 |
Previous Article | Next Article 
Journal of Neuroscience, Vol 15, 3796-3807, Copyright © 1995 by Society for Neuroscience
Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys
P Alvarez, S Zola-Morgan and LR Squire
Group in Neurosciences, University of California at San Diego, La Jolla 92093, USA.
Research in humans and monkeys has demonstrated a system of anatomically
related structures in the medial temporal lobe that is important for memory
function. This system is comprised of the hippocampal region (i.e., the
dentate gyrus, hippocampus proper and subicular complex) and the
entorhinal, perirhinal, and parahippocampal cortices. While the hippocampal
region has long been thought to be important in memory, there are few
systematic studies in primates of the effects on memory of damage limited
to the hippocampal region. We have used magnetic resonance imaging
techniques, together with a stereotaxic approach, to produce bilateral
lesions limited to the hippocampal region (the H lesion). Damage to the
adjacent perirhinal, entorhinal, and parahippocampal cortex was minimal.
Monkeys with the H lesion exhibited significant and long-lasting impairment
on the delayed non-matching to sample task. At the same time, on this and
other amnesia-sensitive tasks, monkeys with the H lesion performed better
overall than monkeys with lesions of the hippocampal region that also
included damage to the adjacent entorhinal and parahippocampal cortices
(the H+ lesion). These findings show that, first, the hippocampal region
itself is essential for normal memory function; and second, the adjacent
entorhinal and parahippocampal cortices, either alone or in combination,
are also an essential component of the medial temporal lobe memory system.
This article has been cited by other articles:

|
 |

|
 |
 
J. L. Gerrard, S. N. Burke, B. L. McNaughton, and C. A. Barnes
Sequence Reactivation in the Hippocampus Is Impaired in Aged Rats
J. Neurosci.,
July 30, 2008;
28(31):
7883 - 7890.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Zarahn, B. Rakitin, D. Abela, J. Flynn, and Y. Stern
Positive Evidence against Human Hippocampal Involvement in Working Memory Maintenance of Familiar Stimuli
Cereb Cortex,
March 1, 2005;
15(3):
303 - 316.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. A. Buckmaster, H. Eichenbaum, D. G. Amaral, W. A. Suzuki, and P. R. Rapp
Entorhinal Cortex Lesions Disrupt the Relational Organization of Memory in Monkeys
J. Neurosci.,
November 3, 2004;
24(44):
9811 - 9825.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M E Lacruz, G Alarcon, N Akanuma, F C K Lum, N Kissani, M Koutroumanidis, N Adachi, C D Binnie, C E Polkey, and R G Morris
Neuropsychological effects associated with temporal lobectomy and amygdalohippocampectomy depending on Wada test failure
J. Neurol. Neurosurg. Psychiatry,
April 1, 2004;
75(4):
600 - 607.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X. Blaizot, A. Martinez-Marcos, M. d. M. Arroyo-Jimenez, P. Marcos, E. Artacho-Perula, M. Munoz, C. Chavoix, and R. Insausti
The Parahippocampal Gyrus in the Baboon: Anatomical, Cytoarchitectonic and Magnetic Resonance Imaging (MRI) Studies
Cereb Cortex,
March 1, 2004;
14(3):
231 - 246.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. G. Coleshill, C. D. Binnie, R. G. Morris, G. Alarcon, W. van Emde Boas, D. N. Velis, A. Simmons, C. E. Polkey, C. W. M. van Veelen, and P. C. van Rijen
Material-Specific Recognition Memory Deficits Elicited by Unilateral Hippocampal Electrical Stimulation
J. Neurosci.,
February 18, 2004;
24(7):
1612 - 1616.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. DESTEXHE and T. J. SEJNOWSKI
Interactions Between Membrane Conductances Underlying Thalamocortical Slow-Wave Oscillations
Physiol Rev,
October 1, 2003;
83(4):
1401 - 1453.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Davachi, J. P. Mitchell, and A. D. Wagner
Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories
PNAS,
February 18, 2003;
100(4):
2157 - 2162.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X. Blaizot, K. Meguro, I. Millien, J. C. Baron, and C. Chavoix
Correlations between Visual Recognition Memory and Neocortical and Hippocampal Glucose Metabolism after Bilateral Rhinal Cortex Lesions in the Baboon: Implications for Alzheimer's Disease
J. Neurosci.,
November 1, 2002;
22(21):
9166 - 9170.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. J. Curtis, L. L. Lindeke, M. K. Georgieff, and C. A. Nelson
Neurobehavioural functioning in neonatal intensive care unit graduates in late childhood and early adolescence
Brain,
July 1, 2002;
125(7):
1646 - 1659.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. A. Hollup, K. G. Kjelstrup, J. Hoff, M.-B. Moser, and E. I. Moser
Impaired Recognition of the Goal Location during Spatial Navigation in Rats with Hippocampal Lesions
J. Neurosci.,
June 15, 2001;
21(12):
4505 - 4513.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. P. Wiebe and U. V. Staubli
Recognition Memory Correlates of Hippocampal Theta Cells
J. Neurosci.,
June 1, 2001;
21(11):
3955 - 3967.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Alvarez, P. A. Lipton, R. Melrose, and H. Eichenbaum
Differential Effects of Damage within the Hippocampal Region on Memory for a Natural, Nonspatial Odor-Odor Association
Learn. Mem.,
March 1, 2001;
8(2):
79 - 86.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
R. E. Clark, S. M. Zola, and L. R. Squire
Impaired Recognition Memory in Rats after Damage to the Hippocampus
J. Neurosci.,
December 1, 2000;
20(23):
8853 - 8860.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. C. Alvarado and J. Bachevalier
Revisiting the Maturation of Medial Temporal Lobe Memory Functions in Primates
Learn. Mem.,
September 1, 2000;
7(5):
244 - 256.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
E. Sybirska, L. Davachi, and P. S. Goldman-Rakic
Prominence of Direct Entorhinal-CA1 Pathway Activation in Sensorimotor and Cognitive Tasks Revealed by 2-DG Functional Mapping in Nonhuman Primate
J. Neurosci.,
August 1, 2000;
20(15):
5827 - 5834.
[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]
|
 |
|

