hippocampus and neocortex: recognition and spatial memory

CONEUR-885; NO. OF PAGES 6

Please cite this article in press as: Vann SD, Albasser MM. Hippocampus and neocortex: recognition and spatial memory, Curr Opin Neurobiol (2011), doi:10.1016/j.conb.2011.02.002

Available online at www.sciencedirect.com

Hippocampus and neocortex: recognition and spatial memorySeralynne D Vann and Mathieu M Albasser

Recognition and spatial memory are typically associated with

the perirhinal cortex and hippocampal formation, respectively.

Solely focusing on these structures for these specific

mnemonic functions may, however, be limiting progress in the

field. The distinction between these subdivisions of memory is

becoming less defined as, for example, hippocampal cells

traditionally considered to encode locations also encode

place–object associations. There is increasing evidence for the

involvement of overlapping networks of brain structures for

aspects of both spatial and recognitionmemory. Futuremodels

of spatial and recognition memory will have to extend beyond

the hippocampus and perirhinal cortex to incorporate a wider

network of cortical and subcortical structures.

AddressSchool of Psychology, Cardiff University, Cardiff, UK

Corresponding author: Vann, Seralynne D ([email protected])

Current Opinion in Neurobiology 2011, 21:1–6

This review comes from a themed issue onBehavioral and cognitive neuroscienceEdited by Ann Graybiel and Richard Morris

0959-4388/$ – see front matter# 2011 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.conb.2011.02.002

IntroductionThe neural processes that allow us to form episodicmemories, that is, remember events we experiencethroughout our lives, are still far from fully understood.Neuropsychological studies have been pivotal in identi-fying those brain structures that are necessary for formingnew memories but typically studies in animals arerequired to investigate these mnemonic processes withhigher anatomical resolution. There continues to be adebate as to whether the term episodic memory can evenbe applied to non-humans; this is particularly relevantwhen considering vivid experiences where rememberingcan give a sense of ‘re-living’ the event in a way that hasbeen likened to mental-time travel (see [1]). Whether ornot episodic memory is directly comparable acrossspecies, there are certainly aspects of episodic memorythat can be assessed in animals such as memory forobjects, spatial routes and locations, and spatiotemporalcontext. The recent use of convergent approaches toassess the neural substrates of both recognition memoryand spatial learning, including electrophysiological

recordings, immediate-early gene imaging, and lesiondisconnection studies, has identified an interactive net-work of regions that support these functions. In thisreview, we will discuss findings from recent studies thathave shed light on aspects of object recognition, spatialmemory, and how these two forms of memory are broughttogether. Recent findings will be put into the context of amore unified model of memory that focuses on inter-actions, rather than dissociations, between brain regions.

Recognition memoryOne component of memory is recognising whether youhave encountered someone or something before. Thisability can be assessed non-verbally by using a prefer-ential viewing paradigm that builds on the innate pre-ference of animals, including humans, to look at, orexplore, something novel. In rats, the spontaneous objectrecognition task has been used to assess the neural sub-strates of recognition memory [2] (see Figure 1). Whilethere is an ongoing debate about the extent to which thehippocampus is required for animals to exhibit normallevels of novel object exploration (see [3,4]), there is ageneral consensus that the perirhinal cortex contributes torecognition memory [5,6]. The inability of perirhinallesion rats to discriminate new objects from previouslyseen objects had been thought to result from animals notremembering the old object. In contrast, however,McTighe et al. [7] recently proposed that the poor per-formance was in fact a result of rats having a false memoryfor the novel object, that is, acting as if the novel objecthad been previously experienced, therefore exploring itless. The authors argue that the loss of the perirhinalcortex leaves animals unable to use the unique complexfeatures associated with the whole object and instead arelimited to using simpler stimulus features that are morelikely shared across objects thus resulting in false recog-nition [7]; this explanation is consistent with recentmodels that question the perceived dichotomy betweenmemory and perception (for a review see [8]). However, ifperirhinal lesion rats do treat novel objects as familiar, thisshould also be demonstrated during the sample phasewhere the animals are presented with previously unseenobjects. In fact, perirhinal lesion rats in both this study [7]and previous studies (e.g. [9,10]) correctly behave as if theobjects are novel as they show comparable levels of objectexploration to control rats during the sample phase; this‘false memory’ account cannot, therefore, provide a gen-eral mechanism for perirhinal lesion effects.

