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• W2753444673 abstract "The hippocampus is famous for mapping locations in spatially organized environments, and several recent studies have shown that hippocampal networks also map moments in temporally organized experiences. Here I consider how space and time are integrated in the representation of memories. The brain pathways for spatial and temporal cognition involve overlapping and interacting systems that converge on the hippocampal region. There is evidence that spatial and temporal aspects of memory are processed somewhat differently in the circuitry of hippocampal subregions but become fully integrated within CA1 neuronal networks as independent, multiplexed representations of space and time. Hippocampal networks also map memories across a broad range of abstract relations among events, suggesting that the findings on spatial and temporal organization reflect a generalized mechanism for organizing memories. The hippocampus is famous for mapping locations in spatially organized environments, and several recent studies have shown that hippocampal networks also map moments in temporally organized experiences. Here I consider how space and time are integrated in the representation of memories. The brain pathways for spatial and temporal cognition involve overlapping and interacting systems that converge on the hippocampal region. There is evidence that spatial and temporal aspects of memory are processed somewhat differently in the circuitry of hippocampal subregions but become fully integrated within CA1 neuronal networks as independent, multiplexed representations of space and time. Hippocampal networks also map memories across a broad range of abstract relations among events, suggesting that the findings on spatial and temporal organization reflect a generalized mechanism for organizing memories. The hippocampus has long been regarded as critical to memory (Clark and Squire, 2013Clark R.E. Squire L.R. Similarity in form and function of the hippocampus in rodents, monkeys, and humans.Proc. Natl. Acad. Sci. USA. 2013; 110: 10365-10370Crossref PubMed Scopus (0) Google Scholar) as well as to supporting the brain’s representation of space (Moser et al., 2008Moser E.I. Kropff E. Moser M.-B. Place cells, grid cells, and the brain’s spatial representation system.Annu. Rev. Neurosci. 2008; 31: 69-89Crossref PubMed Scopus (606) Google Scholar). A potential link between these characterizations is that the hippocampus organizes memories in space, which is a prominent feature of memory that depends on the hippocampus (Eichenbaum et al., 1999Eichenbaum H. Dudchenko P. Wood E. Shapiro M. Tanila H. The hippocampus, memory, and place cells: is it spatial memory or a memory space?.Neuron. 1999; 23: 209-226Abstract Full Text Full Text PDF PubMed Scopus (589) Google Scholar). In addition, memory for specific experiences (episodic memory) is characterized by an organization of events in time (Tulving and Donaldson, 1972Tulving E. Donaldson W. Organization of Memory. Academic Press, 1972: 381-402Google Scholar), and several recent findings have revealed temporally organized hippocampal neuronal activity patterns that support memory (Dragoi and Buzsáki, 2006Dragoi G. Buzsáki G. Temporal encoding of place sequences by hippocampal cell assemblies.Neuron. 2006; 50: 145-157Abstract Full Text Full Text PDF PubMed Scopus (277) Google Scholar, Pastalkova et al., 2008Pastalkova E. Itskov V. Amarasingham A. Buzsáki G. Internally generated cell assembly sequences in the rat hippocampus.Science. 2008; 321: 1322-1327Crossref PubMed Scopus (410) Google Scholar, MacDonald et al., 2011MacDonald C.J. Lepage K.Q. Eden U.T. Eichenbaum H. Hippocampal “time cells” bridge the gap in memory for discontiguous events.Neuron. 2011; 71: 737-749Abstract Full Text Full Text PDF PubMed Scopus (303) Google Scholar, Wikenheiser and Redish, 2015Wikenheiser A.M. Redish A.D. Decoding the cognitive map: ensemble hippocampal sequences and decision making.Curr. Opin. Neurobiol. 2015; 32: 8-15Crossref PubMed Scopus (20) Google Scholar, Cai et al., 2016Cai D.J. Aharoni D. Shuman T. Shobe J. Biane J. Song W. Wei B. Veshkini M. La-Vu M. Lou J. et al.A shared neural ensemble links distinct contextual memories encoded close in time.Nature. 