|
 |

|
 |
 
P. A. Dudchenko, E. R. Wood, and H. Eichenbaum
Neurotoxic Hippocampal Lesions Have No Effect on Odor Span and Little Effect on Odor Recognition Memory But Produce Significant Impairments on Spatial Span, Recognition, and Alternation
J. Neurosci.,
April 15, 2000;
20(8):
2964 - 2977.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. M. Zola, L. R. Squire, E. Teng, L. Stefanacci, E. A. Buffalo, and R. E. Clark
Impaired Recognition Memory in Monkeys after Damage Limited to the Hippocampal Region
J. Neurosci.,
January 1, 2000;
20(1):
451 - 463.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. P. Wiebe and U. V. Staubli
Dynamic Filtering of Recognition Memory Codes in the Hippocampus
J. Neurosci.,
December 1, 1999;
19(23):
10562 - 10574.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Elliott and R. J. Dolan
Differential Neural Responses during Performance of Matching and Nonmatching to Sample Tasks at Two Delay Intervals
J. Neurosci.,
June 15, 1999;
19(12):
5066 - 5073.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. E. Hampson, L. E. Jarrard, and S. A. Deadwyler
Effects of Ibotenate Hippocampal and Extrahippocampal Destruction on Delayed-Match and -Nonmatch-to-Sample Behavior in Rats
J. Neurosci.,
February 15, 1999;
19(4):
1492 - 1507.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Wan, J. P. Aggleton, and M. W. Brown
Different Contributions of the Hippocampus and Perirhinal Cortex to Recognition Memory
J. Neurosci.,
February 1, 1999;
19(3):
1142 - 1148.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Nunn, F. J. X. Graydon, C. E. Polkey, and R. G. Morris
Differential spatial memory impairment after right temporal lobectomy demonstrated using temporal titration
Brain,
January 1, 1999;
122(1):
47 - 59.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K Juottonen, M Lehtovirta, S Helisalmi, P J R. Sr, and H Soininen
Major decrease in the volume of the entorhinal cortex in patients with Alzheimer's disease carrying the apolipoprotein E epsilon 4 allele
J. Neurol. Neurosurg. Psychiatry,
September 1, 1998;
65(3):
322 - 327.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
E. A. Murray and M. Mishkin
Object Recognition and Location Memory in Monkeys with Excitotoxic Lesions of the Amygdala and Hippocampus
J. Neurosci.,
August 15, 1998;
18(16):
6568 - 6582.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. B. Mulder, M. G. Hodenpijl, and F. H. Lopes da Silva
Electrophysiology of the Hippocampal and Amygdaloid Projections to the Nucleus Accumbens of the Rat: Convergence, Segregation, and Interaction of Inputs
J. Neurosci.,
July 1, 1998;
18(13):
5095 - 5102.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Mori, Y. Yoneda, H. Yamashita, N. Hirono, M. Ikeda, and A. Yamadori
Medial temporal structures relate to memory impairment in Alzheimer's disease: an MRI volumetric study
J. Neurol. Neurosurg. Psychiatry,
August 1, 1997;
63(2):
214 - 221.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Corkin, D. G. Amaral, R. G. Gonzalez, K. A. Johnson, and B. T. Hyman
H. M.'s Medial Temporal Lobe Lesion: Findings from Magnetic Resonance Imaging
J. Neurosci.,
May 15, 1997;
17(10):
3964 - 3979.
[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]
|
 |
|

|
 |

|
 |
 
A. H. Gazzaley, N. G. Weiland, B. S. McEwen, and J. H. Morrison
Differential Regulation of NMDAR1 mRNA and Protein by Estradiol in the Rat Hippocampus
J. Neurosci.,
November 1, 1996;
16(21):
6830 - 6838.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. R. Moyer Jr., L. T. Thompson, and J. F. Disterhoft
Trace Eyeblink Conditioning Increases CA1 Excitability in a Transient and Learning-Specific Manner
J. Neurosci.,
September 1, 1996;
16(17):
5536 - 5546.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. L. Rempel-Clower, S. M. Zola, L. R. Squire, and D. G. Amaral
Three Cases of Enduring Memory Impairment after Bilateral Damage Limited to the Hippocampal Formation
J. Neurosci.,
August 15, 1996;
16(16):
5233 - 5255.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L.R. Squire and S.M. Zola
Memory, Memory Impairment, and the Medial Temporal Lobe
Cold Spring Harb Symp Quant Biol,
January 1, 1996;
61(0):
185 - 195.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
O Jensen and J E Lisman
Theta/gamma networks with slow NMDA channels learn sequences and encode episodic memory: role of NMDA channels in recall.
Learn. Mem.,
January 1, 1996;
3(2-3):
264 - 278.
[Abstract]
[PDF]
|
 |
|
|