 |
Previous Article
Journal of Neuroscience, Vol 13, 4549-4561, Copyright © 1993 by Society for Neuroscience
Neural substrates of visual stimulus-stimulus association in rhesus monkeys
EA Murray, D Gaffan and M Mishkin
Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Maryland 20892.
Rhesus monkeys learned 10 visual stimulus-stimulus association, or paired
associates. They then received bilateral removals of either the amygdaloid
complex and underlying cortex, the hippocampal formation and underlying
cortex, or both combined, or they were retained as unoperated controls.
After surgery or rest, the monkeys were tested for their retention of the
preoperatively learned set of paired associates, as well as for their
ability to learn new associations of the same type. Both unoperated
controls and hippocampectomized monkeys relearned the preoperatively
trained set of paired associates almost immediately. By contrast, monkeys
with amygdala removals were moderately retarded in relearning, and monkeys
with combined amygdala and hippocampal ablations were severely retarded.
When confronted with new sets of visual stimuli, monkeys with amygdala
removals or hippocampal removals learned new sets of paired associates at
the same rate as the controls, whereas monkeys with the combined ablation
were again profoundly retarded. Only one monkey with the combined lesion
was able to learn new stimulus-stimulus associations to criterion, and then
only after extensive training, despite the ability of all three animals in
this group to perform delayed matching-to-sample with the same stimuli and
the same intraatrial delays as those used in the paired associate task. At
the end of the main experiment, two of the unoperated controls received
bilateral ablations of the rhinal cortex. These monkeys showed the same
level of difficulty in learning new paired associates as the animals in the
main experiment that had received the combined amygdala plus hippocampal
ablations. The results implicate the medial temporal lobe, and particularly
the rhinal cortex, in the formation of stimulus- stimulus associative
memories.
This article has been cited by other articles:

|
 |

|
 |
 
G. K. Murray, F. Cheng, L. Clark, J. H. Barnett, A. D. Blackwell, P. C. Fletcher, T. W. Robbins, E. T. Bullmore, and P. B. Jones
Reinforcement and Reversal Learning in First-Episode Psychosis
Schizophr Bull,
September 1, 2008;
34(5):
848 - 855.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Liu, R. P. Heitz, A. R. Sampson, W. Zhang, and C. W. Bradberry
Evidence of Temporal Cortical Dysfunction in Rhesus Monkeys following Chronic Cocaine Self-Administration
Cereb Cortex,
September 1, 2008;
18(9):
2109 - 2116.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Cadoret and M. Petrides
Ventrolateral Prefrontal Neuronal Activity Related to Active Controlled Memory Retrieval in Nonhuman Primates
Cereb Cortex,
September 1, 2007;
17(suppl_1):
i27 - i40.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. R. I. Barker, F. Bird, V. Alexander, and E. C. Warburton
Recognition Memory for Objects, Place, and Temporal Order: A Disconnection Analysis of the Role of the Medial Prefrontal Cortex and Perirhinal Cortex
J. Neurosci.,
March 14, 2007;
27(11):
2948 - 2957.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. M. Saksida, T. J. Bussey, C. A. Buckmaster, and E. A. Murray
Impairment and Facilitation of Transverse Patterning after Lesions of the Perirhinal Cortex and Hippocampus, Respectively
Cereb Cortex,
January 1, 2007;
17(1):
108 - 115.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. R. Squire
Lost forever or temporarily misplaced? The long debate about the nature of memory impairment.
Learn. Mem.,
September 1, 2006;
13(5):
522 - 529.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. C. Alvarado and J. Bachevalier
Comparison of the Effects of Damage to the Perirhinal and Parahippocampal Cortex on Transverse Patterning and Location Memory in Rhesus Macaques
J. Neurosci.,
February 9, 2005;
25(6):
1599 - 1609.
[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]
|
 |
|

|
 |

|
 |
 
Z. Liu, B. J. Richmond, E. A. Murray, R. C. Saunders, S. Steenrod, B. K. Stubblefield, D. M. Montague, and E. I. Ginns
DNA targeting of rhinal cortex D2 receptor protein reversibly blocks learning of cues that predict reward
PNAS,
August 17, 2004;
101(33):
12336 - 12341.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. J. Kennedy and M. L. Shapiro
Retrieving Memories via Internal Context Requires the Hippocampus
J. Neurosci.,
August 4, 2004;
24(31):
6979 - 6985.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. E. Gilbert and R. P. Kesner
Recognition Memory for Complex Visual Discriminations Is Influenced by Stimulus Interference in Rodents With Perirhinal Cortex Damage
Learn. Mem.,
November 1, 2003;
10(6):
525 - 530.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. J. Brasted, T. J. Bussey, E. A. Murray, and S. P. Wise
Role of the hippocampal system in associative learning beyond the spatial domain
Brain,
May 1, 2003;
126(5):
1202 - 1223.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Naya, M. Yoshida, and Y. Miyashita
Forward Processing of Long-Term Associative Memory in Monkey Inferotemporal Cortex
J. Neurosci.,
April 1, 2003;
23(7):
2861 - 2871.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Yoshida, Y. Naya, and Y. Miyashita
Anatomical organization of forward fiber projections from area TE to perirhinal neurons representing visual long-term memory in monkeys
PNAS,
April 1, 2003;
100(7):
4257 - 4262.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Orlov, V. Yakovlev, D. Amit, S. Hochstein, and E. Zohary
Serial Memory Strategies in Macaque Monkeys: Behavioral and Theoretical Aspects
Cereb Cortex,
March 1, 2002;
12(3):
306 - 317.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. J. Brasted, T. J. Bussey, E. A. Murray, and S. P. Wise
Fornix Transection Impairs Conditional Visuomotor Learning in Tasks Involving Nonspatially Differentiated Responses
J Neurophysiol,
January 1, 2002;
87(1):
631 - 633.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Messinger, L. R. Squire, S. M. Zola, and T. D. Albright
Neuronal representations of stimulus associations develop in the temporal lobe during learning
PNAS,
September 19, 2001;
(2001)
211431098.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Davachi and P. S. Goldman-Rakic
Primate Rhinal Cortex Participates in Both Visual Recognition and Working Memory Tasks: Functional Mapping With 2-DG
J Neurophysiol,
June 1, 2001;
85(6):
2590 - 2601.
[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]
|
 |
|

