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Cited by 36Memory and Neural MechanismsNeural dynamics and brain functionNeuroscience and Neuropharmacology Research

Flexible weighting of diverse inputs makes hippocampal function malleable

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Aly, Mariam, Turk-Browne, Nicholas B.·2018·Neuroscience Letters
DOI 10.1016/j.neulet.2017.05.063PMC PMC5712489
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Abstract

Classic theories of hippocampal function have emphasized its role as a dedicated memory system, but recent research has shown that it contributes broadly to many aspects of cognition, including attention and perception. We propose that the reason the hippocampus plays such a broad role in cognition is that its function is particularly malleable. We argue that this malleability arises because the hippocampus receives diverse anatomical inputs and these inputs are flexibly weighted based on behavioral goals. We discuss examples of how hippocampal representations can be flexibly weighted, focusing on hippocampal modulation by attention. Finally, we suggest some general neural mechanisms and core hippocampal computations that may enable the hippocampus to support diverse cognitive functions, including attention, perception, and memory. Together, this work suggests that great progress can and has been made in understanding the hippocampus by considering how the domain-general computations it performs allow it to dynamically contribute to many different behaviors.

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  • One possible explanation for the difference in medication response may be related to dysfunctions in neurotransmitter systems that interact with dopamine to modulate cognitive flexibility under uncertainty.

    “One possible explanation for this difference may be related to dysfunctions in neurotransmitter systems that interact with dopamine to modulate cognitive flexibility under uncertainty (Aly and Turk-Browne, 2018).”

    From Predictive coding in neuropsychiatric disorders: a systematic transdiagnostic review. (2025) · cites this paper as Aly and Turk-Browne, 2018

    The Attention section (page unavailable) says dopaminergic and cholinergic systems can alter hippocampal activity patterns and may influence attention. It does not link dysfunction in those systems to differences in medication response, or establish their interaction with dopamine as a mechanism for cognitive flexibility under uncertainty. (LLM, conf=0.82)

