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Current Topics Regarding the Function of the Medial Temporal Lobe Memory System

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Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 37))

Abstract

The first clear insight that the medial temporal lobe of the human brain was in fact a system of anatomically connected structures that were organized into a memory system came in 1957 from the observations by Brenda Milner of the noted amnesic patient H.M. Subsequent work in humans, monkeys, and rodents has identified all of the components of the medial temporal lobe (MTL) that formed the memory system. Currently, work is ongoing to identify the specific contributions each structure in the medial temporal lobe makes towards the formation and storage of long-term declarative memory. The historical background of this work is described including what insights the study of noted neurologic patients H.M. and E.P. provided for understanding the function of the medial temporal lobe. The development of an animal model of medial temporal lobe function is described. Additionally, the insights that lead to the understanding that the brain contains multiple, anatomically discrete, memory systems are described. Finally, three current topics of debate are addressed: First, does the perirhinal cortex exclusively support memory, or does it support both memory and higher order visual perception? Second, is there an anatomical separation between recollection and familiarity? Third, is the organization of spatial memory different between humans and rats, or perhaps the difference is between the working memory capacities of the two species?

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References

  • Aggleton JP, Brown MW (2006) Interleaving brain systems for episodic and recognition memory. Trends Cogn Sci 10:455–463

    Article  PubMed  Google Scholar 

  • Aggleton JP, Hunt PR, Rawlins JNP (1986) The effects of hippocampal lesions upon spatial and non-spatial tests of working memory. Behav Brain Res 19:133–146

    Article  CAS  PubMed  Google Scholar 

  • Aggleton JP, Vann SD, Denby C, Dix S, Mayes AR, Roberts N, Yonelinas AP (2005) Sparing of the familiarity component of recognition memory in a patient with hippocampal pathology. Neuropsychologia 43:1810–1823

    Article  PubMed  Google Scholar 

  • Ahn JR, Lee I (2017) Neural correlates of both perception and memory for objects in the rodent perirhinal cortex. Cereb Cortex 24:1–13

    Google Scholar 

  • Ainge JA, Heron-Maxwell C, Theofilas P, Wright P, de Hoz L, Wood ER (2006) The role of the hippocampus in object recognition in rats: examination of the influence of task parameters and lesion size. Behav Brain Res 167(1):183–195

    Article  PubMed  Google Scholar 

  • Alvarez P, Zola-Morgan S, Squire LR (1995) Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys. J Neurosci 15:3796–3807

    CAS  PubMed  PubMed Central  Google Scholar 

  • Annese J, Schenker-Ahmed NM, Bartsch H, Maechler P, Sheh C, Thomas N, Kayano J, Ghatan A, Bresler N, Frosch MP, Klaming R, Corkin S (2014) Postmortem examination of patient H.M.’s brain based on histological sectioning and digital 3D reconstruction. Nat Commun 5:3122

    Google Scholar 

  • Atkinson RC, Juola JF (1974) Search and decision processes in recognition memory. In: Krantz DH, Atkinson RC, Suppes P (eds) Contemporary developments in mathematical psychology. Freeman, San Francisco, pp 243–290

    Google Scholar 

  • Augustinack JC, van der Kouwe AJ, Salat DH, Benner T, Stevens AA, Annese J, Fischl B, Frosch MP, Corkin S (2014) H.M.’s contributions to neuroscience: a review and autopsy studies. Hippocampus 24(11):1267–1286

    Article  PubMed  PubMed Central  Google Scholar 

  • Baddeley A (2003) Working memory: looking back and looking forward. Nat Rev Neurosci 4:829–839

    Article  CAS  PubMed  Google Scholar 

  • Baddeley AD, Warrington EK (1970) Amnesia and the distinction between long-and short-term memory. J Verbal Learn Verbal Behav 9(2):176–189

    Article  Google Scholar 

  • Baker KB, Kim JJ (2002) Effects of stress and hippocampal NMDA receptor antagonism on recognition memory in rats. Learn Mem 9:58–65

    Article  PubMed  PubMed Central  Google Scholar 

  • Barense MD, Bussey TJ, Lee AC, Rogers TT, Davies RR, Saksida LM, Murray EA, Graham KS (2005) Functional specialization in the human medial temporal lobe. J Neurosci 25:10239–10246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beason-Held LL, Rosene DL, Killiany RJ, Moss MB (1999) Hippocampal formation lesions produce memory impairment in the rhesus monkey. Hippocampus 9:562–574

