Contrasting effects on discrimination learning after hippocampal lesions and conjoint hippocampal-caudate lesions in monkeys

Journal of Neuroscience

Volumn 20, Issue 10, 2000, Pages 3853-3863

  Teng, Edmond ^c   Stefanacci, Lisa ^b   Squire, Larry R ^a,b,c,d   Zola, Stuart M ^a,b,c  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Caudate nucleus; Discrimination learning; Hippocampus; Ibotenic acid lesions; Ischemic lesions; Monkeys; Radio frequency lesions

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; DISCRIMINATION LEARNING; HIPPOCAMPUS; MALE; MEMORY; MONKEY; NERVE TRACT; NONHUMAN; PRIORITY JOURNAL; TEMPORAL LOBE;

EID: 0034657171     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-10-03853.2000     Document Type: Article

References (46)

1. Alvarez P, Zola-Morgan S, Squire LR (1995) Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys. J Neurosci 15:3796-3807.
2. Baxter MG, Hadfield WS, Murray EA (1999) Rhinal cortex lesions produce mild deficits in visual discrimination learning for an auditory secondary reinforcer in rhesus monkeys. Behav Neurosci 113:243-252.
3. Buffalo EA, Stefanacci L, Squire LR, Zola SM (1998) A reexamination of the concurrent discrimination learning task: the importance of inferotemporal cortex, area TE. Behav Neurosci 112:3-14.
4. Buffalo EA, Ramus SJ, Clark RE, Teng E, Squire LR, Zola SM (1999) Dissociation between the effects of damage to perirhinal cortex and Area TE. Learn Mem 6:572-599.
5. Dean P (1976) Effects of inferotemporal lesions on the behavior of monkeys. Psychol Bull 83:41-71.
6. Divac I, Rosvold HE, Szwarcbart MK (1967) Behavioral effects of selective ablation of the caudate nucleus. J Comp Physiol Psychol 63:184-190.
7. Doré FY, Thornton JA, White NM, Murray EA (1998) Selective hippocampal lesions yield nonspatial memory impairment in rhesus monkeys. Hippocampus 8:323-329.
8. Gaffan D (1994) Dissociated effects of perirhinal cortex ablation, fornix transection and amygdalectomy: evidence for multiple memory systems in the primate temporal lobe. Exp Brain Res 99:411-422.
9. Gellerman LW (1933) Chance orders of alternating stimuli in visual discrimination experiments. J Genet Psychol 42:207-208.
10. Graybiel AM (1995) Building action repertoires: memory and learning functions of the basal ganglia. Curr Opin Neurobiol 5:733-741.
11. Gross CG (1973) Visual functions of inferotemporal cortex. In: Handbook of sensory physiology (Autrum H, Jung R, Lowenstein WR, McKay DM, Teuber HL, eds), pp 451-482. Berlin: Springer.
12. Iversen SD (1976) Do hippocampal lesions produce amnesia in animals? Int Rev Neurobiol 19:1-49.
13. Jones B, Mishkin M (1972) Limbic lesions and the problem of stimulus-reinforcement associations. Exp Neurol 36:362-377.
14. Knowlton BJ, Mangels JA, Squire LR (1996) A neostriatal habit learning system in humans. Science 273:1399-1402.
15. Mahut H, Moss M, Zola-Morgan S (1981) Retention deficits after combined amygdalo-hippocampal and selective hippocampal resections in the monkey. Neuropsychologia 19:201-225.
16. Mishkin M, Murray EA (1994) Stimulus recognition. Curr Opin Neurobiol 4:200-206.
17. Mishkin M, Petri HL (1984) Memories and habits: some implications for the analysis of learning and retention. In: Neuropsychology of memory (Squire LR, Butters N, eds), pp 287-296. New York: Guilford.
18. Mishkin M, Malamut B, Bachevalier J (1984) Memories and habits: two neural systems. In: Neurobiology of human learning and memory (Lynch G, McGaugh JL, Weinberger NM, eds), pp 65-77. New York: Guilford.
19. Mishkin M, Suzuki WA, Gadian DG, Vargha-Khadem F (1999) Hierarchical organization of cognitive memory. Phil Trans R Soc Lond B Biol Sci 352:1461-1467.
20. Moss M, Mahut H, Zola-Morgan S (1981) Concurrent discrimination learning of monkeys after hippocampal, entorhinal, or fornix lesions. J Neurosci 1:227-240.
21. Murray EA, Baxter MG, Gaffan D (1998) Monkeys with rhinal cortex damage or neurotoxic hippocampal lesions are impaired on spatial scene learning and object reversals. Behav Neurosci 112:1291-1303.
