Segregating cognitive functions within hippocampal formation: A quantitative meta‐analysis on spatial navigation and episodic memory

The most important cognitive domains where hippocampal formation is crucially involved are navigation and memory. Some evidence suggests that different hippocampal subregions mediate these domains. However, a quantitative meta‐analysis on neuroimaging studies of spatial navigation versus memory is lacking. By means of activation likelihood estimation (ALE), we investigate concurrence of brain regions activated during spatial navigation encoding and retrieval as well as during episodic memory encoding and retrieval tasks in humans. During encoding in spatial navigation, activity was located in more posterior regions of the hippocampal formation, whereas episodic memory encoding was located in more anterior regions. Retrieval in spatial navigation was more strongly lateralized to the right compared to episodic memory retrieval. Within studies on spatial navigation retrieval, immediate recall was located more posterior and delayed recall more anterior. Overlap between concurrence of activation in spatial navigation and episodic memory was rather limited in comparison to uniquely involved regions. This argues in favor of two distinct networks, one for spatial navigation the other for episodic memory within the hippocampal formation. Hum Brain Mapp 35:1129–1142, 2014. © 2013 Wiley Periodicals, Inc.

[1]  J. Peters,et al.  Direct Evidence for Domain-Sensitive Functional Subregions in Human Entorhinal Cortex , 2012, The Journal of Neuroscience.

[2]  S. Hanson,et al.  Dynamic changes in the medial temporal lobe during incidental learning of object-location associations. , 2012, Cerebral cortex.

[3]  Arne D. Ekstrom,et al.  Dissociations within human hippocampal subregions during encoding and retrieval of spatial information , 2011, Hippocampus.

[4]  Lisa M. Giocomo,et al.  Cellular dynamical mechanisms for encoding the time and place of events along spatiotemporal trajectories in episodic memory , 2010, Behavioural Brain Research.

[5]  E. Moser,et al.  A manifold of spatial maps in the brain , 2010, Trends in Cognitive Sciences.

[6]  Jun Liu,et al.  A virtual reality-based FMRI study of reward-based spatial learning , 2010, Neuropsychologia.

[7]  P. Rodríguez.  Human navigation that requires calculating heading vectors recruits parietal cortex in a virtual and visually sparse water maze task in fMRI. , 2010, Behavioral neuroscience.

[8]  Christian F. Doeller,et al.  Lateralized human hippocampal activity predicts navigation based on sequence or place memory , 2010, Proceedings of the National Academy of Sciences.

[9]  Thackery I. Brown,et al.  Which Way Was I Going? Contextual Retrieval Supports the Disambiguation of Well Learned Overlapping Navigational Routes , 2010, The Journal of Neuroscience.

[10]  Patrick Péruch,et al.  Route and survey processing of topographical memory during navigation , 2010, Psychological research.

[11]  Jason B. Mattingley,et al.  Dissociable neural circuits for encoding and retrieval of object locations during active navigation in humans , 2010, NeuroImage.

[12]  C. Pennartz,et al.  Dissociating the “retrieval success” regions of the brain: Effects of retrieval delay , 2010, Neuropsychologia.

[13]  J. Baudewig,et al.  The human parahippocampal cortex subserves egocentric spatial learning during navigation in a virtual maze , 2010, Neurobiology of Learning and Memory.

[14]  Hong-wei Dong,et al.  Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? , 2010, Neuron.

[15]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

[16]  Jean-Christophe Cassel,et al.  Hippocampal‐dependent spatial memory functions might be lateralized in rats: An approach combining gene expression profiling and reversible inactivation , 2009, Hippocampus.

[17]  P. Rodríguez,et al.  Neural decoding of goal locations in spatial navigation in humans with fMRI , 2009, Human brain mapping.

[18]  D. Hassabis,et al.  Decoding Neuronal Ensembles in the Human Hippocampus , 2009, Current Biology.

[19]  F. Woermann,et al.  Neural correlates of episodic and semantic memory retrieval in borderline personality disorder: An fMRI study , 2009, Psychiatry Research: Neuroimaging.

[20]  H. Eichenbaum,et al.  Towards a functional organization of the medial temporal lobe memory system: Role of the parahippocampal and medial entorhinal cortical areas , 2008, Hippocampus.

[21]  R. Kessels,et al.  How the brain remembers and forgets where things are: The neurocognition of object–location memory , 2008, Neuroscience & Biobehavioral Reviews.