    Article  CAS  PubMed  Google Scholar 

  • Broadbent NJ, Squire LR, Clark RE (2004) Spatial memory, recognition memory, and the hippocampus. Proc Natl Acad Sci 101:14515–14520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broadbent NJ, Gaskin S, Squire LR, Clark RE (2009) Object recognition memory and the rodent hippocampus. Learn Mem 17(1):5–11

    Article  PubMed  Google Scholar 

  • Brown MW, Aggleton JP (2001) Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2:51–61

    Article  CAS  PubMed  Google Scholar 

  • Buckley MJ, Gaffan D (1998) Perirhinal cortex ablation impairs configural learning and paired-associate learning equally. Neuropsychologia 36(6):535–546

    Article  CAS  PubMed  Google Scholar 

  • Buckley MJ, Gaffan D (2006) Perirhinal cortical contributions to object perception. Trends Cogn Sci 10(3):100–107

    Article  PubMed  Google Scholar 

  • Buckley MJ, Booth MC, Rolls ET, Gaffan D (2001) Selective perceptual impairments after perirhinal cortex ablation. J Neurosci 21(24):9824–9836

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buffalo EA (2015) Bridging the gap between spatial and mnemonic views of the hippocampal formation. Hippocampus 25(6):713–718

    Article  PubMed  PubMed Central  Google Scholar 

  • Buffalo EA, Ramus SJ, Clark RE, Teng E, Squire LR, Zola SM (1999) Dissociation between the effects of damage to perirhinal cortex and area TE. Learn Mem 6:572–599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buffalo EA, Ramus SJ, Squire LR, Zola SM (2000) Perception and recognition memory in monkeys following lesions of area TE and perirhinal cortex. Learn Mem 7:375–382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bussey TJ, Saksida LM (2005) Object memory and perception in the medial temporal lobe: an alternative approach. Curr Opin Neurobiol 15(6):730–737

    Article  CAS  PubMed  Google Scholar 

  • Bussey TJ, Muir JL, Aggleton JP (1999) Functionally dissociating aspects of event memory: the effects of combined perirhinal and postrhinal cortex lesions on object and place memory in the rat. J Neurosci 19:495–502

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bussey TJ, Duck J, Muir JL, Aggleton JP (2000) Distinct patterns of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat. Behav Brain Res 111:187–202

    Article  CAS  PubMed  Google Scholar 

  • Bussey TJ, Saksida LM, Murray EA (2002) Perirhinal cortex resolves feature ambiguity in complex visual discriminations. Eur J Neurosci 15(2):365–374

    Article  PubMed  Google Scholar 

  • Bussey TJ, Saksida LM, Murray EA (2006) Perirhinal cortex and feature-ambiguous discriminations. Learn Mem 13(2):103–105

    Article  PubMed  Google Scholar 

  • Christian KM, Thompson RF (2003) Neural substrates of eyeblink conditioning: acquisition and retention. Learn Mem 11:427–455

    Article  Google Scholar 

  • Clark RE, Lavond DG (1993) Reversible lesions of the red nucleus during acquisition and retention of a classically conditioned behavior in rabbits. Behav Neurosci 107:264–270

    Article  CAS  PubMed  Google Scholar 

  • Clark RE, Lavond DG (1994) Reacquisition of classical conditioning after removal of cerebellar cortex in Dutch Belted rabbits. Behav Brain Res 61:101–106

    Article  CAS  PubMed  Google Scholar 

  • Clark RE, Martin SJ (2005) Interrogating rodents regarding their object and spatial memory. Curr Opin Neurobiol 15(5):593–598

    Article  CAS  PubMed  Google Scholar 

  • Clark RE, Squire LR (1998) Classical conditioning and brain systems: a key role for awareness. Science 280:77–81

    Article  CAS  PubMed  Google Scholar 

  • Clark RE, Squire LR (2010) An animal model of recognition memory and medial temporal lobe amnesia: history and current issues. Neuropsychologia 48(8):2234–2244

    Article  PubMed  PubMed Central  Google Scholar 

  • Clark RE, Squire LR (2013) Similarity in form and function of the hippocampus in rodents, monkeys, and humans. Proc Natl Acad Sci 110(Suppl 2):10365–10370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark RE, Zhang AA, Lavond DG (1992) Reversible lesions of the cerebellar interpositus nucleus during acquisition and retention of a classically conditioned behavior. Behav Neurosci 106:879–888

    Article  CAS  PubMed  Google Scholar 

  • Clark RE, Zola SM, Squire LR (2000) Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 20:8853–8860

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clark RE, West AN, Zola SM, Squire LR (2001) Rats with lesions of the hippocampus are impaired on the delayed nonmatching-to-sample task. Hippocampus 11(2):176–186