22. Orbach J, Milner B, Rasmussen T (1960) Learning and retention in monkeys after amygdala-hippocampus resection. Arch Neurol 3:230-251.
23. Packard MG, McGaugh JL (1992) Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems. Behav Neurosci 106:439-446.
24. Packard MG, Hirsh R, White NM (1989) Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems. J Neurosci 9:1465-1472.
25. Phillips AG, Carr GD (1987) Cognition and the basal ganglia: a possible substrate for procedural knowledge. Can J Neurol Sci 14:381-385.
26. Phillips RR, Malamut BL, Bachevalier J, Mishkin M (1988) Dissociation of the effects of inferior temporal and limbic lesions on object discrimination learning with 24-h intertrial intervals. Behav Brain Res 27:99-107.
27. Rempel-Clower N, Zola SM, Squire LR (1996) Three cases of enduring memory impairment following bilateral damage limited to the hippocampal formation. J Neurosci 16:5233-5255.
28. Salmon DP, Butters N (1995) Neurobiology of skill and habit learning. Curr Opin Neurobiol 5:184-190.
29. Squire LR, Zola-Morgan S (1983) The neurology of memory: the case for correspondence between the findings for human and nonhuman primate. In: The physiological basis of memory (Deutsch JA, ed), pp 199-268. New York: Academic.
30. Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253:1380-1386.
31. Squire LR, Zola-Morgan S, Chen K (1988) Human amnesia and animal models of amnesia: performance of amnesic patients on tests designed for the monkey. Behav Neurosci 11:210-221.
32. Suzuki WA, Zola-Morgan S, Squire LR, Amaral DG (1993) Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. J Neurosci 13:2430-2451.
33. Szabo J, Cowan WM (1984) A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis). J Comp Neurol 222:265-300.
34. Wang J, Aigner T, Mishkin M (1990) Effects of neostriatal lesions on visual habit formation in rhesus monkeys. Soc Neurosci Abstr 16:617.
35. Wise SP, Murray EA (1999) Role of the hippocampal system in conditional motor learning: Mapping antecedents to action. Hippocampus 9:101-117.
36. Zola S, Squire LR (2000) Memory and brain systems. In: Oxford handbook of memory (Tulving E, Craik F, eds). Oxford: Oxford UP.
37. Zola SM, Squire LR, Teng E, Stefanacci L, Buffalo E, Clark RE (2000) Impaired recognition memory in monkeys after damage limited to the hippocampal region. J Neurosci 20:451-463.
38. Zola-Morgan S, Squire LR (1984) Preserved learning in monkeys with medial temporal lesions: sparing of motor and cognitive skills. J Neurosci 4:1072-1085.
39. Zola-Morgan S, Squire LR (1985) Medial temporal lesions in monkeys impair memory on a variety of tasks sensitive to human amnesia. Behav Neurosci 99:22-34.
40. Zola-Morgan S, Squire LR, Amaral DG (1986) Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6:2950-2967.
41. Zola-Morgan S, Squire LR, Amaral DG (1989a) Lesions of the hippocampal formation but not lesions of the fornix or the mammillary nuclei produce long-lasting memory impairment in monkeys. J Neurosci 9:898-913.
42. Zola-Morgan S, Squire LR, Amaral DG (1989b) Lesions of the amygdala that spare adjacent cortical regions do not impair memory or exacerbate the impairment following lesions of the hippocampal formation. J Neurosci 9:1922-1936.
43. Zola-Morgan S, Squire LR, Amaral DG, Suzuki WA (1989c) Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. J Neurosci 9:4355-4370.
44. Zola-Morgan S, Squire LR, Rempel NL, Clower RP, Amaral DG (1992) Enduring memory impairment in monkeys after ischemic damage to the hippocampus. J Neurosci 9:4355-4370.
45. Zola-Morgan S, Squire LR, Clower RP, Rempel NL (1993) Damage to the perirhinal cortex exacerbates memory impairment following lesions to the hippocampal formation. J Neurosci 13:251-265.
46. Zola-Morgan S, Squire LR, Ramus SJ (1994) Severity of memory impairment in monkeys as a function of locus and extent of damage within the medial temporal lobe memory system. Hippocampus 4:483-495.