2016; 534: 115-118Crossref PubMed Scopus (404) Google Scholar; reviewed in Eichenbaum, 2014Eichenbaum H. Time cells in the hippocampus: a new dimension for mapping memories.Nat. Rev. Neurosci. 2014; 15: 732-744Crossref PubMed Scopus (299) Google Scholar). Combining these lines of evidence, one possible accounting of hippocampal function is the organization of memories in space and time (Eichenbaum, 2017Eichenbaum H. Memory: organization and control.Annu. Rev. Psychol. 2017; 68: 19-45Crossref PubMed Scopus (12) Google Scholar). A key question in pursuing this hypothesis is how neuronal networks within the hippocampus accomplish the combination of spatial and temporal organization. In our everyday lives, we typically conceive of space and time as separate dimensions of experience, but we often combine them in our expression of episodic memories. If I asked about your morning, you likely could recap the full episode as it unfolded in time and across places where successive events occurred. This perspective reflects a common view that episodic memory involves embedding our record of events within a unified representation of spatiotemporal context (e.g., Copara et al., 2014Copara M.S. Hassan A.S. Kyle C.T. Libby L.A. Ranganath C. Ekstrom A.D. Complementary roles of human hippocampal subregions during retrieval of spatiotemporal context.J. Neurosci. 2014; 34: 6834-6842Crossref PubMed Scopus (26) Google Scholar). Also, in formal applications of physics and cosmology, considerations of space straightforwardly include time as a fourth dimension. Most famously, a key component of Einstein’s special relativity theory is that time dilates with speed across reference frames, and this observation forms the basis for our modern conception of “spacetime” as a unification of spatial and temporal dimensions. Here I consider how the brain processes space and time, focusing on whether the brain pathways and mechanisms for spatial and temporal processing reflect distinct spatial and temporal codings or instead reflect a unified representation of spacetime in which memories are localized. The pioneering studies that distinguished “what” and “where” streams of visual processing identified a dedicated brain pathway for spatial cognition and action separate from a different pathway that supports the perception of specific objects (Mishkin and Ungerleider, 1982Mishkin M. Ungerleider L.G. Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys.Behav. Brain Res. 1982; 6: 57-77Crossref PubMed Scopus (0) Google Scholar, Goodale and Milner, 1992Goodale M.A. Milner A.D. Separate visual pathways for perception and action.Trends Neurosci. 1992; 15: 20-25Abstract Full Text PDF PubMed Scopus (2990) Google Scholar). Decades of research have delineated details of the “where” stream as a succession of cortical areas that extends to the parahippocampal cortex (in primates; called postrhinal cortex in rodents) and the medial component of the entorhinal cortex, which are parts of the hippocampal region (Felleman and Van Essen, 1991Felleman D.J. Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex.Cereb. Cortex. 1991; 1: 1-47Crossref PubMed Google Scholar, Suzuki and Amaral, 1994Suzuki W.A. Amaral D.G. Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents.J. Comp. Neurol. 1994; 350: 497-533Crossref PubMed Scopus (745) Google Scholar, Burwell and Amaral, 1998Burwell R.D. Amaral D.G. Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat.J. Comp. Neurol. 1998; 398: 179-205Crossref PubMed Scopus (442) Google Scholar). Numerous functional imaging studies in humans have observed selective activation of the parahippocampal and medial entorhinal cortices when subjects recall scenes in which specific items were studied, thus identifying these areas as representing spatial elements of memories (reviewed in Eichenbaum et al., 2007Eichenbaum H. Yonelinas A.P. Ranganath C. The medial temporal lobe and recognition memory.Annu. Rev. Neurosci. 2007; 30: 123-152Crossref PubMed Scopus (1213) Google Scholar; see below). Studies on the perception of elapsed time (called interval timing) describe a widespread brain system that involves partially distinct pathways and mechanisms from those of the “where” stream (Buhusi and Meck, 2005Buhusi C.V. Meck W.H. What makes us tick? Functional and neural mechanisms of interval timing.Nat. Rev. Neurosci. 