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  1. [1]Felleman DJ Van Essen DC Distributed hierarchical processing in the primate cerebral cortex Cer Cor 1 1991 1 47 1822724
  2. [2]Bussey TJ Saksida LM Object memory and perception in the medial temporal lobe: An alternative approach Curr Op Neurobiol 15 2005 730 737 16271459
  3. [3]Lavenex P Amaral DG Hippocampal-neocortical interaction: A hierarchy of associativity Hippocampus 10 2000 420 430 10985281
  4. [4]Hasson U Chen J Honey CJ Hierarchical process memory: Memory as an integral component of information processing Trends Cog Sci 19 2015 304 313 PMC4457571 25980649
  5. [5]Gavornik JP Bear MF Learned spatiotemporal sequence recognition and prediction in primary visual cortex Nat Neurosci 17 2014 732 737 24657967 PMC4167369
  6. [7]Poort J Khan AG Pachitariu M Nemri A Orsolic I Learning enhances sensory and multiple non-sensory representations in primary visual cortex Neuron 86 2015 1 13 26051421 PMC4503798
  7. [8]Shuler MG Bear MF Reward timing in the primary visual cortex Science 311 2006 1606 1609 16543459
  8. [10]Eichenbaum H Barlow versus Hebb: When is it time to abandon the notion of feature detectors and adopt the cell assembly as the unit of cognition? Neurosci Lett 2017 10.1016/j.neulet.2017.04.006 PMC5628090 28389238 · DOI
  9. [11]McKenzie S Keene CS Farovik A Bladon J Place R Komorowski R Eichenbaum H Representation of memories in the cortical-hippocampal system: Results from the application of population similarity analyses Neurobiol Learn Mem 134 2016 178 191 26748022 PMC4930430
  10. [12]Aly M Turk-Browne NB How hippocampal memory shapes, and is shaped by, attention Hannula DE Duff MC The Hippocampus from Cells to Systems Springer International Publishing AG Switzerland 2017 369 403
  11. [13]Olsen RK Moses SN Riggs L Ryan JD The hippocampus supports multiple cognitive processes through relational binding and comparison Front Hum Neurosci 6 2012 146 1 13 22661938 PMC3363343
  12. [14]Schiller D Eichenbaum H Buffalo EA Davachi L Foster DJ Leutgeb S Ranganath C Memory and space: Towards an understanding of the cognitive map J Neurosci 35 2015 13904 13911 26468191 PMC6608181
  13. [15]Shohamy D Turk-Browne NB Mechanisms for widespread hippocampal involvement in cognition J Exp Psychol: Gen 142 2013 1159 1170 24246058 PMC4065494
  14. [16]Yonelinas AP The hippocampus supports high-resolution binding in the service of perception, working memory, and long-term memory Beh Brain Res 254 2013 34 44 PMC3773061 23721964
  15. [17]Rajasethupathy P Sankaran S Marshel JH Kim CK Ferenczi E Projections from neocortex mediate top-down control of memory retrieval Nature 526 2015 653 659 26436451 PMC4825678
  16. [18]Ito HT Zhang SJ Witter MP Moser EI Moser MB A prefrontal-thalamo-hippocampal circuit for goal-directed spatial navigation Nature 522 2015 50 55 26017312
  17. [19]Shapiro ML Riceberg JS Seip-Cammack K Guise KG Functional interactions of prefrontal cortex and hippocampus in learning and memory Derdikman D Knierim JJ Space, Time, and Memory in the Hippocampal Formation Springer New York 2014 517 560
  18. [22]Muzzio IA Kentros C Kandel E What is remembered? Role of attention on the encoding and retrieval of hippocampal representations J Physiol 12 2009 2837 2854 PMC2718243 19525568
  19. [23]Rowland DC Kentros CG Potential anatomical basis for attentional modulation of hippocampal neurons Ann NY Acad Sci 1129 2008 213 224 18591482
  20. [24]Takeuchi T Duszkiewicz AJ Sonneborn A Spooner PA Yamasaki M Locus coeruleus and dopaminergic consolidation of everyday memory Nature 537 2016 357 362 27602521 PMC5161591
  21. [25]Backus AR Bosch SE Ekman M Vicente-Grabovetsky A Doeller CF Mnemonic convergence in the human hippocampus Nat Comm 7 2016 11991 1 9 PMC4919533 27325442
  22. [26]Mišić B Goñi J Betzel RF Sporns O McIntosh AR A network convergence zone in the hippocampus PLoS Comp Biol 10 2014 e1003982 1 10 PMC4256084 25474350
  23. [28]Lee ACH Yeung LK Barense MD The hippocampus and visual perception Front Hum Neurosci 6 2012 91 1 17 22529794 PMC3328126