    Article  CAS  PubMed  Google Scholar 

  • Clark RE, Reinagel P, Broadbent NJ, Flister ED, Squire LR (2011) Intact performance on feature ambiguous discriminations in rats with lesions of the perirhinal cortex. Neuron 70(1):132–140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corkin S (1984) Lasting consequences of bilateral medial temporal lobectomy: clinical course and experimental findings in H.M. Semin Neurol 4:249–259

    Article  Google Scholar 

  • Corkin S, Amaral DG, Gonzalez RG, Johnson KA, Hyman BT (1997) H.M.’s medial temporal lobe lesion: findings from magnetic resonance imaging. J Neurosci 17:3964–3980

    CAS  PubMed  PubMed Central  Google Scholar 

  • Correll RE, Scoville WB (1965) Effects of medial temporal lesions on visual discrimination performance. J Comp Physiol Psychol 60:175–181

    Article  CAS  PubMed  Google Scholar 

  • Cowan N (2001) The magical number 4 in short-term memory: a reconsideration of mental storage capacity. Behav Brain Sci 24:87–185

    Article  CAS  PubMed  Google Scholar 

  • Darwin C (1873) Origin of certain instincts. Nature 7(179):417–418

    Article  Google Scholar 

  • Daselaar SM, Fleck MS, Cabeza R (2006) Triple dissociation in the medial temporal lobes: recollection, familiarity, and novelty. J Neurophysiol 96:1902–1911

    Article  CAS  PubMed  Google Scholar 

  • de Lima MN, Luft T, Roesler R, Schroder N (2006) Temporary inactivation reveals an essential role of the dorsal hippocampus in consolidation of object recognition memory. Neurosci Lett 405(1–2):142–146

    Article  PubMed  CAS  Google Scholar 

  • Donaldson W (1996) The role of decision processes in remembering and knowing. Mem Cognit 24:523–533

    Article  CAS  PubMed  Google Scholar 

  • Dunn JC (2004) Remember-know: a matter of confidence. Psychol Rev 111:524–542

    Article  PubMed  Google Scholar 

  • Duva CA, Floresco SB, Wunderlich GR, Lao TL, Pinel JPJ, Phillips AG (1997) Disruption of spatial but not object-recognition memory by neurotoxic lesions of the dorsal hippocampus in rats. Behav Neurosci 111:1184–1196

    Article  CAS  PubMed  Google Scholar 

  • Eacott MJ, Gaffan D, Murray EA (1994) Preserved recognition memory for small sets, and impaired stimulus identification for large sets, following rhinal cortex ablations in monkeys. Eur J Neurosci 6:1466–1478

    Article  CAS  PubMed  Google Scholar 

  • Egan JP (1958). Recognition memory and the operating characteristic (Tech. Note AFCRC-TN-58-51). Indiana University, Hearing and Communication Laboratory, Bloomington

    Google Scholar 

  • Eichenbaum H, Cohen NJ (2014) Can we reconcile the declarative memory and spatial navigation views on hippocampal function? Neuron 83(4):764–770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eichenbaum H, Dudchenko P, Wood E, Shapiro M, Tanila H (1999) The hippocampus, memory, and place cells: is it spatial memory or a memory space? Neuron 23:209–226

    Article  CAS  PubMed  Google Scholar 

  • Eichenbaum H, Yonelinas AP, Ranganath C (2007) The medial temporal lobe and recognition memory. Annu Rev Neurosci 30:123–152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ennaceur A, Neave N, Aggleton JP (1996) Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat. Behav Brain Res 80:9–25

    Article  CAS  PubMed  Google Scholar 

  • Fanselow MS, Gale GD (2003) The amygdala, fear, and memory. Ann N Y Acad Sci 985:125–134

    Article  PubMed  Google Scholar 

  • Fortin NJ, Wright SP, Eichenbaum H (2004) Recollection-like memory retrieval in rats is dependent on the hippocampus. Nature 431:188–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forwood SE, Winters BD, Bussey TJ (2005) Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 hours. Hippocampus 15(3):347–355

    Article  CAS  PubMed  Google Scholar 

  • Gaffan D (1974) Recognition impaired and association intact in the memory of monkeys after transaction of the fornix. J Comp Physiol Psychol 88(6):1100–1109

    Article  Google Scholar 

  • Gaskin S, Tremblay A, Mumby DG (2003) Retrograde and anterograde object recognition in rats with hippocampal lesions. Hippocampus 13:962–969

