A Neural Chronometry of Memory Recall
2019; Elsevier BV; Volume: 23; Issue: 12 Linguagem: Inglês
10.1016/j.tics.2019.09.011
ISSN1879-307X
AutoresBernhard P. Staresina, Maria Wimber,
Tópico(s)Neural and Behavioral Psychology Studies
ResumoSimple reminders can bring back a host of vivid memories, experimentally epitomised in cued-recall paradigms.Electrophysiological recordings have elucidated the chronometry with which sensory cues are converted into retrieved memories.At 500 ms after cue onset, a pattern completion process begins in the hippocampus and triggers the reinstatement of the target memory in the neocortex.Cortical reinstatement unfolds between 500 and 1500 ms and gives rise to the subjective feeling of recollection.Reinstatement is governed by intricate temporal dynamics, including the reversal of perceptual processing streams and clocking by theta rhythms. Episodic memory allows us to mentally travel through time. How does the brain convert a simple reminder cue into a full-blown memory of past events and experiences? In this review, we integrate recent developments in the cognitive neuroscience of human memory retrieval, pinpointing the neural chronometry underlying successful recall. Electrophysiological recordings suggest that sensory cues proceed into the medial temporal lobe within the first 500 ms. At this point, a hippocampal process sets in, geared toward internal pattern completion and coordination of cortical memory reinstatement between 500 and 1500 ms. We further highlight the dynamic principles governing the recall process, which include a reversal of perceptual information flows, temporal compression, and theta clocking. Episodic memory allows us to mentally travel through time. How does the brain convert a simple reminder cue into a full-blown memory of past events and experiences? In this review, we integrate recent developments in the cognitive neuroscience of human memory retrieval, pinpointing the neural chronometry underlying successful recall. Electrophysiological recordings suggest that sensory cues proceed into the medial temporal lobe within the first 500 ms. At this point, a hippocampal process sets in, geared toward internal pattern completion and coordination of cortical memory reinstatement between 500 and 1500 ms. We further highlight the dynamic principles governing the recall process, which include a reversal of perceptual information flows, temporal compression, and theta clocking. One of the most remarkable capacities of the human mind is to mentally travel back in time and relive past experiences in great detail. Think of how looking at your vacation photograph album, hearing the first notes of an old favourite song, or smelling the perfume of a loved one can reignite entire experiences and associated emotions, sensations, and thoughts. In experimental terms, a scenario in which an external or a self-generated (i.e., internal) reminder elicits a vivid memory is referred to as cued recall (see Glossary). Intriguingly, the conversion of a simple cue to a full-blown memory can occur within a few hundred milliseconds. Despite decades of neuroimaging research, however, little is known about the precise temporal dynamics that govern successful memory recall. Is there a particular sequence in which particular brain regions need to engage? Where and when does the conversion from cue to target representations occur? Do the neural codes change from perceiving to retrieving? In this review, we discuss new results elucidating the neural chronometry of cued recall. After a brief summary of computational models and fMRI work, we delve into recent findings from human electrophysiology, capitalising on direct invasive recordings and time-resolved multivariate pattern analyses. Mounting evidence suggests the following scenario. Within the first ∼500 ms after cue presentation, information traverses dedicated cortical pathways and progresses toward the medial temporal lobe (MTL). In the MTL cortex, the cue elicits an initial ‘old/new’ signal. If the cue is deemed old/familiar, a hippocampal process sets in at ∼500 ms, in the first instance geared toward reactivating the hippocampal cell assembly assigned to the initial experience (pattern completion). If successful, hippocampal pattern completion triggers the sustained reinstatement of the cortical memory trace between ∼500 and 1500 ms. This is the time interval in which a full-blown mnemonic representation unfolds, with posterior parietal regions contributing to the maintenance and goal-directed manipulation of the target memory (Box 1). On a mechanistic level, memory recall exhibits distinctive temporal dynamics, including flow reversal, time compression, and theta clocking (Figure 1, Key Figure).Box 1Parietal Cortex Contributions to Memory RecallNeuroimaging work has consistently shown engagement of the medial and lateral posterior parietal cortex (PPC) in episodic memory retrieval [94Hutchinson J.B. et al.Posterior parietal cortex and episodic retrieval: convergent and divergent effects of attention and memory.Learn. Mem. 2009; 16: 343-356Crossref PubMed Scopus (168) Google Scholar]. Although beyond the scope of the current review, it deserves mention that the PPC comprises structurally and functionally distinct subregions [95Nelson S.M. et al.A parcellation scheme for human left lateral parietal cortex.Neuron. 