2005; 6: 755-765Crossref PubMed Scopus (920) Google Scholar, Meck et al., 2008Meck W.H. Penney T.B. Pouthas V. Cortico-striatal representation of time in animals and humans.Curr. Opin. Neurobiol. 2008; 18: 145-152Crossref PubMed Scopus (0) Google Scholar). There are many models of the mechanisms of timing (Mauk and Buonomano, 2004Mauk M.D. Buonomano D.V. The neural basis of temporal processing.Annu. Rev. Neurosci. 2004; 27: 307-340Crossref PubMed Scopus (497) Google Scholar), and one prominent model suggests that the capacity for interval timing involves interactions among multiple oscillatory patterns in prefrontal and parietal cortical areas, resulting in unique patterns of activation at different times that are integrated in the striatum (Matell and Meck, 2000Matell M.S. Meck W.H. Neuropsychological mechanisms of interval timing behavior.BioEssays. 2000; 22: 94-103Crossref PubMed Scopus (0) Google Scholar, Lustig et al., 2005Lustig C. Matell M.S. Meck W.H. Not “just” a coincidence: frontal-striatal interactions in working memory and interval timing.Memory. 2005; 13: 441-448Crossref PubMed Scopus (98) Google Scholar). In support of this model, several studies have shown that timing depends on the prefrontal and parietal cortices and striatum and that neurons in these areas signal elapsed time. Thus, damage to the medial prefrontal cortex severely impairs interval timing in rats, and neurons in the medial prefrontal cortex signal elapsed time in rats performing an interval discrimination task (Kim et al., 2013Kim J. Ghim J.-W. Lee J.H. Jung M.W. Neural correlates of interval timing in rodent prefrontal cortex.J. Neurosci. 2013; 33: 13834-13847Crossref PubMed Scopus (44) Google Scholar, Tiganj et al., 2015Tiganj Z. Hasselmo M.E. Howard M.W. A simple biophysically plausible model for long time constants in single neurons.Hippocampus. 2015; 25: 27-37Crossref PubMed Scopus (10) Google Scholar). Several studies have also provided compelling evidence that the parietal cortex is also involved in timing. In monkeys trained to report whether the duration of a test light was longer or shorter than a remembered standard, neurons in the lateral parietal area signal changes in judgments about elapsed time (Leon and Shadlen, 2003Leon M.I. Shadlen M.N. Representation of time by neurons in the posterior parietal cortex of the macaque.Neuron. 2003; 38: 317-327Abstract Full Text Full Text PDF PubMed Scopus (374) Google Scholar, Janssen and Shadlen, 2005Janssen P. Shadlen M.N. A representation of the hazard rate of elapsed time in macaque area LIP.Nat. Neurosci. 2005; 8: 234-241Crossref PubMed Scopus (337) Google Scholar). Functional imaging studies in humans have shown that the parietal-temporal junction is activated when subjects judge the temporal order of stimuli that are presented in rapid succession (Davis et al., 2009Davis B. Christie J. Rorden C. Temporal order judgments activate temporal parietal junction.J. Neurosci. 2009; 29: 3182-3188Crossref PubMed Scopus (53) Google Scholar). Conversely, when subjects are trained to judge the temporal order of two rapidly presented visual stimuli, transcranial magnetic stimulation (TMS) over the parietal-temporal junction impairs judgments about their temporal order (Woo et al., 2009Woo S.-H. Kim K.-H. Lee K.-M. The role of the right posterior parietal cortex in temporal order judgment.Brain Cogn. 2009; 69: 337-343Crossref PubMed Scopus (0) Google Scholar). Also, mental self-projection both to earlier times in life and to specific locations in space engages the parietal cortex within partially distinct cortical networks (Gauthier and van Wassenhove, 2016Gauthier B. van Wassenhove V. Time is not space: core computations and domain-specific Networks for Mental Travels.J. Neurosci. 