    Article  PubMed  Google Scholar 

  • Glees P, Griffith HB (1952) Bilateral destruction of the hippocampus (cornu ammonis) in a case of dementia. Monatsschrift für Psychiatrie und Neurologie 129:193–204

    Article  CAS  Google Scholar 

  • Gordon JA (2011) Oscillations and hippocampal–prefrontal synchrony. Curr Opin Neurobiol 21:486–491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Granon S, Vidal C, Thinus-Blanc C, Changeux JP, Poucet B (1994) Working memory, response selection, and effortful processing in rats with medial prefrontal lesions. Behav Neurosci 108(5):883

    Article  CAS  PubMed  Google Scholar 

  • Grünthal E (1947) Über das klinische Bild nach umschriebenem beiderseitigem Ausfall der Ammonshornrinde. Monatsschrift für Psychiatrie und Neurologie 113:1–16

    Article  Google Scholar 

  • Hales JB, Broadbent NJ, Velu PD, Squire LR, Clark RE (2015) Hippocampus, perirhinal cortex, and complex visual discriminations in rats and humans. Learn Mem 22(2):83–91

    Article  PubMed  PubMed Central  Google Scholar 

  • Hammond RS, Tull LE, Stackman RW (2004) On the delay-dependent involvement of the hippocampus in object recognition memory. Neurobiol Learn Mem 82:26–34

    Article  PubMed  Google Scholar 

  • Hampton RR, Murray EA (2002) Learning of discriminations is impaired, but generalization to altered views is intact, in monkeys (Macaca mulatta) with perirhinal cortex removal. Behav Neurosci 116:363–377

    Article  PubMed  Google Scholar 

  • Heathcote A (2003) Item recognition memory and the ROC. J Exp Psychol Learn Mem Cogn 29:1210–1230

    Article  PubMed  Google Scholar 

  • Hegglin K (1953) Über einen Fall von isolierter linkseitiger Ammonshornerweichung bei präseniler Dementz Monatsschrift für Psychiatrie und Neurologie 125:170–186

    Article  CAS  Google Scholar 

  • Holdstock JS, Mayes AR, Isaac CL, Cezayirli E, Roberts N, O’Reilly R, Norman K (2002) Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans? Hippocampus 12:341–351

    Article  CAS  PubMed  Google Scholar 

  • Holdstock JS, Mayes AR, Gong Q, Roberts N, Kapur N (2005) Item recognition is less impaired than recall and associative recognition in a patient with selective hippocampal damage. Hippocampus 15:203–215

    Article  CAS  PubMed  Google Scholar 

  • Horst NK, Laubach M (2009) The role of rat dorsomedial prefrontal cortex in spatial working memory. Neuroscience 164(2):444–456

    Article  CAS  PubMed  Google Scholar 

  • Hyman JM, Zilli EA, Paley AM, Hasselmo ME (2010) Working memory performance correlates with prefrontal-hippocampal theta interactions but not with prefrontal neuron firing rates. Front Integr Neurosci 4

    Google Scholar 

  • Insausti R, Annese J, Amaral DG, Squire LR (2013) Human amnesia and the medial temporal lobe illuminated by neuropsychological and neurohistological findings for patient E.P. Proc Natl Acad Sci 110(21):E1953–E1962

    Article  CAS  Google Scholar 

  • James W (1890) Principles of psychology. Holt, New York

    Google Scholar 

  • Jeneson A, Squire LR (2012) Working memory, long-term memory, and medial temporal lobe function. Learn Mem 19(1):15–25

    Article  PubMed  PubMed Central  Google Scholar 

  • Jeneson A, Mauldin KN, Squire LR (2010) Intact working memory for relational information after medial temporal lobe damage. J Neurosci 30(41):13624–13629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones M, Wilson M (2005) Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial working memory task. PLoS Biol 2:e402

    Article  CAS  Google Scholar 

  • Kane MJ, Engle RW (2002) The role of prefrontal cortex in working-memory capacity, executive attention, and general fluid intelligence: an individual-differences perspective. Psychon Bull Rev 9(4):637–671

    Article  PubMed  Google Scholar 

  • Kesner RP, Bolland BL, Dakis M (1993) Memory for spatial locations, motor responses, and objects: triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex. Exp Brain Res 93:462–470

    Article  CAS  PubMed  Google Scholar 

  • Kim S, Sapiurka M, Clark RE, Squire LR (2013) Contrasting effects on path integration after hippocampal damage in humans and rats. Proc Natl Acad Sci 110(12):4732–4737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kornecook TJ, Anzarut A, Pinel JP (1999) Rhinal cortex, but not medial thalamic, lesions cause retrograde amnesia for objects in rats. NeuroReport 10:2853–2858