[22]  S. Shergill,et al.  An fMRI study of verbal episodic memory encoding in amnestic mild cognitive impairment , 2008, Cortex.

[23]  Emilio Kropff,et al.  Place cells, grid cells, and the brain's spatial representation system. , 2008, Annual review of neuroscience.

[24]  C. Schmidt,et al.  Partially segregated neural networks for spatial and contextual memory in virtual navigation , 2008, Hippocampus.

[25]  Christopher J. Fox,et al.  Detection of unexpected events during spatial navigation in humans: bottom‐up attentional system and neural mechanisms , 2008, The European journal of neuroscience.

[26]  Daniel L. Schacter,et al.  Remembering the specific visual details of presented objects: Neuroimaging evidence for effects of emotion , 2007, Neuropsychologia.

[27]  L. Swanson,et al.  Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex , 2007, Brain Research Reviews.

[28]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

[29]  Tilo Kircher,et al.  Wechsler Memory Scale Revised Edition: Neural correlates of the visual paired associates subtest adapted for fMRI , 2007, Brain Research.

[30]  Mark D'Esposito,et al.  Efficiency of the prefrontal cortex during working memory in attention-deficit/hyperactivity disorder. , 2007, Journal of the American Academy of Child and Adolescent Psychiatry.

[31]  Cheryl L. Grady,et al.  Common and Unique Neural Activations in Autobiographical, Episodic, and Semantic Retrieval , 2007, Journal of Cognitive Neuroscience.

[32]  D. Hassabis,et al.  Deconstructing episodic memory with construction , 2007, Trends in Cognitive Sciences.

[33]  J. Taube.  The head direction signal: origins and sensory-motor integration. , 2007, Annual review of neuroscience.

[34]  J. Lagopoulos,et al.  An event-related functional MRI study of working memory in euthymic bipolar disorder. , 2007, Journal of psychiatry & neuroscience : JPN.

[35]  Nick F. Ramsey,et al.  Effects of frequent cannabis use on hippocampal activity during an associative memory task , 2007, European Neuropsychopharmacology.

[36]  R. Buckner,et al.  Self-projection and the brain , 2007, Trends in Cognitive Sciences.

[37]  M. Petrides,et al.  Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps , 2007, The European journal of neuroscience.

[38]  E. Maguire,et al.  London taxi drivers and bus drivers: A structural MRI and neuropsychological analysis , 2006, Hippocampus.

[39]  G. E. Alexander,et al.  Activation of brain regions vulnerable to Alzheimer's disease: The effect of mild cognitive impairment , 2006, Neurobiology of Aging.

[40]  R. Cabeza,et al.  Triple dissociation in the medial temporal lobes: recollection, familiarity, and novelty. , 2006, Journal of neurophysiology.

[41]  C. Kentros,et al.  Hippocampal place cells: The “where” of episodic memory? , 2006, Hippocampus.

[42]  T. Ohnishi,et al.  Navigation ability dependent neural activation in the human brain: An fMRI study , 2006, Neuroscience Research.

[43]  Eleanor A. Maguire,et al.  Thoughts, behaviour, and brain dynamics during navigation in the real world , 2006, NeuroImage.

[44]  S. Resnick,et al.  Age differences in the neural systems supporting human allocentric spatial navigation , 2006, Neurobiology of Aging.

[45]  Ulrike Halsband,et al.  Learning in trance: Functional brain imaging studies and neuropsychology , 2006, Journal of Physiology-Paris.

[46]  T. Kishi,et al.  Topographical projection from the hippocampal formation to the amygdala: A combined anterograde and retrograde tracing study in the rat , 2006, The Journal of comparative neurology.

[47]  C. Degueldre,et al.  Sleep after spatial learning promotes covert reorganization of brain activity. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[48]  G. Winocur,et al.  The cognitive neuroscience of remote episodic, semantic and spatial memory , 2006, Current Opinion in Neurobiology.

[49]  C. Forn,et al.  Memory lateralization with 2 functional MR imaging tasks in patients with lesions in the temporal lobe. , 2006, AJNR. American journal of neuroradiology.

[50]  Sterling C. Johnson,et al.  Task-dependent posterior cingulate activation in mild cognitive impairment , 2006, NeuroImage.