2016; 36: 11891-11903Crossref PubMed Scopus (1) Google Scholar). Similarly, several studies have shown that damage or dysfunction of the striatum results in impairments in interval-timing judgments in rats (reviewed in Howard et al., 2015Howard M.W. Shankar K.H. Aue W.R. Criss A.H. A distributed representation of internal time.Psychol. Rev. 2015; 122: 24-53Crossref PubMed Scopus (11) Google Scholar), and, conversely, striatal neurons fire at sequential moments during memory delays in rats performing a fixed-interval lever-pressing task (Mello et al., 2015Mello G.B. Soares S. Paton J.J. A scalable population code for time in the striatum.Curr. Biol. 2015; 25: 1113-1122Abstract Full Text Full Text PDF PubMed Scopus (50) Google Scholar) and in a spatial working memory task (Akhlaghpour et al., 2016Akhlaghpour H. Wiskerke J. Choi J.Y. Taliaferro J.P. Au J. Witten I.B. Dissociated sequential activity and stimulus encoding in the dorsomedial striatum during spatial working memory.eLife. 2016; 5: e19507Crossref PubMed Scopus (2) Google Scholar). Also, striatal neuronal activity predicts judgments of time in rats performing a duration categorization task (Gouvêa et al., 2015Gouvêa T.S. Monteiro T. Motiwala A. Soares S. Machens C. Paton J.J. Striatal dynamics explain duration judgments.eLife. 2015; 4: e11386Crossref PubMed Scopus (9) Google Scholar), and neural ensembles in the striatum signal elapsed time in monkeys performing an interval-timing task (Adler et al., 2012Adler A. Katabi S. Finkes I. Israel Z. Prut Y. Bergman H. Temporal convergence of dynamic cell assemblies in the striato-pallidal network.J. Neurosci. 2012; 32: 2473-2484Crossref PubMed Scopus (33) Google Scholar). Additional studies that characterize interactions among areas report that overlapping cortical networks process memories for spatial and temporal information in extended events. In experiments where human subjects travel through a city in virtual reality, memory for the spatial location and memory for temporal order of events both engage a prefrontal–parietal cortical network along with medial temporal areas. However, interactions between areas associated with remembering where or when specific events occur operate at different network oscillation frequencies, identified by phase synchronization in electroencephalography (EEG) patterns as a measure of network connectivity. In one study, subjects performed a working memory task where they were required to judge the order or location of stimulus presentations on a screen (Watrous et al., 2013Watrous A.J. Tandon N. Conner C.R. Pieters T. Ekstrom A.D. Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval.Nat. Neurosci. 2013; 16: 349-356Crossref PubMed Scopus (88) Google Scholar). Time-frequency analysis of the EEG revealed enhanced power of left frontal theta (5–8 Hz), posterior alpha (9–12 Hz), and left posterior beta (14–28 Hz) during the delay period of correct temporal order trials compared to correct spatial trials. In another study, gamma (30–50 Hz) power at right lateral frontal sites was increased during the delay period of spatial working memory trials as compared to temporal working memory trials (Roberts et al., 2013Roberts B.M. Hsieh L.-T. Ranganath C. Oscillatory activity during maintenance of spatial and temporal information in working memory.Neuropsychologia. 2013; 51: 349-357Crossref PubMed Scopus (0) Google Scholar). These observations of differences in oscillatory patterns associated with spatial and temporal memory success suggest distinct mechanisms for the maintenance of temporal and spatial information in working memory. Similarly, fMRI studies on humans performing the virtual city task have shown that the hippocampus, prefrontal cortex, precuneus, and visual cortex all serve as hubs of high network connectivity. However, within the larger network, the operation of overlapping sub-networks for spatial and temporal memory retrieval is distinguished by higher connectivity within posterior and anterior brain areas, respectively (Schedlbauer et al., 2014Schedlbauer A.M. Copara M.S. Watrous A.J. Ekstrom A.D. Multiple interacting brain areas underlie successful spatiotemporal memory retrieval in humans.Sci. Rep. 2014; 4: 6431Crossref PubMed Scopus (27) Google Scholar). The combined EEG and fMRI findings thus provide parallel evidence of sub-networks for spatial and temporal processing connected via medial temporal areas as a hub for spatial-temporal integration (Figure 1; also see Hsieh and Ranganath, 2015Hsieh L.T. Ranganath C. Cortical and subcortical contributions to sequence retrieval: Schematic coding of temporal context in the neocortical recollection network.Neuroimage. 