 |
Previous Article | Next Article 
The Journal of Neuroscience, March 15, 2000, 20(6):2369-2382
Striatonigrostriatal Pathways in Primates Form an Ascending
Spiral from the Shell to the Dorsolateral Striatum
Suzanne N.
Haber1, 2,
Julie L.
Fudge1, 3, and
Nikolaus R.
McFarland1
Departments of 1 Neurobiology and Anatomy,
2 Neurology, and 3 Psychiatry, University of
Rochester School of Medicine, Rochester, New York 14642
Clinical manifestations in diseases affecting the dopamine system
include deficits in emotional, cognitive, and motor function. Although
the parallel organization of specific corticostriatal pathways is well
documented, mechanisms by which dopamine might integrate information
across different cortical/basal ganglia circuits are less well
understood. We analyzed a collection of retrograde and anterograde
tracing studies to understand how the striatonigrostriatal (SNS)
subcircuit directs information flow between ventromedial (limbic),
central (associative), and dorsolateral (motor) striatal regions. When
viewed as a whole, the ventromedial striatum projects to a wide
range of the dopamine cells and receives a relatively small dopamine
input. In contrast, the dorsolateral striatum (DLS) receives input from
a broad expanse of dopamine cells and has a confined input to the
substantia nigra (SN). The central striatum (CS) receives input from
and projects to a relatively wide range of the SN. The SNS projection
from each striatal region contains three substantia nigra components: a
dorsal group of nigrostriatal projecting cells, a central region
containing both nigrostriatal projecting cells and its reciprocal
striatonigral terminal fields, and a ventral region that receives a
specific striatonigral projection but does not contain its reciprocal
nigrostriatal projection. Examination of results from multiple tracing
experiments simultaneously demonstrates an interface between different
striatal regions via the midbrain dopamine cells that forms an
ascending spiral between regions. The shell influences the core, the
core influences the central striatum, and the central striatum
influences the dorsolateral striatum. This anatomical arrangement
creates a hierarchy of information flow and provides an anatomical
basis for the limbic/cognitive/motor interface via the ventral midbrain.
Key words:
dorsal striatum; frontal cortex; shell; substantia nigra; ventral striatum; ventral tegmental area
Copyright © 2000 Society for Neuroscience 0270-6474/00/2062369-14$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
S. A. Coombes, C. Tandonnet, H. Fujiyama, C. M. Janelle, J. H. Cauraugh, and J. J. Summers
Emotion and motor preparation: A transcranial magnetic stimulation study of corticospinal motor tract excitability
Cogn Affect Behav Neurosci,
December 1, 2009;
9(4):
380 - 388.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
S. J. Gershman, B. Pesaran, and N. D. Daw
Human Reinforcement Learning Subdivides Structured Action Spaces by Learning Effector-Specific Values
J. Neurosci.,
October 28, 2009;
29(43):
13524 - 13531.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. M. A. Pennartz, J. D. Berke, A. M. Graybiel, R. Ito, C. S. Lansink, M. van der Meer, A. D. Redish, K. S. Smith, and P. Voorn
Corticostriatal Interactions during Learning, Memory Processing, and Decision Making
J. Neurosci.,
October 14, 2009;
29(41):
12831 - 12838.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Darvas and R. D. Palmiter
Restriction of dopamine signaling to the dorsolateral striatum is sufficient for many cognitive behaviors
PNAS,
August 25, 2009;
106(34):
14664 - 14669.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Y. Kimchi, M. M. Torregrossa, J. R. Taylor, and M. Laubach
Neuronal Correlates of Instrumental Learning in the Dorsal Striatum
J Neurophysiol,
July 1, 2009;
102(1):
475 - 489.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. H. B. FitzGerald, B. Seymour, and R. J. Dolan
The Role of Human Orbitofrontal Cortex in Value Comparison for Incommensurable Objects
J. Neurosci.,
July 1, 2009;
29(26):
8388 - 8395.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. G. Caron and R. M. Wightman
"To learn, you must pay attention." Molecular insights into teachers' wisdom
PNAS,
May 5, 2009;
106(18):
7267 - 7268.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Zhang, L. Zhang, Y. Liang, A. G. Siapas, F.-M. Zhou, and J. A. Dani
Dopamine Signaling Differences in the Nucleus Accumbens and Dorsal Striatum Exploited by Nicotine
J. Neurosci.,
April 1, 2009;
29(13):
4035 - 4043.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X. A. Perez, K. T. O'Leary, N. Parameswaran, J. M. McIntosh, and M. Quik
Prominent Role of {alpha}3/{alpha}6{beta}2* nAChRs in Regulating Evoked Dopamine Release in Primate Putamen: Effect of Long-Term Nicotine Treatment
Mol. Pharmacol.,
April 1, 2009;
75(4):
938 - 946.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Brischoux, S. Chakraborty, D. I. Brierley, and M. A. Ungless
Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli
PNAS,
March 24, 2009;
106(12):
4894 - 4899.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Y. Kimchi and M. Laubach
Dynamic Encoding of Action Selection by the Medial Striatum
J. Neurosci.,
March 11, 2009;
29(10):
3148 - 3159.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. E. Forbes, A. R. Hariri, S. L. Martin, J. S. Silk, D. L. Moyles, P. M. Fisher, S. M. Brown, N. D. Ryan, B. Birmaher, D. A. Axelson, et al.