  24. [30]Nadel L Peterson MA The hippocampus: Part of an interactive posterior representational system spanning perceptual and memorial systems J Exp Psychol: Gen 142 2013 1242 1254 23895347
  25. [31]Eichenbaum H Cohen NJ Can we reconcile the declarative memory and spatial navigation views on hippocampal function? Neuron 83 2014 764 770 25144874 PMC4148642
  26. [33]Moses SN Ryan JD A comparison and evaluation of the predictions of relational and conjunctive accounts of hippocampal function Hippocampus 16 2006 43 65 16270317
  27. [34]Horner AJ Bisby JA Bush D Lin WJ Burgess N Evidence for holistic episodic recollection via hippocampal pattern completion Nat Comm 6 2015 7462 1 11 PMC4506995 26136141
  28. [35]Mack ML Preston AR Decisions about the past are guided by reinstatement of specific memories in the hippocampus and perirhinal cortex NeuroImage 127 2016 144 157 26702775 PMC4755795
  29. [36]Staresina BP Michelmann S Bonnefond M Jensen O Axmacher N Fell J Hippocampal pattern completion is linked to gamma power increases and alpha power decreases during recollection eLife 5 2016 e17397 1 18 27508355 PMC4980114
  30. [37]Tompary A Duncan K Davachi L High-resolution investigation of memory-specific reinstatement in the hippocampus and perirhinal cortex Hippocampus 26 2016 995 1007 26972485 PMC4949140
  31. [39]Dudukovic NM Preston AR Archie JJ Glover GH Wagner AD High-resolution fMRI reveals match enhancement and attentional modulation in the human medial temporal lobe J Cogn Neurosci 23 2010 670 682 20433244 PMC5746189
  32. [40]Yamaguchi S Hale LA D’Esposito M Knight RT Rapid prefrontal-hippocampal habituation to novel events J Neurosci 24 2004 5356 5363 15190108 PMC6729309
  33. [41]Carr VA Engel SA Knowlton BJ Top-down modulation of hippocampal encoding activity as measured by high-resolution functional MRI Neuropsychologia 51 1829 1837 PMC3829781 23838003
  34. [42]Davachi L Wagner AD Hippocampal contributions to episodic encoding: Insights from relational and item-based learning J Neurophysiol 88 2002 982 990 12163547
  35. [43]Uncapher MR Rugg MD Selecting for memory? The influence of selective attention on the mnemonic binding of contextual information J Neurosci 29 2009 8270 8279 19553466 PMC2730727
  36. [44]Kelemen E Fenton AA Coordinating different representations in the hippocampus Neurobiol Learn Mem 129 2016 50 59 26748023
  37. [45]Muzzio IA Levita L Kulkarni J Monaco J Kentros C Stead M Abbott LF Kandel ER Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus PLoS Biol 7 2009 e1000140 1 20 19564903 PMC2696347
  38. [46]Kentros CG Agnihotri NT Streater S Hawkins RD Kandel ER Increased attention to spatial context increases both place field stability and spatial memory Neuron 42 2004 283 295 15091343
  39. [47]Jackson J Redish AD Network dynamics of hippocampal cell-assembles resemble multiple spatial maps within single tasks Hippocampus 17 2007 1209 1229 17764083
  40. [48]Kelemen E Fenton AA Dynamic grouping of hippocampal neural activity during cognitive control of two spatial frames PLoS Biol 8 2010 e1000403 1 14 20585373 PMC2889929
  41. [50]Aly M Turk-Browne NB Attention stabilizes representations in the human hippocampus Cer Cor 26 2016 783 796 PMC4712804 25766839
  42. [51]Mack ML Love BC Preston AR Dynamic updating of hippocampal object representations reflects new conceptual knowledge Proc Natl Acad Sci 113 2016 13203 13208 27803320 PMC5135299
  43. [52]Monaco JD Rao G Roth ED Knierim JJ Attentive scanning behavior drives one-trial potentiation of hippocampal place fields Nat Neurosci 17 2014 725 731 24686786 PMC4036486
  44. [53]Suthana N Ekstrom A Moshirvaziri S Knowlton B Bookheimer S Dissociations within human hippocampal subregions during encoding and retrieval of spatial information Hippocampus 21 2011 694 701 20882543 PMC3026858
  45. [54]Wolosin SM Zeithamova D Preston AR Distributed hippocampal patterns that discriminate reward context are associated with enhanced associative binding J Exp Psychol: Gen 142 2013 1264 1276 23834024 PMC4731099
