Experience-dependent Hippocampal Pattern Differentiation Prevents Interference During Subsequent Learning

Overview

Journal Nat Commun

Specialty Biology

Date 2016 Dec 8

PMID 27925613

Citations 74

Authors

Serra E Favila

Avi J H Chanales

Brice A Kuhl

Affiliations

Soon will be listed here.

Abstract

The hippocampus is believed to reduce memory interference by disambiguating neural representations of similar events. However, there is limited empirical evidence linking representational overlap in the hippocampus to memory interference. Likewise, it is not fully understood how learning influences overlap among hippocampal representations. Using pattern-based fMRI analyses, we tested for a bidirectional relationship between memory overlap in the human hippocampus and learning. First, we show that learning drives hippocampal representations of similar events apart from one another. These changes are not explained by task demands to discriminate similar stimuli and are fully absent in visual cortical areas that feed into the hippocampus. Second, we show that lower representational overlap in the hippocampus benefits subsequent learning by preventing interference between similar memories. These findings reveal targeted experience-dependent changes in hippocampal representations of similar events and provide a critical link between memory overlap in the hippocampus and behavioural expressions of memory interference.

Citing Articles

Integration of Euclidean and path distances in hippocampal maps.

Ottink L, de Haas N, Doeller C Sci Rep. 2025; 15(1):7104.

PMID: 40016304 PMC: 11868619. DOI: 10.1038/s41598-025-90504-3.

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.

Segregation-to-integration transformation model of memory evolution.

Bavassi L, Fuentemilla L Netw Neurosci. 2024; 8(4):1529-1544.

PMID: 39735504 PMC: 11675164. DOI: 10.1162/netn_a_00415.

Object Feature Memory Is Distorted by Category Structure.

Tandoc M, Dong C, Schapiro A Open Mind (Camb). 2024; 8:1348-1368.

PMID: 39654820 PMC: 11627532. DOI: 10.1162/opmi_a_00170.

The role of REM sleep in neural differentiation of memories in the hippocampus.

McDevitt E, Kim G, Turk-Browne N, Norman K bioRxiv. 2024; .

PMID: 39553942 PMC: 11566016. DOI: 10.1101/2024.11.01.621588.

References

Lewis-Peacock J, Norman K . Competition between items in working memory leads to forgetting. Nat Commun. 2014; 5:5768. PMC: 4284654. DOI: 10.1038/ncomms6768. View

McHugh T, Jones M, Quinn J, Balthasar N, Coppari R, Elmquist J . Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science. 2007; 317(5834):94-9. DOI: 10.1126/science.1140263. View

Markus E, Qin Y, Leonard B, Skaggs W, McNaughton B, Barnes C . Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci. 1995; 15(11):7079-94. PMC: 6578055. View

Kriegeskorte N, Kievit R . Representational geometry: integrating cognition, computation, and the brain. Trends Cogn Sci. 2013; 17(8):401-12. PMC: 3730178. DOI: 10.1016/j.tics.2013.06.007. View

Sahay A, Scobie K, Hill A, OCarroll C, Kheirbek M, Burghardt N . Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature. 2011; 472(7344):466-70. PMC: 3084370. DOI: 10.1038/nature09817. View

Stigliani A, Weiner K, Grill-Spector K . Temporal Processing Capacity in High-Level Visual Cortex Is Domain Specific. J Neurosci. 2015; 35(36):12412-24. PMC: 4563034. DOI: 10.1523/JNEUROSCI.4822-14.2015. View

Smith S, Jenkinson M, Woolrich M, Beckmann C, Behrens T, Johansen-Berg H . Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 2004; 23 Suppl 1:S208-19. DOI: 10.1016/j.neuroimage.2004.07.051. View

Quirk G, Muller R, Kubie J . The firing of hippocampal place cells in the dark depends on the rat's recent experience. J Neurosci. 1990; 10(6):2008-17. PMC: 6570323. View

Chapuis J, Wilson D . Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity. Nat Neurosci. 2011; 15(1):155-61. PMC: 3245808. DOI: 10.1038/nn.2966. View

10.

OReilly R, McClelland J . Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus. 1994; 4(6):661-82. DOI: 10.1002/hipo.450040605. View

11.

deBettencourt M, Cohen J, Lee R, Norman K, Turk-Browne N . Closed-loop training of attention with real-time brain imaging. Nat Neurosci. 2015; 18(3):470-5. PMC: 4503600. DOI: 10.1038/nn.3940. View

12.

Schapiro A, Kustner L, Turk-Browne N . Shaping of object representations in the human medial temporal lobe based on temporal regularities. Curr Biol. 2012; 22(17):1622-7. PMC: 3443305. DOI: 10.1016/j.cub.2012.06.056. View

13.

Poppenk J, Norman K . Briefly cuing memories leads to suppression of their neural representations. J Neurosci. 2014; 34(23):8010-20. PMC: 4044257. DOI: 10.1523/JNEUROSCI.4584-13.2014. View

14.

Hsieh L, Gruber M, Jenkins L, Ranganath C . Hippocampal activity patterns carry information about objects in temporal context. Neuron. 2014; 81(5):1165-1178. PMC: 3984944. DOI: 10.1016/j.neuron.2014.01.015. View

15.

LaRocque K, Smith M, Carr V, Witthoft N, Grill-Spector K, Wagner A . Global similarity and pattern separation in the human medial temporal lobe predict subsequent memory. J Neurosci. 2013; 33(13):5466-74. PMC: 3643502. DOI: 10.1523/JNEUROSCI.4293-12.2013. View

16.

Moss M, Mahut H . Concurrent discrimination learning of monkeys after hippocampal, entorhinal, or fornix lesions. J Neurosci. 1981; 1(3):227-40. PMC: 6564115. View

17.

Norman K, OReilly R . Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. Psychol Rev. 2003; 110(4):611-46. DOI: 10.1037/0033-295X.110.4.611. View

18.

Hulbert J, Norman K . Neural Differentiation Tracks Improved Recall of Competing Memories Following Interleaved Study and Retrieval Practice. Cereb Cortex. 2014; 25(10):3994-4008. PMC: 4585527. DOI: 10.1093/cercor/bhu284. View

19.

Clelland C, Choi M, Romberg C, Clemenson Jr G, Fragniere A, Tyers P . A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science. 2009; 325(5937):210-3. PMC: 2997634. DOI: 10.1126/science.1173215. View

20.

Wimber M, Alink A, Charest I, Kriegeskorte N, Anderson M . Retrieval induces adaptive forgetting of competing memories via cortical pattern suppression. Nat Neurosci. 2015; 18(4):582-9. PMC: 4394359. DOI: 10.1038/nn.3973. View