    Article  CAS  PubMed  Google Scholar 

  • Lashley KS (1929) Brain mechanisms and intelligence. University of Chicago Press, Chicago

    Google Scholar 

  • Lech RK, Suchan B (2013) The medial temporal lobe: memory and beyond. Behav Brain Res 254:45–49

    Article  PubMed  Google Scholar 

  • Lee AC, Bussey TJ, Murray EA, Saksida LM, Epstein RA, Kapur N, Hodges JR, Graham KS (2005) Perceptual deficits in amnesia: challenging the medial temporal lobe mnemonic view. Neuropsychologia 43:1–11

    Article  PubMed  Google Scholar 

  • Maaswinkel H, Jarrard LE, Whishaw IQ (1999) Hippocampectomized rats are impaired in homing by path integration. Hippocampus 9(5):553–561

    Article  CAS  PubMed  Google Scholar 

  • Malamut BL, Saunders RC, Mishkin M (1984) Monkeys with combined amygdalo-hippocampal lesions succeed in object discrimination learning despite 24-hour intertrial intervals. Behav Neurosci 98:759–769

    Article  CAS  PubMed  Google Scholar 

  • Malkova L, Mishkin M (1997) Memory for the location of objects after separate lesions of the hippocampus and parahippocampal cortex in Rhesus monkeys. Soc Neurosci Abstr 23:14

    Google Scholar 

  • Mandler G (1980) Recognizing: the judgment of previous occurrence. Psychol Rev 87:252–271

    Article  Google Scholar 

  • Martin SJ, Clark RE (2007) The rodent hippocampus and spatial memory: from synapses to systems. Cell Mol Life Sci 64(4):401–431

    Article  CAS  PubMed  Google Scholar 

  • McDonald RJ, White NM (1993) A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav Neurosci 127(6):835–853

    Article  Google Scholar 

  • McDougall W (1923) Outline of psychology. Scribners, New York

    Google Scholar 

  • McKee RD, Squire LR (1993) On the development of declarative memory. J Exp Psychol Learn Mem Cognit 19:397–404

    Article  CAS  Google Scholar 

  • Meunier M, Bachevalier J, Mishkin M, Murray EA (1993) Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J Neurosci 13:5418–5432

    CAS  PubMed  PubMed Central  Google Scholar 

  • Milner B (1962) In: Physiologie de l’hippocampe. Passouant P, editor. Centre National de la Recherche Scientifique, Paris, pp 257–272

    Google Scholar 

  • Milner B (1972) Disorders of learning and memory after temporal lobe lesions in man. Clin Neurosurg 19:421–446

    Article  CAS  PubMed  Google Scholar 

  • Milner B, Corkin S, Teuber HL (1968) Further analysis of the hippocampal amnesic syndrome: 14-year followup study of H.M. Neuropsychologia 6:215–234

    Article  Google Scholar 

  • Mishkin M (1978) Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus. Nature 273:297–298

    Article  CAS  PubMed  Google Scholar 

  • Mishkin M (1982) A memory system in the monkey. Philos Trans R Soc Lond B Biol Sci 298:83–95

    Article  CAS  PubMed  Google Scholar 

  • Mishkin M, Delacour J (1975) An analysis of short-term visual memory in the monkey. J Exp Psychol Anim Behav Process 1:326–334

    Article  CAS  PubMed  Google Scholar 

  • Mishkin M, Malamut B, Bachevalier J (1984) Memories and habits: two neural systems. In: Lynch G, McGaugh JL, Weinberger NM (eds) Neurobiology of human learning and memory. Guilford, New York, pp 65–77

    Google Scholar 

  • Moscovitch D, McAndrews MP (2002) Material-specific deficits in remembering in patients with unilateral temporal lobe epilepsy and excisions. Neuropsychologia 40:1335–1342

    Article  PubMed  Google Scholar 

  • Moser EI, Kropff E, Moser MB (2008) Place cells, grid cells, and the brain’s spatial representation system. Neuroscience 31(1):69

    CAS  Google Scholar 

  • Mumby DG, Pinel JP (1994) Rhinal cortex lesions and object recognition in rats. Behav Neurosci 108:11–18

    Article  CAS  PubMed  Google Scholar 

  • Mumby DG, Wood ER, Pinel JPJ (1992) Object-recognition memory is only mildly impaired in rats with lesions of the hippocampus and amygdala. Psychobiology 20:18–27