Extending the substrates of recognition memoryAlthough object recognition in rats has typically beenconsidered in terms of the visual domain, recent studies

www.sciencedirect.com Current Opinion in Neurobiology 2011, 21:1–6

http://dx.doi.org/10.1016/j.conb.2011.02.002

mailto:[email protected]


have modified the spontaneous object recognition para-digm (Figure 1) to show that rats can use non-visual cuesto discriminate novel objects [11,12]. Winters and Reid[12] then showed that rats could effectively combineobject information such that they could visually recognisean object that they had only previously experienced in thenon-visual domain (Figure 1a). Object recognition basedon these different streams of information, visual andtactile, requires the perirhinal cortex and posterior par-ietal cortex, respectively; consistent with findings fromhumans [13], both cortical regions interact to supporttactile-visual cross-modal object recognition [12].

While cross-modal object recognition studies havefocused on perirhinal-parietal cortex interactions, theuse of another paradigm, the bow-tie maze, has shedlight on perirhinal-hippocampal interactions for visualobject recognition. By combining a continuous object-recognition test in the bow-tie maze (Figure 1b) withimmediate-early gene imaging, the authors identified anetwork within the medial temporal lobe, including boththe perirhinal cortex and hippocampus, that was associ-ated with the exploration of novel objects [14]. A differentpattern emerged in subsequent lesion studies as peri-rhinal cortex lesions [15] but not hippocampal [11] norfornix lesions [11] impaired task performance. It, there-fore, appears that while the hippocampus may not berequired for object recognition is does form part of anextended network that is engaged by aspects of objectrecognition. The use of these convergent approaches mayhelp explain some of the apparently incongruent findingsin the literature (see [3,4]).

Space, place and navigationThe hippocampus has long been implicated in spatialmemory in both humans and animals [16]. Cells withinthe hippocampal formation contain a number of electro-physiological properties consistent with their role informing allocentric representations of space, includinghead-direction, place and grid cells [17,18]. Two recentstudies have shown how these electrophysiological prop-erties develop in very young rats from when they firstexplore outside of the nest [19,20]. The authors of bothstudies found that head-direction cells are the first tomature followed by place cells and then grid cells [19,20].The presence of adult-like head-direction cells in the pre-weanling rat suggests some aspects of spatial cognition,such as orientation, are innate or experience independent.The time-frame in which the different cell types reachmaturity has raised the possibility that direction infor-mation may be necessary for establishing place and gridcell networks [19,20]. While head-direction inputs mayprove to be crucial for place and grid cell development,this role is likely to be time-limited as lesions within thehead-direction system in adults typically have only a mildeffect on hippocampal place cell firing [21,22] and tests ofspatial memory [23]. The presence of grid (like) cells in anetwork of brain regions implicated in spatial cognitionand episodic memory in both humans [24!!] and rats [25]could reflect a wider role for these cells in memoryfunction [24!!].

In addition to location representation at the singlecell level, locations are also represented by distinctneural assemblies; studies in both rats and humans have