[51]  May-Britt Moser,et al.  Place cells, spatial maps and the population code for memory , 2005, Current Opinion in Neurobiology.

[52]  S. Heckers,et al.  Hippocampal activation during processing of previously seen visual stimulus pairs , 2005, Psychiatry Research: Neuroimaging.

[53]  Angela M. Uecker,et al.  ALE meta‐analysis: Controlling the false discovery rate and performing statistical contrasts , 2005, Human brain mapping.

[54]  Martin Lepage,et al.  Neural Correlates of Memory for Items and for Associations: An Event-related Functional Magnetic Resonance Imaging Study , 2005, Journal of Cognitive Neuroscience.

[55]  B. Knowlton,et al.  A Dissociation of Encoding and Retrieval Processes in the Human Hippocampus , 2005, The Journal of Neuroscience.

[56]  C. Büchel,et al.  Dissociable Retrosplenial and Hippocampal Contributions to Successful Formation of Survey Representations , 2005, The Journal of Neuroscience.

[57]  Roberto Cabeza,et al.  Neural Correlates of Relational Memory: Successful Encoding and Retrieval of Semantic and Perceptual Associations , 2005, The Journal of Neuroscience.

[58]  R. Todd Constable,et al.  Activation of human hippocampal formation reflects success in both encoding and cued recall of paired associates , 2005, NeuroImage.

[59]  Todd S Woodward,et al.  The influence of working memory load on phase specific patterns of cortical activity. , 2004, Brain research. Cognitive brain research.

[60]  H. Fukuyama,et al.  Neural substrates of the performance of an auditory verbal memory: between-subjects analysis by fMRI , 2004, Brain Research Bulletin.

[61]  Daniela Montaldi,et al.  Recalling spatial information as a component of recently and remotely acquired episodic or semantic memories: an fMRI study. , 2004, Neuropsychology.

[62]  J. Rawlins,et al.  Regional dissociations within the hippocampus—memory and anxiety , 2004, Neuroscience & Biobehavioral Reviews.

[63]  Mark D'Esposito,et al.  A functional MRI study of the influence of practice on component processes of working memory , 2004, NeuroImage.

[64]  Verner P Bingman,et al.  Lateralization of spatial learning in the avian hippocampal formation. , 2004, Behavioral neuroscience.

[65]  E. Tulving.  Episodic memory: from mind to brain. , 2002, Annual review of psychology.

[66]  Hans-Jochen Heinze,et al.  Different cortical activations for subjects using allocentric or egocentric strategies in a virtual navigation task , 2004, Neuroreport.

[67]  Rainer Goebel,et al.  Cortical capacity constraints for visual working memory: dissociation of fMRI load effects in a fronto-parietal network , 2003, NeuroImage.

[68]  Russell A. Poldrack,et al.  Putting names to faces: Successful encoding of associative memories activates the anterior hippocampal formation , 2003, NeuroImage.

[69]  M. Petrides,et al.  Cognitive Strategies Dependent on the Hippocampus and Caudate Nucleus in Human Navigation: Variability and Change with Practice , 2003, The Journal of Neuroscience.

[70]  Stephan Felber,et al.  An FMRI study of episodic encoding and recognition of words in patients with schizophrenia in remission. , 2003, The American journal of psychiatry.

[71]  E. Maguire,et al.  The Well-Worn Route and the Path Less Traveled Distinct Neural Bases of Route Following and Wayfinding in Humans , 2003, Neuron.

[72]  S. Engel,et al.  Dynamics of the Hippocampus During Encoding and Retrieval of Face-Name Pairs , 2003, Science.

[73]  Neil Burgess,et al.  The hippocampus, space, and viewpoints in episodic memory , 2002, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[74]  E. Maguire,et al.  The Human Hippocampus and Spatial and Episodic Memory , 2002, Neuron.

[75]  Paul J Reber,et al.  Comparing the brain areas supporting nondeclarative categorization and recognition memory. , 2002, Brain research. Cognitive brain research.

[76]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[77]  M Teräs,et al.  PET studies on the memory processing of word pairs in bilingual Finnish–English subjects , 2002, Behavioural Brain Research.

[78]  T. Kimura,et al.  Mental navigation in humans is processed in the anterior bank of the parieto-occipital sulcus , 2002, Neuroscience Letters.

[79]  J. Gabrieli,et al.  Neural Correlates of Encoding Space from Route and Survey Perspectives , 2002, The Journal of Neuroscience.