Altered Striatal Activation Predicting Real-World Positive Affect in Adolescent Major Depressive Disorder
Am J Psychiatry,
January 1, 2009;
166(1):
64 - 73.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Knutson and S. M Greer
Anticipatory affect: neural correlates and consequences for choice
Phil Trans R Soc B,
December 12, 2008;
363(1511):
3771 - 3786.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. R Delgado, J. Li, D. Schiller, and E. A Phelps
The role of the striatum in aversive learning and aversive prediction errors
Phil Trans R Soc B,
December 12, 2008;
363(1511):
3787 - 3800.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Di Martino, A. Scheres, D.S. Margulies, A.M.C. Kelly, L.Q. Uddin, Z. Shehzad, B. Biswal, J.R. Walters, F.X. Castellanos, and M.P. Milham
Functional Connectivity of Human Striatum: A Resting State fMRI Study
Cereb Cortex,
December 1, 2008;
18(12):
2735 - 2747.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. J Everitt, D. Belin, D. Economidou, Y. Pelloux, J. W Dalley, and T. W Robbins
Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction
Phil Trans R Soc B,
October 12, 2008;
363(1507):
3125 - 3135.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Strathearn, J. Li, P. Fonagy, and P. R. Montague
What's in a Smile? Maternal Brain Responses to Infant Facial Cues
Pediatrics,
July 1, 2008;
122(1):
40 - 51.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Kasanetz, L. A. Riquelme, V. Della-Maggiore, P. O'Donnell, and M. G. Murer
Functional integration across a gradient of corticostriatal channels controls UP state transitions in the dorsal striatum
PNAS,
June 10, 2008;
105(23):
8124 - 8129.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Belin, A. C. Mar, J. W. Dalley, T. W. Robbins, and B. J. Everitt
High Impulsivity Predicts the Switch to Compulsive Cocaine-Taking
Science,
June 6, 2008;
320(5881):
1352 - 1355.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. M Botvinick
Multilevel structure in behaviour and in the brain: a model of Fuster's hierarchy
Phil Trans R Soc B,
September 29, 2007;
362(1485):
1615 - 1626.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. R. Sadek, P. J. Magill, and J. P. Bolam
A Single-Cell Analysis of Intrinsic Connectivity in the Rat Globus Pallidus
J. Neurosci.,
June 13, 2007;
27(24):
6352 - 6362.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T.W Robbins
Shifting and stopping: fronto-striatal substrates, neurochemical modulation and clinical implications
Phil Trans R Soc B,
May 29, 2007;
362(1481):
917 - 932.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Boileau, A. Dagher, M. Leyton, R. N. Gunn, G. B. Baker, M. Diksic, and C. Benkelfat
Modeling Sensitization to Stimulants in Humans: An [11C]Raclopride/Positron Emission Tomography Study in Healthy Men
Arch Gen Psychiatry,
December 1, 2006;
63(12):
1386 - 1395.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. J. Scott, M. M. Heitzeg, R. A. Koeppe, C. S. Stohler, and J.-K. Zubieta
Variations in the human pain stress experience mediated by ventral and dorsal Basal Ganglia dopamine activity.
J. Neurosci.,
October 18, 2006;
26(42):
10789 - 10795.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. B. Postuma and A. Dagher
Basal Ganglia Functional Connectivity Based on a Meta-Analysis of 126 Positron Emission Tomography and Functional Magnetic Resonance Imaging Publications
Cereb Cortex,
October 1, 2006;
16(10):
1508 - 1521.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. N. Haber, K.-S. Kim, P. Mailly, and R. Calzavara
Reward-Related Cortical Inputs Define a Large Striatal Region in Primates That Interface with Associative Cortical Connections, Providing a Substrate for Incentive-Based Learning.