2 Behavioral and cognitive neuroscience



Figure 1

transparentbarriers

Sample Choice

(a) Y-Maze (b) Bow-Tie Maze (c) Circular-track

Current Opinion in Neurobiology

Recent modifications of the one-trial object recognition task [58] that are based on the premise that animals have an innate preference for novelty; this isdemonstrated by longer exploration times for previously unseen objects or object–place combinations. (a) Y-maze apparatus used to assess cross-modalobjection recognition memory. During the sample phase the rats explore replicas of the same object in the dark. After a delay, the rats are shown twofurther objects, one a replica of those shown during the sample phase and the other a new object. The objects are presented visually and a transparentbarrier prevents the non-visual exploration of the objects. Intact animals are able to visually discriminate objects that had previously only been experiencednon-visually, that is, they spend longer looking at the novel object. (b) The Bow-Tie maze allows rats to be run continuously on multiple trials of the object-recognition task [11,14] and, therefore, addresses some of the limitations associated with one-trial object recognition paradigms [2]. Rats are trained to runfrom one end of the maze to the other for sucrose rewards. The design is such that the novel object in any trial becomes the familiar object in thesubsequent trial. (c) Rats complete laps of the circular-track during which they encounter up to four objects in varying locations. Rats can encounterobjects in previously experienced locations as well as novel locations. By simultaneously recording within the hippocampus, Manns and Eichenbaum [37]were able to assess the rat’s memory for objects and object location at both a neural and behavioural level.

Current Opinion in Neurobiology 2011, 21:1–6 www.sciencedirect.com


identified patterns of neuronal firing within the hippo-campus that represent specific goal locations in both real[26!!] and virtual spatial environments [27!!]. It ispossible that sharp wave network oscillations within theseneural assemblies, both during learning and subsequentrest periods, are necessary for successful location memory[26!!]. In addition, activity in these neural assembliesbefore animals have encountered an environment (‘pre-play’) may benefit subsequent learning [28]. Consistentwith the apparent link between spatial and episodicmemory, distinct patterns of hippocampal activation, thatare stable over time, can also reflect specific episodicmemories [29]. The presence of neural representations ofthe spatial environment is not, however, sufficient forsuccessful place learning as Bast et al. recently demon-strated [30]. Rats with lesions of the intermediate hippo-campus were unable to learn new spatial locations rapidly,within a familiar environment, despite the persistence ofintact spatial representations and neuronal plasticity inthe septal hippocampus [30]. This study addresses theimportant, but often overlooked, distinction betweenforming accurate spatial representations and sub-sequently translating these representations into beha-vioural actions, such as navigation, the latter of whichrequires the intermediate hippocampus [30].

Putting things in contextWhile the traditional focus in animal research has beento assess either memory for objects or memory for places,a growing trend is to combine these different aspects ofmemory within the same task. This is arguably a morerealistic approach in terms of what animals instinctivelylearn and also more comparable to the combined com-ponents of human episodic memory [31,32]. Combiningmemory for objects and the contexts in which they occurin has also shifted the focus away from the moretraditional approach of studying single brain regions,to a more integrated approach where the emphasis ison interactions between multiple regions. Functionaldisconnections of brain regions, using crossed unilaterallesions or temporary inactivations, are particularly infor-mative for addressing these issues. Using this approachit appears that the perirhinal cortex interacts both withthe hippocampus [33] and with the medial prefrontalcortex to support learning about object–place associ-ations [34]; the acquisition of these associations requirescholinergic modulation of perirhinal-prefrontal networkinteractions [35].

A number of elegant studies have combined the use ofintracranial recordings with behaviour to identify furtherhow hippocampal cells ‘learn’ about object–place orobject–context associations. Changes in hippocampal cellfiring are found when rats associate a specific object with aspecific place or context both when the associations arerewarded [36] and non-rewarded [37] (Figure 1c). Record-ings made while rats performed an item–context associ-

ative task revealed item–context specific hippocampalfiring that developed over training such that greaterproportions of firing cells were found once an animalhad learnt to identify the correct item-position pairing[36]. Of particular interest is that these associative repres-entations are built on previously formed representationsof the space and context in which they are learning [36];this finding brings together those models of hippocampalfunction that emphasise its role in either spatial [16] orrelational [38] learning. Accurate performance on theitem–context associative task is not only associated withmodified hippocampal cell firing but also strongercoupling between theta and gamma oscillations in theCA3 field of the hippocampus. These changes in theta-gamma interactions may provide a mechanism for theeffective encoding of distinct episodes [39].