|
 |

|
 |
 
Y. Naya, M. Yoshida, and Y. Miyashita
Backward Spreading of Memory-Retrieval Signal in the Primate Temporal Cortex
Science,
January 26, 2001;
291(5504):
661 - 664.
[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]
|
 |
|

|
 |

|
 |
 
Z. Liu and B. J. Richmond
Response Differences in Monkey TE and Perirhinal Cortex: Stimulus Association Related to Reward Schedules
J Neurophysiol,
March 1, 2000;
83(3):
1677 - 1692.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. A. Erickson and R. Desimone
Responses of Macaque Perirhinal Neurons during and after Visual Stimulus Association Learning
J. Neurosci.,
December 1, 1999;
19(23):
10404 - 10416.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. J. Moore and C. J. Price
A functional neuroimaging study of the variables that generate category-specific object processing differences
Brain,
May 1, 1999;
122(5):
943 - 962.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. J. Hock Jr. and M. D. Bunsey
Differential Effects of Dorsal and Ventral Hippocampal Lesions
J. Neurosci.,
September 1, 1998;
18(17):
7027 - 7032.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Hasegawa, T. Fukushima, T. Ihara, and Y. Miyashita
Callosal Window Between Prefrontal Cortices: Cognitive Interaction to Retrieve Long-Term Memory
Science,
August 7, 1998;
281(5378):
814 - 818.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
T. Grunwald, K. Lehnertz, H. J. Heinze, C. Helmstaedter, and C. E. Elger
Verbal novelty detection within the human hippocampus proper
PNAS,
March 17, 1998;
95(6):
3193 - 3197.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. C. Honey, A. Watt, and M. Good
Hippocampal Lesions Disrupt an Associative Mismatch Process
J. Neurosci.,
March 15, 1998;
18(6):
2226 - 2230.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J. Buckley and D. Gaffan
Perirhinal Cortex Ablation Impairs Visual Object Identification
J. Neurosci.,
March 15, 1998;
18(6):
2268 - 2275.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Thornton, L. A. Rothblat, and E. A. Murray
Rhinal Cortex Removal Produces Amnesia for Preoperatively Learned Discrimination Problems But Fails to Disrupt Postoperative Acquisition and Retention in Rhesus Monkeys
J. Neurosci.,
November 1, 1997;
17(21):
8536 - 8549.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Malkova, D. Gaffan, and E. A. Murray
Excitotoxic Lesions of the Amygdala Fail to Produce Impairment in Visual Learning for Auditory Secondary Reinforcement But Interfere with Reinforcer Devaluation Effects in Rhesus Monkeys
J. Neurosci.,
August 1, 1997;
17(15):
6011 - 6020.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Vargha-Khadem, D. G. Gadian, K. E. Watkins, A. Connelly, W. Van Paesschen, and M. Mishkin
Differential Effects of Early Hippocampal Pathology on Episodic and Semantic Memory
Science,
July 18, 1997;
277(5324):
376 - 380.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
M. J. Buckley, D. Gaffan, and E. A. Murray
Functional Double Dissociation Between Two Inferior Temporal Cortical Areas: Perirhinal Cortex Versus Middle Temporal Gyrus
J Neurophysiol,
February 1, 1997;
77(2):
587 - 598.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Eichenbaum, G. Schoenbaum, B. Young, and M. Bunsey
Functional organization of the hippocampal memory system
PNAS,
November 26, 1996;
93(24):
13500 - 13507.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Oyoshi, H. Nishijo, T. Asakura, Y. Takamura, and T. Ono
Emotional and Behavioral Correlates of Mediodorsal Thalamic Neurons during Associative Learning in Rats
J. Neurosci.,
September 15, 1996;
16(18):
5812 - 5829.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K Sakai, Y Naya, and Y Miyashita
Neuronal tuning and associative mechanisms in form representation.
Learn. Mem.,
January 1, 1994;
1(2):
83 - 105.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Messinger, L. R. Squire, S. M. Zola, and T. D. Albright
Neuronal representations of stimulus associations develop in the temporal lobe during learning
PNAS,
October 9, 2001;
98(21):
12239 - 12244.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|