J. Neurosci.,
August 9, 2006;
26(32):
8368 - 8376.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. J. Lee, J. M. Youn, M. J. O, M. Gallagher, and P. C. Holland
Role of substantia nigra-amygdala connections in surprise-induced enhancement of attention.
J. Neurosci.,
May 31, 2006;
26(22):
6077 - 6081.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. A. Crone, C. Wendelken, S. E. Donohue, and S. A. Bunge
Neural Evidence for Dissociable Components of Task-switching
Cereb Cortex,
April 1, 2006;
16(4):
475 - 486.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. B. Floresco, S. Ghods-Sharifi, C. Vexelman, and O. Magyar
Dissociable Roles for the Nucleus Accumbens Core and Shell in Regulating Set Shifting
J. Neurosci.,
March 1, 2006;
26(9):
2449 - 2457.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. A. Schiltz
Habitual Responding and the Dorsal Striatum
J. Neurosci.,
February 15, 2006;
26(7):
1891 - 1892.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
O. Hikosaka, K. Nakamura, and H. Nakahara
Basal Ganglia Orient Eyes to Reward
J Neurophysiol,
February 1, 2006;
95(2):
567 - 584.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. J. M. J. Vanderschuren, P. Di Ciano, and B. J. Everitt
Involvement of the Dorsal Striatum in Cue-Controlled Cocaine Seeking
J. Neurosci.,
September 21, 2005;
25(38):
8665 - 8670.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. E. McCallum, N. Parameswaran, T. Bordia, J. M. McIntosh, S. R. Grady, and M. Quik
Decrease in {alpha}3*/{alpha}6* Nicotinic Receptors but Not Nicotine-Evoked Dopamine Release in Monkey Brain after Nigrostriatal Damage
Mol. Pharmacol.,
September 1, 2005;
68(3):
737 - 746.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Heinz, T. Siessmeier, J. Wrase, H. G. Buchholz, G. Grunder, Y. Kumakura, P. Cumming, M. Schreckenberger, M. N. Smolka, F. Rosch, et al.
Correlation of Alcohol Craving With Striatal Dopamine Synthesis Capacity and D2/3 Receptor Availability: A Combined [18F]DOPA and [18F]DMFP PET Study in Detoxified Alcoholic Patients
Am J Psychiatry,
August 1, 2005;
162(8):
1515 - 1520.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. J. Hernandez, M. E. Andrzejewski, K. Sadeghian, J. B. Panksepp, and A. E. Kelley
AMPA/kainate, NMDA, and dopamine D1 receptor function in the nucleus accumbens core: A context-limited role in the encoding and consolidation of instrumental memory
Learn. Mem.,
May 1, 2005;
12(3):
285 - 295.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. A. Seger and C. M. Cincotta
The Roles of the Caudate Nucleus in Human Classification Learning
J. Neurosci.,
March 16, 2005;
25(11):
2941 - 2951.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Guigoni, Q. Li, I. Aubert, S. Dovero, B. H. Bioulac, B. Bloch, A. R. Crossman, C. E. Gross, and E. Bezard
Involvement of Sensorimotor, Limbic, and Associative Basal Ganglia Domains in L-3,4-Dihydroxyphenylalanine-Induced Dyskinesia
J. Neurosci.,
February 23, 2005;
25(8):
2102 - 2107.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Heinz, T. Siessmeier, J. Wrase, D. Hermann, S. Klein, S. M. Grusser-Sinopoli, H. Flor, D. F. Braus, H. G. Buchholz, G. Grunder, et al.
