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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

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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.

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Notes

  1. The strongest proof in neuropsychological research is the so-called double dissociation, i.e., function A but not function B is disrupted by lesion C, while function B is affected by lesion D which in turn does not interfere with function A.

References

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baddeley A (1992) Working memory. Science 255(5044):556–559

    Article  CAS  PubMed  Google Scholar 

  • Baddeley AD, Patterson K (1971) The relation between long-term and short-term memory. Br Med Bull 27(3):237–242

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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):12–21

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Blümcke I, Thom M, Wiestler OD (2002) Ammon’s horn sclerosis: a maldevelopmental disorder associated with temporal lobe epilepsy. Brain Pathol 12(2):199–211

    PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Cohen J (1998) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum, Hillsdale

    Google Scholar 

  • Corsi PM (1972) Human Memory and the Medial Temporal Region of the Brain. Dissertation, McGill University, Montreal

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, Montrouge

    Google Scholar 

  • Eichenbaum H (2013) What H.M. taught us. J Cogn Neurosci 25(1):14–21. https://doi.org/10.1162/jocn_a_00285

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Gleissner U, Helmstaedter C, Elger CE (2002) Memory reorganization in adult brain: observations in three patients with temporal lobe epilepsy. Epilepsy Res 48(3):229–234

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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):3193–3197

    Article  CAS  PubMed  Google Scholar 

  • 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, Göttingen

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Helmstaedter C, Pohl C, Hufnagel A, Elger CE (1991) Visual learning deficits in nonresected patients with right temporal lobe epilepsy. Cortex 27(4):547–555

    Article  CAS  PubMed  Google Scholar 

  • 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):39–45

    Article  Google Scholar 

  • 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):110–131

    Article  CAS  Google Scholar 

  • Helmstaedter C, Lendt M, Lux S (2001) VLMT Verbaler Lern- und Merkfähigkeitstest. Beltz Test GmbH, Göttingen

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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):260–264

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Miller GA (1956) The magical number seven plus or minus two: some limits on our capacity for processing information. Psychol Rev 63(2):81–97

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Nyberg L (2005) Any novelty in hippocampal formation and memory? Curr Opin Neurol 18(4):424–428

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113

    Article  CAS  PubMed  Google Scholar 

  • Ranganath C, D’Esposito M (2001) Medial temporal lobe activity associated with active maintenance of novel information. Neuron 31(5):865–873

    Article  CAS  PubMed  Google Scholar 

  • Rey A (1964) L’examen clinique en psychologie. Presses Universitaires de France, Paris

    Google Scholar 

  • 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):2154–2158

    Article  CAS  PubMed  Google Scholar 

  • Squire LR (1982) The neuropsychology of human memory. Annu Rev Neurosci 5:241–273. https://doi.org/10.1146/annurev.ne.05.030182.001325

    Article  CAS  PubMed  Google Scholar 

  • Squire LR (1987–1988) The organization and neural substrates of human memory. Int J Neurol 21–22:218–222

    PubMed  Google Scholar 

  • 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):1221–1227

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Wager TD, Smith EE (2003) Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci 3(4):255–274

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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):69–74

    Article  CAS  PubMed  Google Scholar 

  • 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):220–225

    Article  Google Scholar 

  • 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):59–67

    Article  CAS  PubMed  Google Scholar 

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Witt, JA., Coras, R., Becker, A.J. et al. 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. Brain Struct Funct 224, 1599–1607 (2019). https://doi.org/10.1007/s00429-019-01857-1

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