[80]  E. Maguire,et al.  Neurodevelopmental Aspects of Spatial Navigation: A Virtual Reality fMRI Study , 2002, NeuroImage.

[81]  M. Baulac,et al.  Anatomy of verbal memory: a functional MRI study , 2002, Surgical and Radiologic Anatomy.

[82]  B R Rosen,et al.  Encoding novel face‐name associations: A functional MRI study , 2001, Human brain mapping.

[83]  J B Poline,et al.  Human cortical networks for new and familiar sequences of saccades. , 2001, Cerebral cortex.

[84]  A. R. McIntosh,et al.  An Examination of the Effects of Stimulus Type, Encoding Task, and Functional Connectivity on the Role of Right Prefrontal Cortex in Recognition Memory , 2001, NeuroImage.

[85]  Anthony Randal McIntosh,et al.  Transperceptual Encoding and Retrieval Processes in Memory: A PET Study of Visual and Haptic Objects , 2001, NeuroImage.

[86]  S. Petersen,et al.  Direct Comparison of Prefrontal Cortex Regions Engaged by Working and Long-Term Memory Tasks , 2001, NeuroImage.

[87]  A. Alavi,et al.  Effect of schizophrenia on frontotemporal activity during word encoding and recognition: a PET cerebral blood flow study. , 2001, The American journal of psychiatry.

[88]  Dick J. Veltman,et al.  Parahippocampal Activation during Successful Recognition of Words: A Self-Paced Event-Related fMRI Study , 2001, NeuroImage.

[89]  T W Picton,et al.  Comparative electrophysiological and hemodynamic measures of neural activation during memory‐retrieval , 2001, Human brain mapping.

[90]  A R McIntosh,et al.  Episodic encoding and recognition of pictures and words: role of the human medial temporal lobes. , 2000, Acta psychologica.

[91]  S. Bricogne,et al.  Neural Correlates of Topographic Mental Exploration: The Impact of Route versus Survey Perspective Learning , 2000, NeuroImage.

[92]  S. Petersen,et al.  Memory's echo: vivid remembering reactivates sensory-specific cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[93]  A. Ylinen,et al.  Reciprocal Connections between the Amygdala and the Hippocampal Formation, Perirhinal Cortex, and Postrhinal Cortex in Rat: A Review , 2000, Annals of the New York Academy of Sciences.

[94]  R. Burwell.  The Parahippocampal Region: Corticocortical Connectivity , 2000, Annals of the New York Academy of Sciences.

[95]  Hanna Damasio,et al.  The neuroanatomical correlates of route learning impairment , 2000, Neuropsychologia.

[96]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[97]  Robert E. Hampson,et al.  Distribution of spatial and nonspatial information in dorsal hippocampus , 1999, Nature.

[98]  D. Schmidt,et al.  Neuronal correlates of encoding and retrieval in episodic memory during a paired-word association learning task: a functional magnetic resonance imaging study , 1999, Experimental Brain Research.

[99]  J. Taylor,et al.  Episodic retrieval activates the precuneus irrespective of the imagery content of word pair associates. A PET study. , 1999, Brain : a journal of neurology.

[100]  H. Müller-Gärtner,et al.  Encoding and retrieval in declarative learning: a positron emission tomography study , 1998, Behavioural Brain Research.

[101]  S. Taylor,et al.  The Effect of Emotional Content on Visual Recognition Memory: A PET Activation Study , 1998, NeuroImage.

[102]  Olaf B. Paulson,et al.  Brain Activation during Word Identification and Word Recognition , 1998, NeuroImage.

[103]  Alan C. Evans,et al.  A role for the hippocampal formation in implicit memory: a 3‐D PET study , 1998, Neuroreport.

[104]  Richard S. J. Frackowiak,et al.  Knowing where and getting there: a human navigation network. , 1998, Science.

[105]  S. Petersen,et al.  Hemispheric Specialization in Human Dorsal Frontal Cortex and Medial Temporal Lobe for Verbal and Nonverbal Memory Encoding , 1998, Neuron.

[106]  N. Alpert,et al.  Impaired recruitment of the hippocampus during conscious recollection in schizophrenia , 1998, Nature Neuroscience.

[107]  D. Schacter,et al.  Functional–Anatomic Study of Episodic Retrieval Using fMRI I. Retrieval Effort versus Retrieval Success , 1998, NeuroImage.