Correlation Between Dopamine D2 Receptors in the Ventral Striatum and Central Processing of Alcohol Cues and Craving
Am J Psychiatry,
October 1, 2004;
161(10):
1783 - 1789.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Francois, D. Grabli, K. McCairn, C. Jan, C. Karachi, E.-C. Hirsch, J. Feger, and L. Tremblay
Behavioural disorders induced by external globus pallidus dysfunction in primates II. Anatomical study
Brain,
September 1, 2004;
127(9):
2055 - 2070.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. J. Porrino, D. Lyons, H. R. Smith, J. B. Daunais, and M. A. Nader
Cocaine Self-Administration Produces a Progressive Involvement of Limbic, Association, and Sensorimotor Striatal Domains
J. Neurosci.,
April 7, 2004;
24(14):
3554 - 3562.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Cools, L. Clark, and T. W. Robbins
Differential Responses in Human Striatum and Prefrontal Cortex to Changes in Object and Rule Relevance
J. Neurosci.,
February 4, 2004;
24(5):
1129 - 1135.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Heimer
A New Anatomical Framework for Neuropsychiatric Disorders and Drug Abuse
Am J Psychiatry,
October 1, 2003;
160(10):
1726 - 1739.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. L. Robinson, B. J. Venton, M. L.A.V. Heien, and R. M. Wightman
Detecting Subsecond Dopamine Release with Fast-Scan Cyclic Voltammetry in Vivo
Clin. Chem.,
October 1, 2003;
49(10):
1763 - 1773.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. L. Fudge and A. B. Emiliano
The Extended Amygdala and the Dopamine System: Another Piece of the Dopamine Puzzle
J Neuropsychiatry Clin Neurosci,
August 1, 2003;
15(3):
306 - 316.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
P. Mailly, S. Charpier, A. Menetrey, and J.-M. Deniau
Three-Dimensional Organization of the Recurrent Axon Collateral Network of the Substantia Nigra Pars Reticulata Neurons in the Rat
J. Neurosci.,
June 15, 2003;
23(12):
5247 - 5257.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. J. Cragg
Variable Dopamine Release Probability and Short-Term Plasticity between Functional Domains of the Primate Striatum
J. Neurosci.,
May 15, 2003;
23(10):
4378 - 4385.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. C. Cromwell and W. Schultz
Effects of Expectations for Different Reward Magnitudes on Neuronal Activity in Primate Striatum
J Neurophysiol,
May 1, 2003;
89(5):
2823 - 2838.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. S Mayberg
Modulating dysfunctional limbic-cortical circuits in depression: towards development of brain-based algorithms for diagnosis and optimised treatment
Br. Med. Bull.,
March 1, 2003;
65(1):
193 - 207.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F.-M. Zhou, C. Wilson, and J. A. Dani
Muscarinic and Nicotinic Cholinergic Mechanisms in the Mesostriatal Dopamine Systems
Neuroscientist,
February 1, 2003;
9(1):
23 - 36.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
H. S. Mayberg and A. M. Lozano
Penfield revisited?: Understanding and modifying behavior by deep brain stimulation for PD
Neurology,
November 12, 2002;
59(9):
1298 - 1299.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Ramanathan, J. J. Hanley, J.-M. Deniau, and J. P. Bolam
Synaptic Convergence of Motor and Somatosensory Cortical Afferents onto GABAergic Interneurons in the Rat Striatum
J. Neurosci.,
September 15, 2002;
22(18):
8158 - 8169.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Kaneda, A. Nambu, H. Tokuno, and M. Takada
Differential Processing Patterns of Motor Information Via Striatopallidal and Striatonigral Projections
J Neurophysiol,
September 1, 2002;
88(3):
1420 - 1432.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Ito, J. W. Dalley, T. W. Robbins, and B. J. Everitt
Dopamine Release in the Dorsal Striatum during Cocaine-Seeking Behavior under the Control of a Drug-Associated Cue
J. Neurosci.,
July 15, 2002;
22(14):
6247 - 6253.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. J. Cragg, C. J. Hille, and S. A. Greenfield
Functional Domains in Dorsal Striatum of the Nonhuman Primate Are Defined by the Dynamic Behavior of Dopamine
J. Neurosci.,
July 1, 2002;
22(13):
5705 - 5712.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. J. Everitt and M. E. Wolf
Psychomotor Stimulant Addiction: A Neural Systems Perspective
J. Neurosci.,
May 1, 2002;
22(9):
3312 - 3320.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Neuhoff, A. Neu, B. Liss, and J. Roeper
Ih Channels Contribute to the Different Functional Properties of Identified Dopaminergic Subpopulations in the Midbrain
J. Neurosci.,
February 15, 2002;
22(4):
1290 - 1302.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Haber and N. R. Mcfarland
The Place of the Thalamus in Frontal Cortical-Basal Ganglia Circuits
Neuroscientist,
August 1, 2001;
7(4):
315 - 324.
[Abstract]
[PDF]
|
 |
|
|

|