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When does conscious memory become dependent on the hippocampus? The role of memory load and the differential relevance of left hippocampal integrity for short- and long-term aspects of verbal memory performance

  • Juri-Alexander WittEmail author
  • Roland Coras
  • Albert J. Becker
  • Christian E. Elger
  • Ingmar Blümcke
  • Christoph Helmstaedter
Original Article

Abstract

Supraspan list learning tests are sensitive measures used to assess temporal lobe dysfunction. Most frequently employed is the Rey Auditory Verbal Learning and Memory Test (RAVLT). The test’s structure is determined by a short- and long-term memory component. During the first of five learning trials, the short-term memory component is the highest and steadily decreases over the following trials, while the long-term memory component concurrently increases and reaches its maximum at the delayed recall after a retention interval of 30 min. The study aimed to test the hypothesis that the functional relevance of left hippocampal integrity for conscious memory rises along with the increasing degree of the long-term memory component. Moreover, we investigated whether classical measures of short-term and working memory are also dependent on the hippocampus. The analysis was based on 37 adult patients who had undergone surgery for left mesial temporal lobe epilepsy. Neuronal cell densities of the resected left hippocampus were correlated with the presurgical memory performance across trials of the VLMT (the German RAVLT) and with digit span and working memory capacity (WMS-R). Whereas digit span and working memory capacity were not related to hippocampal cell counts, there was a significant correlation between left hippocampal integrity and VLMT memory performance, already regarding the first supraspan learning trial. Correlations steadily increased during the learning course. The highest correlation was seen regarding the delayed free recall. The results indicate an increasing correspondence between the integrity of the left hippocampus and verbal memory with an increasing long-term memory component. Immediate recall of verbal material became already dependent on left hippocampal integrity when the verbal memory load exceeded the memory span (supraspan list learning), while classical span measures that assess verbal short-term and working memory were not affected by left hippocampal pathology.

Keywords

Hippocampus Neuronal cell counts Cell densities Cornu ammonis Dentate gyrus Memory Declarative memory Working memory Learning 

Notes

Compliance with ethical standards

Conflict of interest

The authors state that they have no conflicts of interest regarding the manuscript.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

