 |
 Previous Article | Next Article 
Journal of Neuroscience, Vol 9, 1465-1472, Copyright © 1989 by Society for Neuroscience
Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems
MG Packard, R Hirsh and NM White
Department of Psychology, McGill University, Montreal, Quebec, Canada.
The present experiments were designed to examine the hypothesis that the
mammalian brain contains anatomically distinct memory systems. Rats with
bilateral lesions of caudate nucleus or fimbria-fornix and a control group
were tested postoperatively on 1 of 2 versions of the radial maze task. In
a standard win-shift version, each of the 8 arms of the maze was baited
once, and the number of errors (revisits) in the first 8 choices of each
trial was recorded. Fimbria-fornix rats were impaired in choice accuracy,
while caudate animals were unimpaired relative to controls. Different
groups of rats with similar lesions were tested on a newly developed
win-stay version of the radial maze, in which the location of 4 randomly
selected baited arms was signaled by a light at the entrance to each arm,
and which required rats to revisit arms in which reinforcement had been
previously acquired within a trial. Rats with fimbria-fornix lesions were
superior to controls in choice accuracy on the win-stay radial maze task,
while caudate animals were impaired relative to controls. The results
demonstrate a double dissociation of the mnemonic functions of the
hippocampus and caudate nucleus. Some implications of the presence of 2
memory systems in the mammalian brain are discussed.
This article has been cited by other articles:
|
|
|
|
 
R. Ito, T. W. Robbins, C. M. Pennartz, and B. J. Everitt
Functional Interaction between the Hippocampus and Nucleus Accumbens Shell Is Necessary for the Acquisition of Appetitive Spatial Context Conditioning
J. Neurosci.,
July 2, 2008;
28(27):
6950 - 6959.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. E. Atallah, J. W. Rudy, and R. C. O'Reilly
The role of the dorsal striatum and dorsal hippocampus in probabilistic and deterministic odor discrimination tasks
Learn. Mem.,
April 25, 2008;
15(5):
294 - 298.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. F. Doeller, J. A. King, and N. Burgess
Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory
PNAS,
April 15, 2008;
105(15):
5915 - 5920.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Nagano-Saito, M. Leyton, O. Monchi, Y. K. Goldberg, Y. He, and A. Dagher
Dopamine Depletion Impairs Frontostriatal Functional Connectivity during a Set-Shifting Task
J. Neurosci.,
April 2, 2008;
28(14):
3697 - 3706.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. D. Bohbot, J. Lerch, B. Thorndycraft, G. Iaria, and A. P. Zijdenbos
Gray Matter Differences Correlate with Spontaneous Strategies in a Human Virtual Navigation Task
J. Neurosci.,
September 19, 2007;
27(38):
10078 - 10083.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. J. McAuliffe, B. Joseph, and C. V. Vorhees
Isoflurane-Delayed Preconditioning Reduces Immediate Mortality and Improves Striatal Function in Adult Mice After Neonatal Hypoxia-Ischemia
Anesth. Analg.,
May 1, 2007;
104(5):
1066 - 1077.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. J. Broadbent, L. R. Squire, and R. E. Clark
Rats depend on habit memory for discrimination learning and retention
Learn. Mem.,
March 8, 2007;
14(3):
145 - 151.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Schwabe, M. S. Oitzl, C. Philippsen, S. Richter, A. Bohringer, W. Wippich, and H. Schachinger
Stress modulates the use of spatial versus stimulus-response learning strategies in humans
Learn. Mem.,
January 1, 2007;
14(1-2):
109 - 116.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. G. Murphy, N. P. Rahnama, and A. J. Silva
Investigation of Age-Related Cognitive Decline Using Mice as a Model System: Behavioral Correlates
Am J Geriatr Psychiatry,
December 1, 2006;
14(12):
1004 - 1011.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. A. Teather and R. J. Wurtman
Chronic Administration of UMP Ameliorates the Impairment of Hippocampal-Dependent Memory in Impoverished Rats
J. Nutr.,
November 1, 2006;
136(11):
2834 - 2837.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Steidl, S. Mohi-uddin, and A. K. Anderson
Effects of emotional arousal on multiple memory systems: Evidence from declarative and procedural learning
Learn. Mem.,
September 1, 2006;
13(5):
650 - 658.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Foerde, B. J. Knowlton, and R. A. Poldrack
Modulation of competing memory systems by distraction
PNAS,
August 1, 2006;
103(31):
11778 - 11783.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Orban, G. Rauchs, E. Balteau, C. Degueldre, A. Luxen, P. Maquet, and P. Peigneux
Sleep after spatial learning promotes covert reorganization of brain activity
PNAS,
May 2, 2006;
103(18):
7124 - 7129.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Martel, A. Millard, R. Jaffard, and J.-L. Guillou
Stimulation of hippocampal adenylyl cyclase activity dissociates memory consolidation processes for response and place learning.