2015; 121: 78-90Crossref PubMed Scopus (9) Google Scholar). Furthermore, taken together, these observations support the notion that spatial memory and temporal memory are mediated by overlapping and interacting brain systems that converge on the hippocampal region. There is substantial additional evidence that the parahippocampal cortex and medial entorhinal cortex support memory for spatial and temporal contexts. Functional imaging studies have reported that the parahippocampal cortex is activated when human subjects view spatial scenes (Epstein and Kanwisher, 1998Epstein R. Kanwisher N. A cortical representation of the local visual environment.Nature. 1998; 392: 598-601Crossref PubMed Scopus (1592) Google Scholar, Epstein et al., 2007Epstein R.A. Parker W.E. Feiler A.M. Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition.J. Neurosci. 2007; 27: 6141-6149Crossref PubMed Scopus (170) Google Scholar) as well as pictures of objects that have strong associations with a spatial context (e.g., a refrigerator) compared with objects that have no strong contextual association (a pencil; Bar and Aminoff, 2003Bar M. Aminoff E. Cortical analysis of visual context.Neuron. 2003; 38: 347-358Abstract Full Text Full Text PDF PubMed Scopus (352) Google Scholar). In a further study, Aminoff et al., 2007Aminoff E. Gronau N. Bar M. The parahippocampal cortex mediates spatial and nonspatial associations.Cereb. Cortex. 2007; 17: 1493-1503Crossref PubMed Scopus (188) Google Scholar trained human subjects on spatial and temporal contextual associations by having subjects repeatedly view a set of meaningless visual patterns in the same spatial arrangement, always together but in different spatial arrangements, or individually. They then used fMRI to compare to level of activation for items trained individually to those when items were trained within a spatial and temporal context. The activation patterns within parahippocampal cortex partially distinguished a parahippocampal area that activated in response to items that were associated by spatial arrangement from another parahippocampal area that activated for items that co-occurred in time without spatial regularity. Experiments that explicitly tested memory for spatial and temporal contexts or a spatial arrangement of object cues have shown that the parahippocampal cortex activates when human subjects remember either spatial or temporal context. In fMRI studies of spatial context, Davachi et al., 2003Davachi L. Mitchell J.P. Wagner A.D. Multiple routes to memory: distinct medial temporal lobe processes build item and source memories.Proc. Natl. Acad. Sci. USA. 2003; 100: 2157-2162Crossref PubMed Scopus (571) Google Scholar reported that the parahippocampal area is activated when subjects recall a spatial scene with which object stimuli were associated. Libby et al., 2014Libby L.A. Hannula D.E. Ranganath C. Medial temporal lobe coding of item and spatial information during relational binding in working memory.J. Neurosci. 2014; 34: 14233-14242Crossref PubMed Scopus (27) Google Scholar tested subjects on memory for objects in specific locations in an array, and they used multivoxel pattern analysis to determine the extent of object and location coding in hippocampal areas. They found that, whereas activity patterns in the perirhinal cortex carried information about individual objects, activity patterns in the parahippocampal cortex carried information about the configuration of spatial locations that was to be remembered, although the patterns of activation in these areas was not predictive of memory success per se. Another fMRI study reported that the medial entorhinal cortex activates associated with the familiarity of object locations, as contrasted with the observation that the lateral entorhinal cortex activates associated with the familiarity of object identities (Reagh and Yassa, 2014Reagh Z.M. Yassa M.A. Object and spatial mnemonic interference differentially engage lateral and medial entorhinal cortex in humans.Proc. Natl. Acad. Sci. USA. 2014; 111: E4264-E4273Crossref PubMed Scopus (0) Google Scholar). In a study on the temporal organization of memories, Hsieh et al., 2014Hsieh L.-T. Gruber M.J. Jenkins L.J. Ranganath C. Hippocampal activity patterns carry information about objects in temporal context.Neuron. 