References

  1. Axmacher N, Mormann F, Fernández G, Cohen MX, Elger CE, Fell J (2007) Sustained neural activity patterns during working memory in the human medial temporal lobe. J Neurosci 27(29):7807–7816.  https://doi.org/10.1523/jneurosci.0962-07.2007 Google Scholar
  2. Baddeley A (1992) Working memory. Science 255(5044):556–559Google Scholar
  3. Baddeley AD, Patterson K (1971) The relation between long-term and short-term memory. Br Med Bull 27(3):237–242Google Scholar
  4. Baddeley A, Jarrold C, Vargha-Khadem F (2011) Working memory and the hippocampus. J Cogn Neurosci 23(12):3855–3861.  https://doi.org/10.1162/jocn_a_00066 Google Scholar
  5. Barbey AK, Koenigs M, Grafman J (2013) Dorsolateral prefrontal contributions to human working memory. Cortex J Devoted Study Nerv Syst Behav 49(5):1195–1205.  https://doi.org/10.1016/j.cortex.2012.05.022 Google Scholar
  6. Baxendale SA, Van Paesschen W, Thompson PJ, Duncan JS, Harkness WF, Shorvon SD (1998) Hippocampal cell loss and gliosis: relationship to preoperative and postoperative memory function. Neuropsychiatry Neuropsychol Behav Neurol 11(1):12–21Google Scholar
  7. Berg AT (2008) The natural history of mesial temporal lobe epilepsy. Curr Opin Neurol 21(2):173–178.  https://doi.org/10.1097/WCO.0b013e3282f36ccd Google Scholar
  8. Blümcke I, Thom M, Wiestler OD (2002) Ammon’s horn sclerosis: a maldevelopmental disorder associated with temporal lobe epilepsy. Brain Pathol 12(2):199–211Google Scholar
  9. Blümcke I, Pauli E, Clusmann H, Schramm J, Becker A, Elger C, Merschhemke M, Meencke H-J, Lehmann T, Deimling A, Scheiwe C, Zentner J, Volk B, Romstöck J, Stefan H, Hildebrandt M (2007) A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathol (Berl) 113(3):235–244.  https://doi.org/10.1007/s00401-006-0187-0 Google Scholar
  10. Blümcke I, Kistner I, Clusmann H, Schramm J, Becker AJ, Elger CE, Bien CG, Merschhemke M, Meencke H-J, Lehmann T, Buchfelder M, Weigel D, Buslei R, Stefan H, Pauli E, Hildebrandt M (2009) Towards a clinico-pathological classification of granule cell dispersion in human mesial temporal lobe epilepsies. Acta Neuropathol (Berl) 117(5):535–544.  https://doi.org/10.1007/s00401-009-0512-5 Google Scholar
  11. Blümcke I, Thom M, Aronica E, Armstrong DD, Bartolomei F, Bernasconi A, Bernasconi N, Bien CG, Cendes F, Coras R, Cross JH, Jacques TS, Kahane P, Mathern GW, Miyata H, Moshe SL, Oz B, Ozkara C, Perucca E, Sisodiya S, Wiebe S, Spreafico R (2013) International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: a Task Force report from the ILAE Commission on Diagnostic Methods. Epilepsia 54(7):1315–1329.  https://doi.org/10.1111/epi.12220 Google Scholar
  12. Brand M, Markowitsch HJ (2003) The principle of bottleneck structures. In: Kluwe RH, Lüer G, Rösler F (eds) Principles of learning and memory. Birkhäuser, Basel.  https://doi.org/10.1007/978-3-0348-8030-5_10 Google Scholar
  13. Burgess N (2008) Spatial cognition and the brain. Ann N Y Acad Sci 1124(1):77–97.  https://doi.org/10.1196/annals.1440.002 Google Scholar
  14. Cohen J (1998) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum, HillsdaleGoogle Scholar
  15. Corsi PM (1972) Human Memory and the Medial Temporal Region of the Brain. Dissertation, McGill University, MontrealGoogle Scholar
  16. Cowey CM, Green S (1996) The hippocampus: a “working memory” structure? The effect of hippocampal sclerosis on working memory. Memory 4(1):19–30.  https://doi.org/10.1080/741940668 Google Scholar
  17. D’Esposito M (2007) From cognitive to neural models of working memory. Philos Trans R Soc Lond B Biol Sci 362(1481):761–772.  https://doi.org/10.1098/rstb.2007.2086 Google Scholar
  18. Djordjevic J, Jones-Gotman M (2011) Inquiry on assessments across epilepsy centers in different countries. In: Helmstaedter C, Hermann B, Kahane P, Arzimanoglou A (eds) Neuropsychology in the care of people with epilepsy. John Libbey Eurotext, MontrougeGoogle Scholar