There is growing evidence for automatic encoding ofobject–context associations within the hippocampus fromboth lesion [40] and immediate-early gene studies [14].The rapid acquisition of new associations can be assistedby the use of schemas [41]; this is consistent with objectassociations and location learning being built on pre-existing hippocampal spatial representations, as theserepresentations form a neural framework onto whichthese additional associations can be rapidly acquired.

Extending the substrates of spatial memoryAlthough the hippocampus is often the main focus ofspatial memory it is important to consider it at it as part ofa wider network of inter-connected brain regions that alsocontribute to mnemonic function [42,43]. There is emer-ging evidence for distinct yet complementary roles for thehippocampus and prefrontal cortex both in rats [44] andhumans [45]; interactions between these structures,which may be of particular importance for the recollectionof contexts (e.g. source memory) and associative memory,appear to involve theta oscillations [46,47]. It, therefore,appears that the hippocampus, perirhinal cortex andprefrontal cortex all form part of the neural system thatsupports memory for items and the contexts in which theyoccur, (e.g., [33,34]).

The retrosplenial cortex has also been identified as apotentially important structure for aspects of spatial andepisodic memory, consistent with its central positionamong other key memory structures including theanterior thalamic nuclei, hippocampal formation,posterior parietal cortex [48] and prefrontal cortex [49].One possibility is that the retrosplenial cortex is necess-ary for both scene construction [50] and the subsequentmanipulation of the scenes between different view-points, such as egocentric or world-centred [49,51](Figure 2). In addition to those cortical sites alreadydiscussed, recent findings from both human and ratstudies have reinforced the importance of the medialdiencephalon, that is, the mammillary bodies and

Hippocampus and neocortex: recognition and spatial memory Vann and Albasser 3





anterior thalamic nuclei, for memory [52] and for normalhippocampal function [53]; preliminary findings alsohighlight a role for the limbicmidbrain in spatial memoryprocesses [54,55]. To advance further our current un-derstanding of the neural systems that support memory,future models will need to extend beyond hippocampal-based memory systems and incorporate the contributionof these other cortical and subcortical regions.

ConclusionsSpatial and recognition memory have typically beenconsidered to be distinct types of memory that are sup-ported by separate brain regions: the hippocampal for-mation and perirhinal cortex, respectively. However, anoveremphasis on these specific neural structures and theirrespective importance for spatial and recognition memorymay impede progress in the field. Recent research hasbrought together divergent models of memory, by usingbehavioural tests that combine aspects of spatial andobject memory and by appreciating the importance ofinteractions between structures rather than simple dis-sociations [56]. The use of novel electrophysiologicalrecording techniques [57!!], and convergent approachesthat allow multiple brain regions to be examined simul-taneously, will assist with the technically more demand-ing challenge of understanding interactions between

several brain regions as opposed to focusing on thecontributions of single structures. This will be a necessarystep in advancing current models of spatial and recog-nition memory to incorporate the contributions of a widernetwork of structures.

AcknowledgementsSDV is funded by a Wellcome Trust Senior Research Fellowship in BasicBiomedical Science [WT090954AIA]; MMA is funded by a Wellcome Trustresearch grant [WT087855]. The authors wish to thank Andrew Nelson andJohn Aggleton for their extremely helpful comments on the manuscript.

References and recommended readingPapers of particular interest, published within the annual period ofreview, have been highlighted as:

! of special interest!! of outstanding interest

1. Tulving E: Episodic memory: from mind to brain. Annu RevPsychol 2002, 53:1-25.

2. Ennaceur A: One-trial object recognition in rats and mice:methodological and theoretical issues. Behav Brain Res 2010,215:244-254.

3. Brown MW, Aggleton JP: Recognition memory: what are theroles of the perirhinal cortex and hippocampus? Nat RevNeurosci 2001, 2:51-61.

4. Clark RE, Squire LR: An animal model of recognition memoryandmedial temporal lobe amnesia: history and current issues.Neuropsychologia 2010, 48:2234-2244.