2014; 81: 1165-1178Abstract Full Text Full Text PDF PubMed Scopus (89) Google Scholar trained human subjects on sequences of objects, and then they used multivoxel pattern analysis to measure the similarity of activation patterns for the same objects in different temporal sequences. They found that, whereas the perirhinal cortex activated in similar multivoxel patterns for specific objects across sequences, the parahippocampal cortex activated in similar patterns for temporal positions across sequences, indicating a representation of temporal organization. Another fMRI study showed that the parahippocampal cortex also activates during the retrieval of the temporal order of a series of scenes in a movie as compared to a control condition where subjects logically inferred the order of scenes from the same movie (Lehn et al., 2009Lehn H. Steffenach H.-A. van Strien N.M. Veltman D.J. Witter M.P. Håberg A.K. A specific role of the human hippocampus in recall of temporal sequences.J. Neurosci. 2009; 29: 3475-3484Crossref PubMed Scopus (95) Google Scholar). Additional evidence from studies on rodents indicates that space and time are integrated in the medial entorhinal cortex. Lipton and Eichenbaum, 2008Lipton P.A. Eichenbaum H. Complementary roles of hippocampus and medial entorhinal cortex in episodic memory.Neural Plast. 2008; 2008: 258467Crossref PubMed Scopus (43) Google Scholar recorded from medial entorhinal neurons in rats alternating between paths in a T-maze where left-turn and right-turn routes through the maze overlapped just before the critical choice in the task. They found that medial entorhinal neurons had spatially specific firing patterns, and these patterns differed for left-turn and right-turn trajectories, including sections of the maze that the rats traversed on both trajectories. Thus, the spatial firing patterns of medial entorhinal neurons discriminated paths depending on the trajectory to a goal that defined the temporal context of that episode (see also Frank et al., 2000Frank L.M. Brown E.N. Wilson M. Trajectory encoding in the hippocampus and entorhinal cortex.Neuron. 2000; 27: 169-178Abstract Full Text Full Text PDF PubMed Google Scholar). Furthermore, Kraus et al., 2015Kraus B.J. Brandon M.P. Robinson 2nd, R.J. Connerney M.A. Hasselmo M.E. Eichenbaum H. During running in place, grid cells integrate elapsed time and distance run.Neuron. 2015; 88: 578-589Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar found that medial entorhinal grid cells, which have highly specific spatial firing patterns during open field exploration, also fire at sequential moments while running in place for specific periods on a treadmill, and the activity of these cells signaled both elapsed time and distance run on the treadmill. These results indicate that the same neurons that code locations in space are the cells that code moments in a temporally structured experience, although individual neurons differed in the extent to which they coded time and distance (see below). Taken together, the findings on humans and animals provide strong evidence indicating that the role of parahippocampal and medial entorhinal cortical areas in memory extends equally to the representation of spatial and temporal organization. Given that space and time are represented together in major cortical afferents to the hippocampus, it might be expected that these dimensions also be merged throughout the circuitry of the hippocampus itself. Evidence from functional imaging studies in humans and lesion and recording studies in animals provides different perspectives on whether space and time are processed distinctly or fully integrated within the hippocampal subdivisions. Hippocampal circuitry involves sequential and parallel stages of information processing, such that the entorhinal cortex projects to all hippocampal subdivisions and intrinsic pathways involve successive projections from CA3 to CA2 and CA1 and from CA2 to CA1 (Figure 1; Amaral and Lavenex, 2006Amaral D. Lavenex P. Hippocampal neuroanatomy.in: Andersen P. Morris R. Amaral D. Bliss T. O’Keefe J. The Hippocampus Book. Oxford University Press, 2006: 37-114Google Scholar, Dudek et al., 2016Dudek S.M. Alexander G.M. Farris S. Rediscovering area CA2: unique properties and functions.Nat. Rev. Neurosci. 