    Google Scholar 

  • Mumby DG, Pinel JPJ, Kornecook TJ, Shen MJ, Redila VA (1995) Memory deficits following lesions of hippocampus or amygdala in rat: assessment by an object-memory test battery. Psychobiology 23:26–36

    Google Scholar 

  • Mumby DG, Wood ER, Duva CA, Kornecook TJ, Pinel JPJ, Phillips AG (1996) Ischemia-induced object-recognition deficits in rats are attenuated by hippocampal ablation before or soon after ischemia. Behav Neurosci 110:266–281

    Article  CAS  PubMed  Google Scholar 

  • Mumby DG, Tremblay A, Lecluse V, Lehmann H (2005) Hippocampal damage and anterograde object-recognition in rats after long retention intervals. Hippocampus 15(8):1050–1056

    Article  PubMed  Google Scholar 

  • Murray EA, Mishkin M (1984) Severe tactual as well as visual memory deficits follow combined removal of the amygdala and hippocampus in monkeys. J Neurosci 4:2565–2580

    CAS  PubMed  PubMed Central  Google Scholar 

  • Murray EA, Mishkin M (1998) Object recognition and location memory in monkeys with excitotoxic lesions of the amygdala and hippocampus. J Neurosci 18:6568–6582

    CAS  PubMed  PubMed Central  Google Scholar 

  • Naya Y, Yoshida M, Miyashita Y (2003) Forward processing of long-term associative memory in monkey inferotemporal cortex. J Neurosci 23:2861–2871

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nemanic S, Alvarado MC, Bachevalier J (2004) The hippocampal/parahippocampal regions and recognition memory: insights from visual paired comparison versus object delayed nonmatching in monkeys. J Neurosci 24:2013–2026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press

    Google Scholar 

  • O’Brien N, Lehmann H, Lecluse V, Mumby DG (2006) Enhanced context-dependency of object recognition in rats with hippocampal lesions. Behav Brain Res 170(1):156–162

    Article  PubMed  Google Scholar 

  • Orbach J, Milner B, Rasmussen T (1960) Learning and retention in monkeys after amygdala-hippocampus resection. Arch Neurol 3:230–251

    Article  CAS  PubMed  Google Scholar 

  • Overman WH, Ormsby G, Mishkin M (1990) Picture recognition vs. picture discrimination learning in monkeys with medial temporal removals. Exp Brain Res 79:18–24

    Article  CAS  PubMed  Google Scholar 

  • Packard MG, Hirsh R, White NM (1989) Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems. J Neurosci 9:1465–1472

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parkinson JK, Murray EA, Mishkin MA (1988) A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects. J Neurosci 8:4159–4167

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parron C, Save E (2004) Evidence for entorhinal and parietal cortices involvement in path integration in the rat. Exp Brain Res 159(3):349–359

    Article  PubMed  Google Scholar 

  • Pascalis O, Hunkin NM, Holdstock JS, Isaac CL, Mayes AR (2004) Visual paired comparison performance is impaired in a patient with selective hippocampal lesions and relatively intact item recognition. Neuropsychologia 42:1293–1300

    Article  CAS  PubMed  Google Scholar 

  • Pavlov I (1927) Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex. (trans: Anrep GV). Oxford University Press, New York

    Google Scholar 

  • Prusky GT, Douglas RM, Nelson L, Shabanpoor A, Sutherland RJ (2004) Visual memory task for rats reveals an essential role for hippocampus and perirhinal cortex. PNAS 101(14):5064–5068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rampon C, Tang YP, Goodhouse J, Shimizu E, Kyin M, Tsien JZ (2000) Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat Neurosci 3(3):238–244

    Article  CAS  PubMed  Google Scholar 

  • Ramus SJ, Zola-Morgan S, Squire LR (1994) Effects of lesions of perirhinal cortex or parahippocampal cortex on memory in monkeys. Soc Neurosci Abs 20:1074

    Google Scholar 

  • Rossato JI, Bevilaqua LR, Myskiw JC, Medina JH, Izquierdo I, Cammarota M (2007) On the role of hippocampal protein synthesis in the consolidation and reconsolidation of object recognition memory. Learn Mem 14(1):36–46

    Article  PubMed  PubMed Central  Google Scholar 

  • Rotello CM, Macmillan NA, Reeder JA (2004) Sum-difference theory of remembering and knowing: a two-dimensional signal detection model. Psychol Rev 111:588–616

    Article  PubMed  Google Scholar 

  • Rotello CM, Macmillan NA, Reeder JA, Wong M (2005) The remember response: Subject to bias, graded, and not a process-pure indicator of recollection. Psychon Bull Rev 12:865–873