  46. [55]Zeineh MM Engel SA Thompson PM Bookheimer SY Dynamics of the hippocampus during encoding and retrieval of face-name pairs Science 299 2003 577 580 12543980
  47. [56]Aly M Turk-Browne NB Attention promotes episodic encoding by stabilizing hippocampal representations Proc Natl Acad Sci 113 2016 E420 E429 26755611 PMC4743819
  48. [57]Summerfield JJ Lepsien J Gitelman DR Mesulam MM Nobre AC Orienting attention based on long-term memory experience Neuron 49 2006 905 916 16543137
  49. [58]Stokes MG Atherton K Patai EZ Nobre AC Long-term memory prepares neural activity for perception Proc Natl Acad Sci 109 2012 E360 E367 22109554 PMC3277524
  50. [59]Voss JL Cohen NJ Hippocampal-cortical contributions to strategic exploration during perceptual discrimination Hippocampus 27 2017 642 652 28241401 PMC5435547
  51. [60]Buckner RL The role of the hippocampus in prediction and imagination Ann Rev Psychol 61 2010 27 48 19958178
  52. [61]Brown TI Carr VA LaRocque KF Favila SE Gordon AM Prospective representation of navigational goals in the human hippocampus Science 352 2016 1323 1326 27284194
  53. [62]Balaguer J Spiers H Hassabis D Summerfield C Neural mechanisms of hierarchical planning in a virtual subway network Neuron 90 2016 893 903 27196978 PMC4882377
  54. [64]Pfeiffer BE Foster DJ Hippocampal place-cell sequences depict future paths to remembered goals Nature 497 2013 74 81 23594744 PMC3990408
  55. [65]Ólafsdóttir HF Barry C Saleem AB Hassabis D Spiers HJ Hippocampal place cells construct reward related sequences through unexplored space eLife 4 2015 e06063 1 17 26112828 PMC4479790
  56. [66]Dudchenko PA Wood ER Splitter cells: Hippocampal place cells whose firing is modulated by where the animal is going or where it has been Derdikman D Knierim JJ Space, Time, and Memory in the Hippocampal Formation Springer New York 2014 253 272
  57. [67]Bornstein AM Daw ND Cortical and hippocampal correlates of deliberation during model-based decisions for rewards in humans PLoS Comp Biol 9 2013 e1003387 1 19 PMC3854511 24339770
  58. [68]Hindy NC Ng FY Turk-Browne NB Linking pattern completion in the hippocampus to predictive coding in visual cortex Nat Neurosci 19 2016 665 667 27065363 PMC4948994
  59. [69]Schapiro AC Kustner LV Turk-Browne NB Shaping of object representations in the human medial temporal lobe based on temporal regularities Curr Biol 22 2012 1622 1627 22885059 PMC3443305
  60. [70]Turk-Browne NB Scholl BJ Johnson MK Chun MM Implicit perceptual anticipation triggered by statistical learning J Neurosci 30 2010 11177 11187 20720125 PMC2947492
  61. [71]Hollup SA Molden S Donnett JG Moser MB Moser EI Accumulation of hippocampal place fields at the goal location in an annular watermaze task J Neurosci 21 2001 1635 1644 11222654 PMC6762966
  62. [72]Hok V Lenck-Santini PP Roux S Save E Muller RU Poucet B Goal-related activity in hippocampal place cells J Neurosci 27 2007 472 482 17234580 PMC6672791
  63. [73]Kennedy PJ Shapiro ML Motivational states activate distinct hippocampal representations to guide goal-directed behaviors Proc Natl Acad Sci 106 2009 10805 10810 19528659 PMC2705558
  64. [74]Barron HC Dolan RJ Behrens TEJ Online evaluation of novel choices by simultaneous representation of multiple memories Nat Neurosci 16 2013 1492 1498 24013592 PMC4001211
  65. [75]Newman EL Gupta K Climer JR Monaghan CK Hasselmo ME Cholinergic modulation of cognitive processing: Insights drawn from computational models Front Beh Neurosci 6 2012 24 1 19 PMC3374475 22707936
  66. [76]Brazhnik ES Muller RU Fox SE Muscarinic blockade slows and degrades the location-specific firing of hippocampal pyramidal cells J Neurosci 23 2003 611 621 12533621 PMC6741889
  67. [77]Knierim JJ Neunuebel JP Tracking the flow of hippocampal computation: Pattern separation, pattern completion, and attractor dynamics Neurobiol Learn Mem 129 2016 38 49 26514299 PMC4792674
  68. [79]Turk-Browne NB Functional interactions as big data in the human brain Science 342 2013 580 584 24179218 PMC3970973