Figure 2

ATN

Prefrontal cortex

Parietal cortex

Perirhinal cortex

Hippocampus Parahippoacmpal

Occipital cortex

Retrosplenial cortex

Executive, scenemanipulation

Object-basedinformation

Head direction,theta

Body-orientedinformation

Egocentricframework

Allocentricframework

Scene translation

Visual information

Scene-basedinformation

Event within a scene,scene construction

Current Opinion in Neurobiology

How the retrosplenial cortex might contribute to episodic and spatial memory by manipulating and translating information between differentframeworks, for example, between egocentric (self-centred) and allocentric (world-centred) views [51]. Figure taken from [49]; ATN, anterior thalamicnucleus.



5. Winters BD, Saksida LM, Bussey TJ: Implications of animalobject memory research for human amnesia.Neuropsychologia 2010, 48:2251-2261.

6. Brown MW, Warburton EC, Aggleton JP: Recognition memory:material, processes, and substrates. Hippocampus 2010,20:1228-1244.

7. McTighe SM, Cowell RA, Winters BD, Bussey TJ, Saksida LM:Paradoxical false memory for objects after brain damage.Science 2010, 330:1408-1410.

8. Graham KS, Barense MD, Lee AC: Going beyond LTM in theMTL: a synthesis of neuropsychological and neuroimagingfindings on the role of themedial temporal lobe inmemory andperception. Neuropsychologia 2010, 48:831-853.

9. Mumby DG, Piterkin P, Lecluse V, Lehmann H: Perirhinal cortexdamage and anterograde object-recognition in rats after longretention intervals. Behav Brain Res 2007, 185:82-87.

10. Bartko SJ, Winters BD, Cowell RA, Saksida LM, Bussey TJ:Perirhinal cortex resolves feature ambiguity in configuralobject recognition and perceptual oddity tasks. Learn Mem2007, 14:821-832.

11. Albasser MM, Chapman RJ, Amin E, Iordanova MD, Vann SD,Aggleton JP: New behavioral protocols to extend ourknowledge of rodent object recognition memory. Learn Mem2010, 17:407-419.

12. Winters BD, Reid JM: A distributed cortical representationunderlies crossmodal object recognition in rats. J Neurosci2010, 30:6253-6261.

13. Holdstock JS, Hocking J, Notley P, Devlin JT, Price CJ:Integrating visual and tactile information in the perirhinalcortex. Cereb Cortex 2009, 19:2993-3000.

14. Albasser MM, Poirier GL, Aggleton JP: Qualitatively differentmodes of perirhinal-hippocampal engagement when ratsexplore novel vs. familiar objects as revealed by c-Fosimaging. Eur J Neurosci 2010, 31:134-147.

15. Horne MR, Iordanova MD, Albasser MM, Aggleton JP, Honey RC,Pearce JM: Lesions of the perirhinal cortex do not impairintegration of visual and geometric information in rats. BehavNeurosci 2010, 124:311-320.

16. O’Keefe J, Nadel L: The Hippocampus as a Cognitive Map.Oxford: Clarendon Press; 1978.

17. Moser EI, Kropff E, Moser MB: Place cells, grid cells, and thebrain’s spatial representation system. Annu Rev Neurosci 2008,31:69-89.

18. Derdikman D, Moser EI: Amanifold of spatial maps in the brain.Trends Cogn Sci 2010, 14:561-569.

19. Wills TJ, Cacucci F, Burgess N, O’Keefe J: Development of thehippocampal cognitive map in preweanling rats. Science 2010,328:1573-1576.

20. Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL,Witter MP, Moser EI, Moser MB: Development of the spatialrepresentation system in the rat. Science 2010,328:1576-1580.

21. Calton JL, Stackman RW, Goodridge JP, Archey WB,Dudchenko PA, Taube JS: Hippocampal place cell instabilityafter lesions of the head direction cell network. J Neurosci2003, 23:9719-9731.

22. Sharp PE, Koester K: Lesions of the mammillary body regionseverely disrupt the cortical head direction, but not place cellsignal. Hippocampus 2008, 18:766-784.