Learn. Mem.,
May 1, 2006;
13(3):
342 - 348.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. H. Son, D. Geum, S. Chung, E. J. Kim, J.-H. Jo, C.-M. Kim, K. H. Lee, H. Kim, S. Choi, H. T. Kim, et al.
Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity.
J. Neurosci.,
March 22, 2006;
26(12):
3309 - 3318.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. R. Fletcher, M. E. Calhoun, P. R. Rapp, and M. L. Shapiro
Fornix Lesions Decouple the Induction of Hippocampal Arc Transcription from Behavior But Not Plasticity
J. Neurosci.,
February 1, 2006;
26(5):
1507 - 1515.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Schoenbaum and T. A. Stalnaker
Thanks for the memories...
Learn. Mem.,
November 1, 2005;
12(6):
547 - 548.
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. C. Pych, Q. Chang, C. Colon-Rivera, R. Haag, and P. E. Gold
Acetylcholine release in the hippocampus and striatum during place and response training
Learn. Mem.,
November 1, 2005;
12(6):
564 - 572.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Lenartowicz and A. R. McIntosh
The Role of Anterior Cingulate Cortex in Working Memory is Shaped by Functional Connectivity
J. Cogn. Neurosci.,
July 1, 2005;
17(7):
1026 - 1042.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. E. Canal, S. J. Stutz, and P. E. Gold
Glucose injections into the dorsal hippocampus or dorsolateral striatum of rats prior to T-maze training: Modulation of learning rates and strategy selection
Learn. Mem.,
July 1, 2005;
12(4):
367 - 374.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Wolbers and C. Buchel
Dissociable Retrosplenial and Hippocampal Contributions to Successful Formation of Survey Representations
J. Neurosci.,
March 30, 2005;
25(13):
3333 - 3340.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. W. McElroy and D. L. Korol
Intrahippocampal muscimol shifts learning strategy in gonadally intact young adult female rats
Learn. Mem.,
March 1, 2005;
12(2):
150 - 158.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. A. Teather and R. J. Wurtman
Dietary CDP-choline supplementation prevents memory impairment caused by impoverished environmental conditions in rats
Learn. Mem.,
January 1, 2005;
12(1):
39 - 43.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Marsh, G. M. Alexander, M. G. Packard, H. Zhu, J. C. Wingard, G. Quackenbush, and B. S. Peterson
Habit Learning in Tourette Syndrome: A Translational Neuroscience Approach to a Developmental Psychopathology
Arch Gen Psychiatry,
December 1, 2004;
61(12):
1259 - 1268.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Arkadir, G. Morris, E. Vaadia, and H. Bergman
Independent Coding of Movement Direction and Reward Prediction by Single Pallidal Neurons
J. Neurosci.,
November 10, 2004;
24(45):
10047 - 10056.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. A. Christie and S. M. Hersch
Demonstration of nondeclarative sequence learning in mice: Development of an animal analog of the human serial reaction time task
Learn. Mem.,
November 1, 2004;
11(6):
720 - 723.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Cavaco, S. W. Anderson, J. S. Allen, A. Castro-Caldas, and H. Damasio
The scope of preserved procedural memory in amnesia
Brain,
August 1, 2004;
127(8):
1853 - 1867.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. H. Yin and B. J. Knowlton
Contributions of Striatal Subregions to Place and Response Learning
Learn. Mem.,
July 1, 2004;
11(4):
459 - 463.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Ergorul and H. Eichenbaum
The Hippocampus and Memory for "What," "Where," and "When"
Learn. Mem.,
July 1, 2004;
11(4):
397 - 405.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. G. Ashby and B. J. Spiering
The Neurobiology of Category Learning
Behav Cogn Neurosci Rev,
June 1, 2004;
3(2):
101 - 113.