  19. Eichenbaum H (2013) What H.M. taught us. J Cogn Neurosci 25(1):14–21.  https://doi.org/10.1162/jocn_a_00285 Google Scholar
  20. Fernández G, de Greiff A, von Oertzen J, Reuber M, Lun S, Klaver P, Ruhlmann J, Reul J, Elger CE (2001) Language mapping in less than 15 min: real-time functional MRI during routine clinical investigation. Neuroimage 14(3):585–594.  https://doi.org/10.1006/nimg.2001.0854 Google Scholar
  21. Gleissner U, Helmstaedter C, Elger CE (2002) Memory reorganization in adult brain: observations in three patients with temporal lobe epilepsy. Epilepsy Res 48(3):229–234Google Scholar
  22. Gleissner U, Helmstaedter C, Schramm J, Elger CE (2004) Memory outcome after selective amygdalohippocampectomy in patients with temporal lobe epilepsy: 1-year follow-up. Epilepsia 45(8):960–962.  https://doi.org/10.1111/j.0013-9580.2004.42203.x Google Scholar
  23. Grunwald T, Lehnertz K, Heinze HJ, Helmstaedter C, Elger CE (1998) Verbal novelty detection within the human hippocampus proper. Proc Natl Acad Sci USA 95(6):3193–3197Google Scholar
  24. Härting C, Markowitsch HJ, Neufeld H, Calabrese P, Deisinger K (2000) WMS-R—Wechsler Gedächtnis Test—Revidierte Fassung. Deutsche Adaptation der revidierten Fassung der Wechsler-Memory-Scale. Hogrefe, GöttingenGoogle Scholar
  25. Helmstaedter C, Witt J-A (2017) How neuropsychology can improve the care of individual patients with epilepsy. Looking back and into the future. Seizure 44:113–120.  https://doi.org/10.1016/j.seizure.2016.09.010 Google Scholar
  26. Helmstaedter C, Pohl C, Hufnagel A, Elger CE (1991) Visual learning deficits in nonresected patients with right temporal lobe epilepsy. Cortex 27(4):547–555Google Scholar
  27. Helmstaedter C, Elger CE, Hufnagel A, Zentner J, Schramm J (1996) Different effects of left anterior temporal lobectomy, selective amygdalohippocampectomy, and temporal cortical lesionectomy on verbal learning, memory, and recognition. J Epilepsy 9(1):39–45Google Scholar
  28. Helmstaedter C, Grunwald T, Lehnertz K, Gleissner U, Elger CE (1997) Differential involvement of left temporolateral and temporomesial structures in verbal declarative learning and memory: evidence from temporal lobe epilepsy. Brain Cognit 35(1):110–131Google Scholar
  29. Helmstaedter C, Lendt M, Lux S (2001) VLMT Verbaler Lern- und Merkfähigkeitstest. Beltz Test GmbH, GöttingenGoogle Scholar
  30. Isaacs KL, Barr WB, Nelson PK, Devinsky O (2006) Degree of handedness and cerebral dominance. Neurology 66(12):1855–1858.  https://doi.org/10.1212/01.wnl.0000219623.28769.74 Google Scholar
  31. Jeneson A, Mauldin KN, Squire LR (2010) Intact working memory for relational information after medial temporal lobe damage. J Neurosci Off J Soc Neurosci 30(41):13624–13629.  https://doi.org/10.1523/JNEUROSCI.2895-10.2010 Google Scholar
  32. Kral T, Clusmann H, Urbach J, Schramm J, Elger CE, Kurthen M, Grunwald T (2002) Preoperative evaluation for epilepsy surgery (Bonn Algorithm). Zentralblatt für Neurochirurgie 63(3):106–110.  https://doi.org/10.1055/s-2002-35826 Google Scholar
  33. Loring DW, Strauss E, Hermann BP, Perrine K, Trenerry MR, Barr WB, Westerveld M, Chelune GJ, Lee GP, Meador KJ (1999) Effects of anomalous language representation on neuropsychological performance in temporal lobe epilepsy. Neurology 53(2):260–264Google Scholar
  34. Markowitsch HJ, Kalbe E, Kessler J, von Stockhausen HM, Ghaemi M, Heiss WD (1999) Short-term memory deficit after focal parietal damage. J Clin Exp Neuropsychol 21(6):784–797.  https://doi.org/10.1076/jcen.21.6.784.853 Google Scholar
  35. Miller GA (1956) The magical number seven plus or minus two: some limits on our capacity for processing information. Psychol Rev 63(2):81–97Google Scholar
  36. Müller NG, Knight RT (2006) The functional neuroanatomy of working memory: contributions of human brain lesion studies. Neuroscience 139(1):51–58.  https://doi.org/10.1016/j.neuroscience.2005.09.018 Google Scholar