23. Vann SD: Transient spatial deficit associated with bilaterallesions of the lateral mammillary nuclei. Eur J Neurosci 2005,21:820-824.

24.!!

Doeller CF, Barry C, Burgess N: Evidence for grid cells in ahuman memory network. Nature 2010, 463:657-661.

The authors found the mean firing directions of directional grid cells inrats to be aligned with grids. fMRI in humans exploring virtual environ-ment revealed a comparable signal in a network of regions. Networkincluded entorhinal/subicular, posterior and medial parietal, lateral

temporal and medial prefrontal areas. The coherence of the directionalsignal across entorhinal cortex correlated with spatial memory perfor-mance.

25. Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP,Moser EI, Moser MB: Grid cells in pre- and parasubiculum. NatNeurosci 2010, 13:987-994.

26.!!

Dupret D, O’Neill J, Pleydell-Bouverie B, Csicsvari J: Thereorganization and reactivation of hippocampal maps predictspatial memory performance. Nat Neurosci 2010, 13:995-1002.

The authors recorded hippocampal network activity during the acquisi-tion, consolidation and recall of a spatial memory task. Place related firingpatterns in CA1were reorganised to represent new goal location. Firingpatterns associated with sharp wave/ripple network oscillations pre-dicted memory performance. Results suggest sharp wave/ripple networkoscillations may contribute to spatial memory consolidation.

27.!!

Hassabis D, Chu C, Rees G, Weiskopf N, Molyneux PD,Maguire EA: Decoding neuronal ensembles in the humanhippocampus. Curr Biol 2009, 19:546-554.

Participants navigated a virtual environment while undergoing high reso-lution fMRI. The authors decoded activity across populations of neuronsin human medial temporal lobe. The location of the participant within thevirtual environment could be reliably predicted from pattern of activity inthe hippocampus. Dissociation was found between activity in the hippo-campus and parahippocampal gyrus.

28. Dragoi G, Tonegawa S: Preplay of future place cell sequencesby hippocampal cellular assemblies. Nature 2010.

29. Chadwick MJ, Hassabis D, Weiskopf N, Maguire EA: Decodingindividual episodic memory traces in the humanhippocampus. Curr Biol 2010, 20:544-547.

30. Bast T, Wilson IA, Witter MP, Morris RG: From rapid placelearning to behavioral performance: a key role for theintermediate hippocampus. PLoS Biol 2009, 7:e1000089.

31. Clayton NS, Dickinson A: Episodic-like memory during cacherecovery by scrub jays. Nature 1998, 395:272-274.

32. Eacott MJ, Norman G: Integratedmemory for object, place, andcontext in rats: a possible model of episodic-like memory? JNeurosci 2004, 24:1948-1953.

33. Jo YS, Lee I: Disconnection of the hippocampal-perirhinalcortical circuits severely disrupts object–place pairedassociative memory. J Neurosci 2010, 30:9850-9858.

34. Barker GR, Bird F, Alexander V, Warburton EC: Recognitionmemory for objects, place, and temporal order: adisconnection analysis of the role of the medial prefrontalcortex and perirhinal cortex. J Neurosci 2007, 27:2948-2957.

35. Barker GR,Warburton EC:Critical role of the cholinergic systemfor object-in-place associative recognition memory. LearnMem 2009, 16:8-11.

36. Komorowski RW, Manns JR, Eichenbaum H: Robust conjunctiveitem-place coding by hippocampal neurons parallels learningwhat happens where. J Neurosci 2009, 29:9918-9929.

37. Manns JR, Eichenbaum H: A cognitive map for object memoryin the hippocampus. Learn Mem 2009, 16:616-624.

38. Cohen NJ, Eichenbaum H: Memory, Amnesia, and theHippocampal System. Cambridge, MA, London: MIT; 1993.

39. Tort AB, Komorowski RW, Manns JR, Kopell NJ, Eichenbaum H:Theta-gamma coupling increases during the learning of item–context associations. Proc Natl Acad Sci USA 2009,106:20942-20947.