[108]  E. Tulving,et al.  Age‐related differences in effective neural connectivity during encoding and recall , 1997, Neuroreport.

[109]  Richard S. J. Frackowiak,et al.  Recalling Routes around London: Activation of the Right Hippocampus in Taxi Drivers , 1997, The Journal of Neuroscience.

[110]  M. Mishkin,et al.  Differential effects of early hippocampal pathology on episodic and semantic memory. , 1997, Science.

[111]  L. Nadel,et al.  Memory consolidation, retrograde amnesia and the hippocampal complex , 1997, Current Opinion in Neurobiology.

[112]  A. Berthoz,et al.  Mental navigation along memorized routes activates the hippocampus, precuneus, and insula , 1997, Neuroreport.

[113]  A R McIntosh,et al.  The neural correlates of intentional learning of verbal materials: a PET study in humans. , 1996, Brain research. Cognitive brain research.

[114]  L. Swanson,et al.  Structural Evidence for Functional Domains in the Rat Hippocampus , 1996, Science.

[115]  RU Muller,et al.  The hippocampus as a cognitive graph , 1996, The Journal of general physiology.

[116]  L. Squire,et al.  Retrograde amnesia and memory consolidation: a neurobiological perspective , 1995, Current Opinion in Neurobiology.

[117]  B. McNaughton,et al.  Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[118]  B L McNaughton,et al.  Dynamics of the hippocampal ensemble code for space. , 1993, Science.

[119]  F M Miezin,et al.  Activation of the hippocampus in normal humans: a functional anatomical study of memory. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[120]  H Eichenbaum,et al.  The theory that wouldn't die: A critical look at the spatial mapping theory of hippocampal function , 1991, Hippocampus.

[121]  R. Muller,et al.  The firing of hippocampal place cells in the dark depends on the rat's recent experience , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[122]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[123]  H. Eichenbaum,et al.  Representation in the hippocampus: what do hippocampal neurons code? , 1988, Trends in Neurosciences.

[124]  Leslie G. Ungerleider,et al.  Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys , 1982, Behavioural Brain Research.

[125]  J. Gray,et al.  Précis of The neuropsychology of anxiety: An enquiry into the functions of the septo-hippocampal system , 1982, Behavioral and Brain Sciences.

[126]  Brenda Milner,et al.  The role of the right hippocampus in the recall of spatial location , 1981, Neuropsychologia.

[127]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[128]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[129]  B. Cosquer,et al.  The ventral hippocampus is necessary for expressing a spatial memory , 2011, Brain Structure and Function.

[130]  Alex Martin,et al.  Access the most recent version at doi: 10.1101/lm.251906 , 2006 .

[131]  R. Cabeza,et al.  Cognitive neuroscience of emotional memory , 2006, Nature Reviews Neuroscience.

[132]  Craig J. Brozinsky,et al.  Lag‐sensitive repetition suppression effects in the anterior parahippocampal gyrus , 2005, Hippocampus.

[133]  G. Winocur,et al.  “I have often walked down this street before”: fMRI Studies on the hippocampus and other structures during mental navigation of an old environment , 2004, Hippocampus.

[134]  I. Whishaw,et al.  Impaired place navigation in place and matching‐to‐place swimming pool tasks follows both retrosplenial cortex lesions and cingulum bundle lesions in rats , 2004, Hippocampus.

[135]  Maija Pihlajamäki,et al.  Encoding of novel picture pairs activates the perirhinal cortex: An fMRI study , 2003, Hippocampus.

[136]  N. Alpert,et al.  Prefrontal regions supporting spontaneous and directed application of verbal learning strategies: evidence from PET. , 2001, Brain : a journal of neurology.

[137]  F. H. Lopes da Silva,et al.  Cortico‐hippocampal communication by way of parallel parahippocampal‐subicular pathways , 2000, Hippocampus.

[138]  L. Nadel,et al.  Multiple trace theory of human memory: Computational, neuroimaging, and neuropsychological results , 2000, Hippocampus.

[139]  Jonas Persson,et al.  Large Scale Neurocognitive Networks Underlying Episodic Memory , 2000, Journal of Cognitive Neuroscience.

[140]  M. Moser,et al.  Functional differentiation in the hippocampus , 1998, Hippocampus.