  69. [80]Córdova NI Tompary A Turk-Browne NB Attentional modulation of background connectivity between ventral visual cortex and the medial temporal lobe Neurobiol Learn Mem 10.1016/j.nlm.2016.06.011 PMC5018439 27321163 · DOI
  70. [81]Ranganath C Ritchey M Two cortical systems for memory-guided behavior Nat Rev Neurosci 13 2012 713 726 22992647
  71. [82]Hannula DE Ranganath C The eyes have it: Hippocampal activity predicts expression of memory in eye movements Neuron 63 2009 592 599 19755103 PMC2747814
  72. [83]Hannula DE Ryan JD Tranel D Cohen NJ Rapid onset relational memory effects are evident in eye movement behavior, but not in hippocampal amnesia J Cogn Neurosci 19 2007 1690 1705 17854282
  73. [84]Ryals AJ Wang JX Polnaszek KL Voss JL Hippocampal contribution to implicit configuration memory expressed via eye movements during scene exploration Hippocampus 25 2015 1028 1041 25620526 PMC4514574
  74. [85]Aly M Ranganath C Yonelinas AP Detecting changes in scenes: The hippocampus is critical for strength-based perception Neuron 78 2013 1127 1137 23791201 PMC3694276
  75. [86]Baxter MG Involvement of medial temporal lobe structures in memory and perception Neuron 61 2009 667 677 19285463
  76. [88]Collin SHP Milivojevic B Doeller CF Memory hierarchies map onto the hippocampal long axis in hippocampus Nat Neurosci 18 2015 1562 1564 26479587 PMC4665212
  77. [90]McTighe SM Mar AC Romberg C Bussey TJ Sakisda LM A new touchscreen test of pattern separation: Effect of hippocampal lesions NeuroReport 20 2009 881 885 19421077
  78. [91]Keinath AT Wang ME Wann EG Yuan RK Dudman JT Muzzio IA Precise spatial coding is preserved along the longitudinal hippocampal axis Hippocampus 24 2014 1533 1548 25045084 PMC4447627
  79. [93]Duncan K Ketz N Inati SJ Davachi L Evidence for area CA1 as a match/mismatch detector: A high-resolution fMRI study of the human hippocampus Hippocampus 22 2012 389 398 21484934 PMC3529001
  80. [94]Elfman KW Aly M Yonelinas AP Neurocomputational account of memory and perception: Thresholded and graded signals in the hippocampus Hippocampus 24 2014 1672 1686 25112784
  81. [95]Carrillo-Rein L Yang W Bando Y Peterka DS Yuste R Imprinting and recalling cortical ensembles Science 353 2016 691 694 27516599 PMC5482530
  82. [96]Kent BA Hvoslef-Eide M Saksida LM Bussey TJ The representational-hierarchical view of pattern separation: Not just hippocampus, not just space, not just memory? Neurobiol Learn Mem 129 2016 99 106 26836403
  83. [97]Nortmann N Rekauzke S Onat S König P Jancke D Primary visual cortex represents the difference between past and present Cer Cor 25 2015 1427 1440 PMC4428292 24343889
  84. [98]Miller EK Cohen JD An integrative theory of prefrontal cortex function Ann Rev Neurosci 24 2001 167 202 11283309
  85. [100]Kumaran D Hassabis D McClelland JL What learning systems do intelligent agents need? Complementary learning systems theory updated Trends Cog Sci 20 2016 512 534 27315762

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Authors
Aly, M., & Turk-Browne, N. B.
Affiliations
Princeton University (US)
Corresponding author
Aly, Mariam
ORCID
Aly, Mariam
Venue
Neuroscience Letters
Publisher
Elsevier BV
Published
2018-07
Volume
680
Pages
13-22
ISSN
0304-3940 (ISSN-L)
DOI
10.1016/j.neulet.2017.05.063
PMC
PMC5712489
OpenAlex
W2621335817
Cited by
36
References
15
Citations by year
2026: 3 · 2025: 3 · 2024: 5 · 2023: 4 · 2022: 2 · 2021: 3 · 2020: 8 · 2019: 4 · 2018: 3
FWCI
0.46
Type
journal article
Language
en
Open access
Licence
Locations
  • Neuroscience Letters (acceptedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
Funders
  • National Institutes of Health (UL1TR001863)
  • National Eye Institute (R01EY021755)
  • National Center for Advancing Translational Sciences
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
hippocampus, hippocampal function, malleability, input weighting, attention, memory, perception, behavioral objectives, neural mechanisms
MeSH terms
Attention, Hippocampus, Humans, Memory, Perception

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