40. Piterkin P, Cole E, Cossette MP, Gaskin S, Mumby DG: A limitedrole for the hippocampus in the modulation of novel-objectpreference by contextual cues. Learn Mem 2008,15:785-791.

41. Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA,Wood ER, Witter MP, Morris RG: Schemas and memoryconsolidation. Science 2007, 316:76-82.

42. Parent MA, Wang L, Su J, Netoff T, Yuan LL: Identification of thehippocampal input to medial prefrontal cortex in vitro. CerebCortex 2010, 20:393-403.

Hippocampus and neocortex: recognition and spatial memory Vann and Albasser 5





43. van Strien NM, Cappaert NL, Witter MP: The anatomy ofmemory: an interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 2009, 10:272-282.

44. DeVito LM, Eichenbaum H: Distinct contributions of thehippocampus and medial prefrontal cortex to the ‘‘what-where-when’’ components of episodic-like memory in mice.Behav Brain Res 2010, 215:318-325.

45. Zeithamova D, Preston AR: Flexible memories: differential rolesfor medial temporal lobe and prefrontal cortex in cross-episode binding. J Neurosci 2010, 30:14676-14684.

46. Jones MW, Wilson MA: Theta rhythms coordinatehippocampal-prefrontal interactions in a spatial memory task.PLoS Biol 2005, 3:e402.

47. Anderson KL, Rajagovindan R, Ghacibeh GA, Meador KJ, Ding M:Theta oscillations mediate interaction between prefrontalcortex and medial temporal lobe in human memory. CerebCortex 2010, 20:1604-1612.

48. Calton JL, Taube JS: Where am I and how will I get there fromhere? A role for posterior parietal cortex in the integration ofspatial information and route planning. Neurobiol Learn Mem2009, 91:186-196.

49. Vann SD, Aggleton JP, Maguire EA: What does the retrosplenialcortex do? Nat Rev Neurosci 2009, 10:792-802.

50. Summerfield JJ, Hassabis D, Maguire EA: Differentialengagement of brain regions within a ‘core’ network duringscene construction. Neuropsychologia 2010, 48:1501-1509.

51. Byrne P, Becker S, Burgess N: Remembering the past andimagining the future: a neural model of spatial memory andimagery. Psychol Rev 2007, 114:340-375.

52. Vann SD, Tsivilis D, Denby CE, Quamme JR, Yonelinas AP,Aggleton JP, Montaldi D, Mayes AR: Impaired recollection butspared familiarity in patients with extended hippocampalsystem damage revealed by 3 convergent methods. Proc NatlAcad Sci USA 2009, 106:5442-5447.

53. Vann SD, Albasser MM: Hippocampal, retrosplenial, andprefrontal hypoactivity in a model of diencephalicamnesia: evidence towards an interdependent subcortical–cortical memory network. Hippocampus 2009,19:1090-1102.

54. Vann SD: Re-evaluating the role of the mammillary bodies inmemory. Neuropsychologia 2010, 48:2316-2327.

55. Vann SD: Gudden’s ventral tegmental nucleus is vital formemory: re-evaluating diencephalic inputs for amnesia. Brain2009, 132:2372-2384.

56. Henson RN, Gagnepain P: Predictive, interactive multiplememory systems. Hippocampus 2010, 20:1315-1326.

57.!!

Harvey CD, Collman F, Dombeck DA, Tank DW: Intracellulardynamics of hippocampal place cells during virtual navigation.Nature 2009, 461:941-946.

The authors developed a novel virtual-reality system that allowed themto make in vivo whole cell recordings in mice. Mice were able toperform spatial behaviours by using a spherical ball that interactedwith a computer generated environment. The authors used this tech-nique to identify subthreshold features and intracellular dynamics ofplace fields.

58. Ennaceur A, Delacour J: A new one-trial test for neurobiologicalstudies of memory in rats. 1: Behavioral data. Behav Brain Res1988, 31:47-59.






hippocampus and neocortex: recognition and spatial memory

Documents