[Abstract]
[PDF]
|
|
|
|
|
|
|
N. Schmitzer-Torbert and A. D. Redish
Neuronal Activity in the Rodent Dorsal Striatum in Sequential Navigation: Separation of Spatial and Reward Responses on the Multiple T Task
J Neurophysiol,
May 1, 2004;
91(5):
2259 - 2272.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. D. Lieberman, G. Y. Chang, J. Chiao, S. Y. Bookheimer, and B. J. Knowlton
An Event-Related fMRI Study of Artificial Grammar Learning in a Balanced Chunk Strength Design
J. Cogn. Neurosci.,
March 1, 2004;
16(3):
427 - 438.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. A. Christie and J. C. Dalrymple-Alford
A New Rat Model of the Human Serial Reaction Time Task: Contrasting Effects of Caudate and Hippocampal Lesions
J. Neurosci.,
February 4, 2004;
24(5):
1034 - 1039.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. R. Sage, S. G. Anagnostaras, S. Mitchell, J. M. Bronstein, A. De Salles, D. Masterman, and B. J. Knowlton
Analysis of Probabilistic Classification Learning in Patients With Parkinson's Disease Before and After Pallidotomy Surgery
Learn. Mem.,
May 1, 2003;
10(3):
226 - 236.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. W. Weickert, A. Terrazas, L. B. Bigelow, J. D. Malley, T. Hyde, M. F. Egan, D. R. Weinberger, and T. E. Goldberg
Habit and Skill Learning in Schizophrenia: Evidence of Normal Striatal Processing With Abnormal Cortical Input
Learn. Mem.,
November 1, 2002;
9(6):
430 - 442.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. G. Mair, J. K. Koch, J. B. Newman, J. R. Howard, and J. A. Burk
A Double Dissociation within Striatum between Serial Reaction Time and Radial Maze Delayed Nonmatching Performance in Rats
J. Neurosci.,
August 1, 2002;
22(15):
6756 - 6765.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. A. Poldrack
Neural systems for perceptual skill learning.
Behav Cogn Neurosci Rev,
March 1, 2002;
1(1):
76 - 83.
[Abstract]
[PDF]
|
|
|
|
|
|
|
A. E. Baldwin, K. Sadeghian, and A. E. Kelley
Appetitive Instrumental Learning Requires Coincident Activation of NMDA and Dopamine D1 Receptors within the Medial Prefrontal Cortex
J. Neurosci.,
February 1, 2002;
22(3):
1063 - 1071.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. A. Teather, M. G. Packard, and N. G. Bazan
Post-Training Cyclooxygenase-2 (COX-2) Inhibition Impairs Memory Consolidation
Learn. Mem.,
January 1, 2002;
9(1):
41 - 47.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. D. Berke, H. B. Eichenbaum, S. R. Vorel, and E. L. Gardner
Drug Addiction and the Hippocampus
Science,
November 9, 2001;
294(5545):
1235a - 1235.