2016; 17: 89-102Crossref PubMed Scopus (22) Google Scholar). Outputs of this circuitry are from CA3 to subcortical areas and from CA1 back to the entorhinal cortex and other cortical areas both directly and indirectly via the subiculum. Thus, because CA3 and CA1 have independent inputs and outputs, it is possible that each of these areas makes separate contributions to spatial or temporal processing in the absence of the other, as has been reported in some of the studies described below. There is a long history of studies showing hippocampal activation in humans associated with memories for events in spatial context (reviewed in Eichenbaum et al., 2007Eichenbaum H. Yonelinas A.P. Ranganath C. The medial temporal lobe and recognition memory.Annu. Rev. Neurosci. 2007; 30: 123-152Crossref PubMed Scopus (1213) Google Scholar). One particularly compelling demonstration involved testing human subjects on memory for objects in specific locations in an array. Multivoxel pattern analysis revealed that hippocampal activity patterns predicted accurate memory for particular object-location relationships (Libby et al., 2014Libby L.A. Hannula D.E. Ranganath C. Medial temporal lobe coding of item and spatial information during relational binding in working memory.J. Neurosci. 2014; 34: 14233-14242Crossref PubMed Scopus (27) Google Scholar). In recent years, several studies have also reported activation of the hippocampus associated with memory for the temporal organization of memories (Hsieh et al., 2014Hsieh L.-T. Gruber M.J. Jenkins L.J. Ranganath C. Hippocampal activity patterns carry information about objects in temporal context.Neuron. 2014; 81: 1165-1178Abstract Full Text Full Text PDF PubMed Scopus (89) Google Scholar, Lehn et al., 2009Lehn H. Steffenach H.-A. van Strien N.M. Veltman D.J. Witter M.P. Håberg A.K. A specific role of the human hippocampus in recall of temporal sequences.J. Neurosci. 2009; 29: 3475-3484Crossref PubMed Scopus (95) Google Scholar; see also Ezzyat and Davachi, 2014Ezzyat Y. Davachi L. Similarity breeds proximity: pattern similarity within and across contexts is related to later mnemonic judgments of temporal proximity.Neuron. 2014; 81: 1179-1189Abstract Full Text Full Text PDF PubMed Scopus (57) Google Scholar, DuBrow and Davachi, 2016DuBrow S. Davachi L. Temporal binding within and across events.Neurobiol. Learn. Mem. 2016; 134: 107-114Crossref PubMed Scopus (13) Google Scholar; review in Eichenbaum, 2014Eichenbaum H. Time cells in the hippocampus: a new dimension for mapping memories.Nat. Rev. Neurosci. 2014; 15: 732-744Crossref PubMed Scopus (299) Google Scholar). For example, Lehn et al., 2009Lehn H. Steffenach H.-A. van Strien N.M. Veltman D.J. Witter M.P. Håberg A.K. A specific role of the human hippocampus in recall of temporal sequences.J. Neurosci. 2009; 29: 3475-3484Crossref PubMed Scopus (95) Google Scholar let subjects watch a novel movie and later, during fMRI, asked them to rearrange and replay scenes from the movie in correct order. To identify areas specifically involved in the retrieval of temporal order, they used a control condition where subjects logically inferred the order of scenes from the same movie. Strong hippocampal activation was specifically related to retrieval of temporal order and positively correlated with accuracy of sequence recall. Also, Hsieh and Ranganath, 2015Hsieh L.T. Ranganath C. Cortical and subcortical contributions to sequence retrieval: Schematic coding of temporal context in the neocortical recollection network.Neuroimage. 2015; 121: 78-90Crossref PubMed Scopus (9) Google Scholar used multivoxel pattern similarity analysis of fMRI data during retrieval of learned object sequences to systematically investigate hippocampal coding of object and temporal context information. Hippocampal activity patterns carried information about the temporal positions of objects in learned sequences, but not about objects or temporal positions in random sequences. In addition, hippocampal activation patterns" @default.
• W2753444673 created "2017-09-15" @default.
• W2753444673 creator A5091615509 @default.
• W2753444673 date "2017-08-01" @default.
• W2753444673 modified "2023-10-17" @default.
• W2753444673 title "On the Integration of Space, Time, and Memory" @default.
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