    Article  PubMed  Google Scholar 

  • Rotello CM, Macmillan NA., Hicks JL, Hautus M (2006) Interpreting the effects of response bias on remember-know judgments using signal-detection and threshold models. Mem Cog 34:1598–1614

    Article  Google Scholar 

  • Rothblat LA, Kromer LR (1991) Object recognition memory in the rat: the role of the hippocampus. Behav Brain Res 42:25–32

    Article  CAS  PubMed  Google Scholar 

  • Rugg MD, Yonelinas AP (2003) Human recognition memory: a cognitive neuroscience perspective. Trends Cogn Sci 7:313–319

    Article  PubMed  Google Scholar 

  • Ryle G (1949) The concept of mind. Hutchinson, San Francisco

    Google Scholar 

  • Sapiurka M, Squire LR, Clark RE (2016) Distinct roles of hippocampus and medial prefrontal cortex in spatial and nonspatial memory. Hippocampus 26(12):1515–1524

    Article  PubMed  PubMed Central  Google Scholar 

  • Save E, Guazzelli A, Poucet B (2001) Dissociation of the effects of bilateral lesions of the dorsal hippocampus and parietal cortex on path integration in the rat. Behav Neurosci 115(6):1212–1223

    Article  CAS  PubMed  Google Scholar 

  • Scoville WB (1954) The limbic lobe in man. J Neurosurg 11:64–66

    Article  CAS  PubMed  Google Scholar 

  • Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiat 20:11–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shrager Y, Gold JJ, Hopkins RO, Squire LR (2006) Intact visual perception in memory-impaired patients with medial temporal lobe lesions. J Neurosci 26:2235–2240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shrager Y, Kirwan CB, Squire LR (2008) Neural basis of the cognitive map: path integration does not require hippocampus or entorhinal cortex. Proc Natl Acad Sci 105(33):12034–12038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slotnick SD, Dodson CS (2005) Support for a continuous (single-process) model of recognition memory and source memory. Mem Cognit 33:151–170

    Article  PubMed  Google Scholar 

  • Smith DG, Duncan MJJ (2004) Testing theories of recognition memory by predicting performance across paradigms. J Exp Psychol Learn Mem Cogn 30:615–625

    Article  PubMed  Google Scholar 

  • Spellman T, Rigotti M, Ahmari SE, Fusi S, Gogos JA, Gordon JA (2015) Hippocampal-prefrontal input supports spatial encoding in working memory. Nature 522(7556):309–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Squire LR (1992) Memory and the hippocampus, a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195–231

    Article  CAS  PubMed  Google Scholar 

  • Squire LR (2009) The legacy of patient H.M. for neuroscience. Neuron 15:61(1):6–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Squire LR, Wixted JT (2011) The cognitive neuroscience of human memory since H.M. Annu Rev Neurosci 34:259–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Squire LR, Zola SM (1996) Structure and function of declarative and nondeclarative memory systems. Proc Natl Acad Sci 93(24):13515–13522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253:1380–1386

    Article  CAS  PubMed  Google Scholar 

  • Squire LR, Stark CEL, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279–306

    Article  CAS  PubMed  Google Scholar 

  • Squire LR, Wixted JT, Clark RE (2007) Recognition memory and the medial temporal lobe: a new perspective. Nat Rev Neurosci 8(11):872–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stefanacci L, Buffalo EA, Schmolck H, Squire LR (2000) Profound amnesia after damage to the medial temporal lobe: a neuroanatomical and neuropsychological profile of patient E.P. J Neurosci 20:7024–7036

    CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki WA (2009) Perception and the medial temporal lobe: evaluating the current evidence. Neuron 61(5):657–666

    Article  CAS  PubMed  Google Scholar 

  • Suzuki WA, Zola-Morgan S, Squire LR, Amaral DG (1993) Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. J Neurosci 13:2430–2451

    CAS  PubMed  PubMed Central  Google Scholar 

  • Teng E, Squire LR (1999) Memory for places learned long ago is intact after hippocampal damage. Nature 12;400(6745):675–677

    Article  CAS  PubMed  Google Scholar 

  • Teng E, Stefanacci L, Squire LR, Zola SM (2000) Contrasting effects on discrimination learning after hippocampal lesions and conjoint hippocampal-caudate lesions in monkeys. J Neurosci 20(10):3853–3863

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tulving E, Schacter DL (1990) Priming and human memory systems. Science 247:301–306

    Article  CAS  PubMed  Google Scholar 

  • Viskontas IV, Knowlton BJ, Steinmetz PN, Fried I (2006) Differences in mnemonic processing by neurons in the human hippocampus and parahippocampal regions. J Cogn Neurosci 18(10):1654–1662