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. J. Kim, H. J. Lee, J.-S. Han, and M. G. Packard
Amygdala Is Critical for Stress-Induced Modulation of Hippocampal Long-Term Potentiation and Learning
J. Neurosci.,
July 15, 2001;
21(14):
5222 - 5228.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Dagher, A. M. Owen, H. Boecker, and D. J. Brooks
The role of the striatum and hippocampus in planning: A PET activation study in Parkinson's disease
Brain,
May 1, 2001;
124(5):
1020 - 1032.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Fernandez-Ruiz, J. Wang, T. G. Aigner, and M. Mishkin
Visual habit formation in monkeys with neurotoxic lesions of the ventrocaudal neostriatum
PNAS,
March 27, 2001;
98(7):
4196 - 4201.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. G. Packard, S. F. Vecchioli, J. P. Schroeder, and A. Gasbarri
Task-Dependent Role for Dorsal Striatum Metabotropic Glutamate Receptors in Memory
Learn. Mem.,
March 1, 2001;
8(2):
96 - 103.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
R. A. Poldrack and J. D. E. Gabrieli
Characterizing the neural mechanisms of skill learning and repetition priming: Evidence from mirror reading
Brain,
January 1, 2001;
124(1):
67 - 82.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Teng, L. Stefanacci, L. R. Squire, and S. M. Zola
Contrasting Effects on Discrimination Learning after Hippocampal Lesions and Conjoint Hippocampal-Caudate Lesions in Monkeys
J. Neurosci.,
May 15, 2000;
20(10):
3853 - 3863.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. L. McGaugh
Memory--a Century of Consolidation
Science,
January 14, 2000;
287(5451):
248 - 251.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
S. B. Floresco, D. N. Braaksma, and A. G. Phillips
Thalamic-Cortical-Striatal Circuitry Subserves Working Memory during Delayed Responding on a Radial Arm Maze
J. Neurosci.,
December 15, 1999;
19(24):
11061 - 11071.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Sebret, I. Lena, D. Crete, T. Matsui, B. P. Roques, and V. Dauge
Rat Hippocampal Neurons Are Critically Involved in Physiological Improvement of Memory Processes Induced by Cholecystokinin-B Receptor Stimulation
J. Neurosci.,
August 15, 1999;
19(16):
7230 - 7237.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J.-L. Guillou, G. M. Rose, and D. M. F. Cooper
Differential Activation of Adenylyl Cyclases by Spatial and Procedural Learning
J. Neurosci.,
July 15, 1999;
19(14):
6183 - 6190.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. D. Devan and N. M. White
Parallel Information Processing in the Dorsal Striatum: Relation to Hippocampal Function
J. Neurosci.,
April 1, 1999;
19(7):
2789 - 2798.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Tremblay, J. R. Hollerman, and W. Schultz
Modifications of Reward Expectation-Related Neuronal Activity During Learning in Primate Striatum
J Neurophysiol,
August 1, 1998;
80(2):
964 - 977.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. C. McNay and P. E. Gold
Memory Modulation Across Neural Systems: Intra-Amygdala Glucose Reverses Deficits Caused by Intraseptal Morphine on a Spatial Task But Not on an Aversive Task
J. Neurosci.,
May 15, 1998;
18(10):
3853 - 3858.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. L. McGaugh, L. Cahill, and B. Roozendaal
Involvement of the amygdala in memory storage: Interaction with other brain systems
PNAS,
November 26, 1996;
93(24):
13508 - 13514.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. R. Squire and S. M. Zola
Structure and function of declarative and nondeclarative memory systems
PNAS,
November 26, 1996;
93(24):
13515 - 13522.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. J. Knowlton, J. A. Mangels, and L. R. Squire
A Neostriatal Habit Learning System in Humans
Science,
September 6, 1996;
273(5280):
1399 - 1402.
[Abstract]
|
|
|
|
|
|
|
B J Knowlton, L R Squire, and M A Gluck
Probabilistic classification learning in amnesia.
Learn. Mem.,
January 1, 1994;
1(2):
106 - 120.
[Abstract]
[PDF]
|
|
|
|
|
|
|
B. Knowlton and L. Squire
The learning of categories: parallel brain systems for item memory and category knowledge
Science,
December 10, 1993;
262(5140):
1747 - 1749.
[Abstract]
[PDF]
|
|
|
|
|
|
|
R Desimone
The physiology of memory: recordings of things past
Science,
October 9, 1992;
258(5080):
245 - 246.
[PDF]
|
|
|
|
|
|
|
L. Squire and S Zola-Morgan
The medial temporal lobe memory system
Science,
September 20, 1991;
253(5026):
1380 - 1386.
[Abstract]
[PDF]
|
|
|
|
