr. Opin. Neurobiol.
6: 221–227.
- 44
Shizgal, P. & K. Conover.
1996. On the neural computation of utility.
Curr. Directions Psychol. Sci.
5(2): 37–43.
- 45
Rompre, P.P. & P. Shizgal.
1986. Electrophysiological characteristics of neurons in forebrain regions implicated in self-stimulation of the medial forebrain bundle in the rat.
Brain Res.
364: 338–349.
- 46
Shizgal, P. & B. Murray. 1989. Neuronal basis of intracranial self-stimulation. In The neuropharmacological basis of reward. J.M. Lieman & S.J. Coopers, Eds.: 106-163. Oxford University Press. Oxford.
- 47
Koob, G.F., P.P. Sana & F.E. Bloom.
1998. Neuroscience of addiction.
Neuron
21: 1–20.
- 48
Schultz, W., P. Apicella, E. Scarnati & T. Ljungberg.
1992. Neuronal activity in monkey ventral striatum related to the expectation of reward.
J. Neurosci.
12: 4595–4610.
- 49
Williams, G.V. 1989. Neuronal activity in the primate caudate nucleus and ventral striatum reflects the association between stimuli determining behavior. In Neural Mechanisms in Disorders of Movement. A.R. Crossman & M.A. Sambrook, Eds.: 63-73. John Libbey. London.
- 50
Breiter, H.C., J.D. Berke, W.A. Kennedy, B.R. Rosen & S.E. Hyman.
1996c. Activation of striatum and amygdala during reward conditioning: an fMRI study.
NeuroImage
3(3): S220.
- 51
Tai, C.T., A.J.M. Clark, J. Feldon & J.N.P. Rawlins.
1991. Electrolytic lesions of the nucleus accumbens in rats which abolish the PREE enhance the locomotor response to amphetamine.
Exp. Brain Res.
86: 333–340.
- 52
Stern, C.E. & R.E. Passingham.
1996. The nucleus accumbens in monkeys (Macaca fascicularis): II.
Emotion and motivation. Behav. Brain Res.
75: 179–193.
- 53
Eccles, J.C. 1989. Evolution of the Brain, Creation of the Self. Routledge. New York.
- 54
MacLean, P.D. 1986. Culminating developments in the evolution of the limbic system: the thalamocingulate division. In The Limbic System: Functional Organization and Clinical Disorders. B.K. Doane & K.E. Livingston, Eds. Raven Press. New York.
- 55
Wise, R.A.
1982. Neuroleptics and operant behavior: the anhedonia hypothesis.
Behav. Brain Sci.
5: 39–87.
- 56
Robinson, T.E. & K.C. Berridge.
1993. The neural basis of drug craving: an incentive-sensitization theory of addiction.
Brain Res. Brain Res. Rev.
18: 247–291.
- 57
Blackburn, J., J. Pfaus & A. Phillips.
1992. Dopamine functions in appetitive and defensive behaviors.
Prog. Neurobiol.
3: 247–279.
- 58
Salamone, J.D., M.S. Cousins & B.J. Snyder.
1997. Behavioral functions of nucleus accumbens dopamine empirical and conceptual problems with the anhedonia hypothesis.
Neurosci. Biobehav. Rev.
21: 341–359.
- 59
Weiss, S.R.B., R.M. Post, A. Pert, R. Woodward & D. Murman.
1989. Context-dependent cocaine sensitization: differential effect of haloperidol on development versus expression.
Pharmacol. Biochem. Behav.
34: 655.
- 60
Everitt, B.J.
1997. Craving cocaine cues: cognitive neuroscience meets drug addiction research.
Trends Cogn. Sci.
1(1): 1–2.
- 61
Kahneman, D., P.P. Wakker & R. Sarin.
1997. Back to Bentham? Explorations of experienced utility.
Q. J. Economics
112(2): 375–405.
- 62
Childress, A.R.
et al.
1999. Brain correlates of cue-induced cocaine and opiate craving.
Am. J. Psychol.
22: 933.
- 63
Grant, S., E. London, D. Newlin, V. Villemagne, X. Liu, C. Contoreggi, R. Phillips & A. Margolin.
1996. Activation of memory circuits during cue-elicited cocaine craving.
Proc. Natl. Acad. Sci. USA
93: 12040–12045.
- 64
Schweitzer, J.
et al.
1996. The neuroanatomy of drug craving in crack cocaine addiction: a PET analysis.
Soc. Neurosci. Abstr.
22: 933.
- 65
Ito, N., H. Ishida, F. Miyakawa & H. Naito.
1974. Microelectrode study of projections from the amygdaloid complex to the nucleus accumbens in the cat.
Brain Res.
67: 338–341.
- 66
Yim, C.Y. & G.J. Mogenson.
1982. Response of nucleus accumbens neurons to amygdala stimulation and its modification by dopamine.
Brain Res.
239: 401–415.
- 67
Russchen, F.T., I. Bakst, D.G. Amaral & J.L. Price.
1985. The amygdalostiatal projections in the monkey.
An anterograde tracing study. Brain Res.
329: 241–257.
- 68
Amaral, D.G., J.L. Price, A. Pitkanen & S.T. Carmichael. 1992. Anatomical organization of the primate amygdala complex. In The Amygdala. J.P. Aggleton, Ed. John Wiley-Liss. New York.
- 69
Jones, B. & M. Mishkin.
1972. Limbic lesion and the problem of stimulus-reinforcement association.
Exp. Neurol.
36: 362–377.
- 70
Spiegler, B.J. & M. Mishkin.
1981. Evidence for the sequential participation of inferior temporal cortex and amygdala in the acquisition of stimulus-reward associations.
Behav. Brain Res.
3: 303–317.
- 71
Gaffan, D. & S. Harrison.
1987. Amygdalectomy and disconnection in visual learning for auditory secondary reinforcementby monkeys.
J. Neurosci.
7: 2285–2292.
- 72
Gaffan, D. & S. Harrison.
1988. Disconnection of the amygdala from visual association cortex impairs visual reward-association learning in monkeys.
J. Neurosci.
8: 3144–3150.
- 73
Cador, M., T.W. Robbins & B.J. Everitt.
1989. Involvment of the amygdala in stimulus-reward association: interaction with the ventral stratium.
Neuroscience
30(1): 77–86.
- 74
Ledoux, J.E. 1992. Emotion and the amygdala. In The amygdala: neurobiological aspects of emotion, memory and mental dysfunction. J.P. Aggleton, Ed.: 339-351. Wiley-Liss. New York.
- 75
Hatfield, T., J.-S. Han, M. Conley, M. Gallagher & P. Holland.
1996. Neurotoxic lesions of basolateral, but not central, amygdala interfere with pavlovian second-order conditioning and reinforcer devaluation effects.
J. Neurosci.
16: 5256–5265.
- 76
Rolls, E.T. 1991. The processing of face information in the primate temporal lobe. In Processing Images of Faces. V. Bruce & M. Burton, Eds. Ablex. Norwood, NJ.