Multiple Routes to Memory: Distinct Medial Temporal Lobe Processes Build Item and Source Memories

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2003 Feb 13

PMID 12578977

Citations 347

Authors

Lila Davachi

Jason P Mitchell

Anthony D Wagner

Affiliations

Soon will be listed here.

Abstract

A central function of memory is to permit an organism to distinguish between stimuli that have been previously encountered and those that are novel. Although the medial temporal lobe (which includes the hippocampus and surrounding perirhinal, parahippocampal, and entorhinal cortices) is known to be crucial for recognition memory, controversy remains regarding how the specific subregions within the medial temporal lobe contribute to recognition. We used event-related functional MRI to examine the relation between activation in distinct medial temporal lobe subregions during memory formation and the ability (i) to later recognize an item as previously encountered (item recognition) and (ii) to later recollect specific contextual details about the prior encounter (source recollection). Encoding activation in hippocampus and in posterior parahippocampal cortex predicted later source recollection, but was uncorrelated with item recognition. In contrast, encoding activation in perirhinal cortex predicted later item recognition, but not subsequent source recollection. These outcomes suggest that the subregions within the medial temporal lobe subserve distinct, but complementary, learning mechanisms.

Citing Articles

Lack of context modulation in human single neuron responses in the medial temporal lobe.

Rey H, Panagiotaropoulos T, Gutierrez L, Chaure F, Nasimbera A, Cordisco S Cell Rep. 2025; 44(1):115218.

PMID: 39823228 PMC: 11781864. DOI: 10.1016/j.celrep.2024.115218.

Repetition dynamically and rapidly increases cortical, but not hippocampal, offline reactivation.

Yu W, Zadbood A, Chanales A, Davachi L Proc Natl Acad Sci U S A. 2024; 121(40):e2405929121.

PMID: 39316058 PMC: 11459139. DOI: 10.1073/pnas.2405929121.

A short natural history of mental time travels: a journey still travelled?.

Osvath M, Johansson M Philos Trans R Soc Lond B Biol Sci. 2024; 379(1913):20230402.

PMID: 39278257 PMC: 11496716. DOI: 10.1098/rstb.2023.0402.

Neuroimaging of autobiographical memory in dementia with Lewy bodies: a story of insula.

Tisserand A, Blanc F, Muller C, Durand H, Demuynck C, Ravier A Brain Commun. 2024; 6(4):fcae272.

PMID: 39210911 PMC: 11358644. DOI: 10.1093/braincomms/fcae272.

Correlates of Theta and Gamma Activity during Visuospatial Incidental/Intentional Encoding and Retrieval Indicate Differences in Processing in Young and Elderly Healthy Participants.

Junco-Munoz M, Mejia-Rodriguez O, Cervantes-Alfaro J, Tellez-Anguiano A, Lopez-Vazquez M, Olvera-Cortes M Brain Sci. 2024; 14(8).

PMID: 39199479 PMC: 11352628. DOI: 10.3390/brainsci14080786.

References

Meunier M, Hadfield W, Bachevalier J, Murray E . Effects of rhinal cortex lesions combined with hippocampectomy on visual recognition memory in rhesus monkeys. J Neurophysiol. 1996; 75(3):1190-205. DOI: 10.1152/jn.1996.75.3.1190. View

Henson R, Rugg M, Shallice T, Josephs O, Dolan R . Recollection and familiarity in recognition memory: an event-related functional magnetic resonance imaging study. J Neurosci. 1999; 19(10):3962-72. PMC: 6782715. View

Buffalo E, Reber P, Squire L . The human perirhinal cortex and recognition memory. Hippocampus. 1998; 8(4):330-9. DOI: 10.1002/(SICI)1098-1063(1998)8:4<330::AID-HIPO3>3.0.CO;2-L. View

OCraven K, Kanwisher N . Mental imagery of faces and places activates corresponding stiimulus-specific brain regions. J Cogn Neurosci. 2001; 12(6):1013-23. DOI: 10.1162/08989290051137549. View

Squire L . Memory systems. C R Acad Sci III. 1998; 321(2-3):153-6. DOI: 10.1016/s0764-4469(97)89814-9. View

Fiez J . Phonology, semantics, and the role of the left inferior prefrontal cortex. Hum Brain Mapp. 1997; 5(2):79-83. View

Zola S, Squire L . Relationship between magnitude of damage to the hippocampus and impaired recognition memory in monkeys. Hippocampus. 2001; 11(2):92-8. DOI: 10.1002/hipo.1027. View

Strange B, Otten L, Josephs O, Rugg M, Dolan R . Dissociable human perirhinal, hippocampal, and parahippocampal roles during verbal encoding. J Neurosci. 2002; 22(2):523-8. PMC: 6758661. View

Squire L . Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev. 1992; 99(2):195-231. DOI: 10.1037/0033-295x.99.2.195. View

10.

OReilly R, Rudy J . Conjunctive representations in learning and memory: principles of cortical and hippocampal function. Psychol Rev. 2001; 108(2):311-45. DOI: 10.1037/0033-295x.108.2.311. View

11.

Ricci P, Zelkowicz B, Nebes R, Meltzer C, Mintun M, Becker J . Functional neuroanatomy of semantic memory: recognition of semantic associations. Neuroimage. 1999; 9(1):88-96. DOI: 10.1006/nimg.1998.0386. View

12.

Hopkins R, Kesner R, Goldstein M . Item and order recognition memory in subjects with hypoxic brain injury. Brain Cogn. 1995; 27(2):180-201. DOI: 10.1006/brcg.1995.1016. View

13.

Friedman D, Trott C . An event-related potential study of encoding in young and older adults. Neuropsychologia. 2000; 38(5):542-57. DOI: 10.1016/s0028-3932(99)00122-0. View

14.

Schacter D, Wagner A . Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval. Hippocampus. 1999; 9(1):7-24. DOI: 10.1002/(SICI)1098-1063(1999)9:1<7::AID-HIPO2>3.0.CO;2-K. View

15.

OReilly R, Rudy J . Computational principles of learning in the neocortex and hippocampus. Hippocampus. 2000; 10(4):389-97. DOI: 10.1002/1098-1063(2000)10:4<389::AID-HIPO5>3.0.CO;2-P. View

16.

Petersen S, Fox P, Posner M, Mintun M, Raichle M . Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature. 1988; 331(6157):585-9. DOI: 10.1038/331585a0. View

17.

Poldrack R, Wagner A, Prull M, Desmond J, Glover G, Gabrieli J . Functional specialization for semantic and phonological processing in the left inferior prefrontal cortex. Neuroimage. 1999; 10(1):15-35. DOI: 10.1006/nimg.1999.0441. View

18.

Paller K, Wagner A . Observing the transformation of experience into memory. Trends Cogn Sci. 2005; 6(2):93-102. DOI: 10.1016/s1364-6613(00)01845-3. View

19.

Brown M, Aggleton J . Recognition memory: what are the roles of the perirhinal cortex and hippocampus?. Nat Rev Neurosci. 2001; 2(1):51-61. DOI: 10.1038/35049064. View

20.

Suzuki W, Amaral D . Cortical inputs to the CA1 field of the monkey hippocampus originate from the perirhinal and parahippocampal cortex but not from area TE. Neurosci Lett. 1990; 115(1):43-8. DOI: 10.1016/0304-3940(90)90515-b. View