    Article  PubMed  Google Scholar 

  • von Bekhterev M (1900) Demonstration eines Gehirns mit Zerstörung der vorderen und inneren Theile der Hirnrinde beider Schläfenlappen. Neurologisches Zeitblatt 19:990–991

    Google Scholar 

  • Wais PE, Wixted JT, Hopkins RO, Squire LR (2006) The hippocampus supports both the recollection and the familiarity components of recognition memory. Neuron 49(3):459–466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wais PE, Squire LR, Wixted JT (2010) In search of recollection and familiarity signals in the hippocampus. J Cogn Neurosci 22(1):109–123

    Article  PubMed  PubMed Central  Google Scholar 

  • Warrington EK, Taylor AM (1973) Immediate memory for faces: long- or short-term memory? Q J Exp Psychol 25(3):316–322

    Article  CAS  PubMed  Google Scholar 

  • Whishaw IQ, Hines DJ, Wallace DG (2001) Dead reckoning (path integration) requires the hippocampal formation: Evidence from spontaneous exploration and spatial learning tasks in light (allothetic) and dark (idiothetic) tests. Behav Brain Res 127(1–2):49–69

    Article  CAS  PubMed  Google Scholar 

  • Wiig KA, Bilkey DK (1995) Lesions of rat perirhinal cortex exacerbate the memory deficit observed following damage to the fimbria-fornix. Behav Neurosci 109:620–630

    Article  CAS  PubMed  Google Scholar 

  • Winograd T (1975) Frame representations and the declarative-procedural controversy. In: Bobrow D et al (eds) Representation and understanding: studies in cognitive science. Academic, New York, pp 185–210

    Chapter  Google Scholar 

  • Winters BD, Bussey TJ (2005) Transient inactivation of perirhinal cortex disrupts encoding, retrieval, and consolidation of object recognition memory. J Neurosci 25:52–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winters BD, Forwood SE, Cowell RA, Saksida LM, Bussey TJ (2004) Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: heterogeneity of function within the temporal lobe. J Neurosci 24:5901–5908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winters BD, Saksida LM, Bussey TJ (2008) Object recognition memory: neurobiological mechanisms of encoding, consolidation and retrieval. Neurosci Biobehav Rev 32(5):1055–1070

    Article  PubMed  Google Scholar 

  • Wixted JT (2007) Dual-process theory and signal-detection theory of recognition memory. Psychol Rev 114:152–176

    Article  PubMed  Google Scholar 

  • Wixted JT, Stretch V (2004) In defense of the signal detection interpretation of remember/know judgments. Psychon Bull Rev 11:616–641

    Article  PubMed  Google Scholar 

  • Wood ER, Dudchenko PA, Eichenbaum H (1999) The global record of memory in hippocampal neuronal activity. Nature 397:613–616

    Article  CAS  PubMed  Google Scholar 

  • Xiang JZ, Brown MW (1998) Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe. Neuropharmacology 37:657–676

    Article  CAS  PubMed  Google Scholar 

  • Yonelinas AP (1994) Receiver-operating characteristics in recognition memory: evidence for a dual-process model. J Exp Psychol Learn Mem Cogn 20:1341–1354

    Article  CAS  PubMed  Google Scholar 

  • Yonelinas AP, Kroll NE, Quamme JR, Lazzara MM, Sauve MJ, Widaman KF, Knight RT (2002) Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity. Nat Neurosci 5:1236–1241

    Article  CAS  PubMed  Google Scholar 

  • Zola SM, Squire LR, Teng E, Stefanacci L, Buffalo EA, Clark RE (2000) Impaired recognition memory in monkeys after damage limited to the hippocampal region. J Neurosci 20:451–463

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zola-Morgan S, Squire LR (1984) Preserved learning in monkeys with medial temporal lesions: Sparing of motor and cognitive skills. J Neurosci 4:1072–1085

    Google Scholar 

  • Zola-Morgan S, Squire LR (1985) Medial temporal lesions in monkeys impair memory on a variety of tasks sensitive to human amnesia. Behav Neurosci 99:22–34

    Article  CAS  PubMed  Google Scholar 

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Clark, R.E. ( 2017). Current Topics Regarding the Function of the Medial Temporal Lobe Memory System. In: Clark, R.E., Martin, S. (eds) Behavioral Neuroscience of Learning and Memory. Current Topics in Behavioral Neurosciences, vol 37. Springer, Cham. https://doi.org/10.1007/7854_2017_481

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