  37. Müller H, Hasse-Sander I, Horn R, Helmstaedter C, Elger CE (1997) Rey Auditory-Verbal Learning Test: structure of a modified German version. J Clin Psychol 53(7):663–671.  https://doi.org/10.1002/(SICI)1097-4679(199711)53:7%3C663::AID-JCLP4%3E3.0.CO;2-J Google Scholar
  38. Nyberg L (2005) Any novelty in hippocampal formation and memory? Curr Opin Neurol 18(4):424–428Google Scholar
  39. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113Google Scholar
  40. Ranganath C, D’Esposito M (2001) Medial temporal lobe activity associated with active maintenance of novel information. Neuron 31(5):865–873Google Scholar
  41. Rey A (1964) L’examen clinique en psychologie. Presses Universitaires de France, ParisGoogle Scholar
  42. Sass KJ, Buchanan CP, Kraemer S, Westerveld M, Kim JH, Spencer DD (1995) Verbal memory impairment resulting from hippocampal neuron loss among epileptic patients with structural lesions. Neurology 45(12):2154–2158Google Scholar
  43. Squire LR (1982) The neuropsychology of human memory. Annu Rev Neurosci 5:241–273.  https://doi.org/10.1146/annurev.ne.05.030182.001325 Google Scholar
  44. Squire LR (1987–1988) The organization and neural substrates of human memory. Int J Neurol 21–22:218–222Google Scholar
  45. Strauss E, Satz P, Wada J (1990) An examination of the crowding hypothesis in epileptic patients who have undergone the carotid amytal test. Neuropsychologia 28(11):1221–1227Google Scholar
  46. Vogt VL, Äikiä M, Del Barrio A, Boon P, Borbély C, Bran E, Braun K, Carette E, Clark M, Cross JH, Dimova P, Fabo D, Foroglou N, Francione S, Gersamia A, Gil-Nagel A, Guekht A, Harrison S, Hecimovic H, Heminghyt E, Hirsch E, Javurkova A, Kälviäinen R, Kavan N, Kelemen A, Kimiskidis VK, Kirschner M, Kleitz C, Kobulashvili T, Kosmidis MH, Kurtish SY, Lesourd M, Ljunggren S, Lossius MI, Malmgren K, Mameniskiené R, Martin-Sanfilippo P, Marusic P, Miatton M, Özkara Ç, Pelle F, Rubboli G, Rudebeck S, Ryvlin P, van Schooneveld M, Schmid E, Schmidt P-M, Seeck M, Steinhoff BJ, Shavel-Jessop S, Tarta-Arsene O, Trinka E, Viggedal G, Wendling A-S, Witt J-A, Helmstaedter C (2017) Current standards of neuropsychological assessment in epilepsy surgery centers across Europe. Epilepsia 58(3):343–355.  https://doi.org/10.1111/epi.13646 Google Scholar
  47. Wager TD, Smith EE (2003) Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci 3(4):255–274Google Scholar
  48. Winston GP, Stretton J, Sidhu MK, Symms MR, Thompson PJ, Duncan JS (2013) Structural correlates of impaired working memory in hippocampal sclerosis. Epilepsia 54(7):1143–1153.  https://doi.org/10.1111/epi.12193 Google Scholar
  49. Witt JA, Helmstaedter C (2009) Neuropsychologie bei Epilepsie. Teil II: Gibt es eine gemeinsame Basis zur Etablierung diagnostischer Leitlinien? Fortschritte der Neurologie · Psychiatrie 77(12):691–698.  https://doi.org/10.1055/s-0028-1109799 Google Scholar
  50. Witt J-A, Coras R, Schramm J, Becker AJ, Elger CE, Blümcke I, Helmstaedter C (2014) The overall pathological status of the left hippocampus determines preoperative verbal memory performance in left mesial temporal lobe epilepsy. Hippocampus 24(4):446–454.  https://doi.org/10.1002/hipo.22238 Google Scholar
  51. Wood AG, Saling MM, O’Shea MF, Jackson GD, Berkovic SF (1999) Reorganization of verbal memory and language: a case of dissociation. J Int Neuropsychol Soc 5(1):69–74Google Scholar
  52. Wyler AR, Dohan FC, Schweitzer JB, Berry AD (1992) A grading system for mesial temporal pathology (hippocampal sclerosis) from anterior temporal lobectomy. J Epilepsy 5(4):220–225Google Scholar
  53. Zentner J, Wolf HK, Helmstaedter C, Grunwald T, Aliashkevich AF, Wiestler OD, Elger CE, Schramm J (1999) Clinical relevance of amygdala sclerosis in temporal lobe epilepsy. J Neurosurg 91(1):59–67Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of EpileptologyUniversity of Bonn Medical CenterBonnGermany
  2. 2.Department of NeuropathologyUniversity Hospital of ErlangenErlangenGermany
  3. 3.Department of NeuropathologyUniversity of Bonn Medical CenterBonnGermany

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