2010; 67: 156-170Abstract Full Text Full Text PDF PubMed Scopus (250) Google Scholar, 96Sestieri C. et al.The contribution of the human posterior parietal cortex to episodic memory.Nat. Rev. Neurosci. 2017; 18: 183Crossref PubMed Scopus (59) Google Scholar, 97Wagner A.D. et al.Parietal lobe contributions to episodic memory retrieval.Trends Cogn. Sci. 2005; 9: 445-453Abstract Full Text Full Text PDF PubMed Scopus (1005) Google Scholar, 98Sestieri C. et al.Attention to memory and the environment: functional specialization and dynamic competition in human posterior parietal cortex.J. Neurosci. 2010; 30: 8445-8456Crossref PubMed Scopus (71) Google Scholar]. Recall/reinstatement effects in the PPC seem to differ qualitatively from those in occipitotemporal regions [99Xiao X. et al.Transformed neural pattern reinstatement during episodic memory retrieval.J. Neurosci. 2017; 37: 2986-2998Crossref PubMed Scopus (13) Google Scholar, 100Favila S.E. et al.Parietal representations of stimulus features are amplified during memory retrieval and flexibly aligned with top-down goals.J. Neurosci. 2018; 38: 7809-7821Crossref PubMed Scopus (3) Google Scholar] and prominent views hold that parts of the PPC serve as an amodal episodic buffer [97Wagner A.D. et al.Parietal lobe contributions to episodic memory retrieval.Trends Cogn. Sci. 2005; 9: 445-453Abstract Full Text Full Text PDF PubMed Scopus (1005) Google Scholar, 101Baddeley A. The episodic buffer: a new component of working memory?.Trends Cogn. Sci. 2000; 4: 417-423Abstract Full Text Full Text PDF PubMed Scopus (3318) Google Scholar] or are deployed for working with memories in a goal-directed fashion once they are recalled [89Cabeza R. et al.The parietal cortex and episodic memory: an attentional account.Nat. Rev. Neurosci. 2008; 9: 613Crossref PubMed Scopus (679) Google Scholar, 96Sestieri C. et al.The contribution of the human posterior parietal cortex to episodic memory.Nat. Rev. Neurosci. 2017; 18: 183Crossref PubMed Scopus (59) Google Scholar]. Common to these accounts is that the PPC responds to a bottom-up mnemonic signal, and as reviewed in the main text, the most likely candidate to generate this signal is the hippocampus. By varying the interval of maintenance of a recalled episodic detail, fMRI data suggest that hippocampal engagement during successful recall is transient, whereas PPC engagement is sustained and covaries in time with the maintenance interval [102Vilberg K.L. Rugg M.D. The neural correlates of recollection: transient versus sustained fMRI effects.J. Neurosci. 2012; 32: 15679-15687Crossref PubMed Scopus (54) Google Scholar]. Moreover, a recent fMRI study found that mnemonic decodability in the PPC correlated with that in MTL regions [103Guidotti R. et al.Choice-predictive activity in parietal cortex during source memory decisions.Neuroimage. 2019; 189: 589-600Crossref PubMed Scopus (0) Google Scholar]. Both of these results are consistent with the notion that a hippocampal memory signal precedes and influences PPC engagement, although it is difficult to infer the exact temporal relationship between these regions based solely on fMRI dynamics. One recent study used fMRI in conjunction with source-reconstructed EEG/MEG and revealed a recall effect in the left precuneus from 600 to 1600 ms after cue onset [104Bergström Z.M. et al.Multimodal imaging reveals the spatiotemporal dynamics of recollection.Neuroimage. 2013; 68: 141-153Crossref PubMed Scopus (21) Google Scholar]. Human intracranial recordings from parietal regions are relatively rare compared with MTL coverage. Besides two studies using simple old/new recognition memory paradigms [29Rutishauser U. et al.Representation of retrieval confidence by single neurons in the human medial temporal lobe.Nat. Neurosci. 2015; 18: 1041Crossref PubMed Scopus (43) Google Scholar, 105Gonzalez A. et al.Electrocorticography reveals the temporal dynamics of posterior parietal cortical activity during recognition memory decisions.Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 11066-11071Crossref PubMed Scopus (0) Google Scholar], one study [106Foster B.L. et al.Neural populations in human posteromedial cortex display opposing responses during memory and numerical processing.Proc. Natl. Acad. Sci. U. S. A. 2012; 109: 15514-15519Crossref PubMed Scopus (37) Google Scholar] used an autobiographical memory task, more strongly reliant on recall processes. Pronounced engagement of the PPC was observed (high-gamma signal; 70–180 Hz), with an average onset of the parietal response at 600 ms. Together these studies suggest that PPC contributions unfold after the hippocampal recall process has begun. We speculate that there might be a push–pull relationship between the hippocampus and PPC. In particular, the hippocampus initiates cortical reinstatement in a bottom-up, holistic fashion [64Horner A.J. et al.Evidence for holistic episodic recollection via hippocampal pattern completion.Nat. Commun. 2015; 6: 7462Crossref PubMed Google Scholar], whereas the PPC aids and refines recall by deploying working memory/attentional resources to recover the task-relevant mnemonic features [107Kuhl B.A. et al.Dissociable neural mechanisms for goal-directed versus incidental memory reactivation.J. Neurosci. 2013; 33: 16099-16109Crossref PubMed Scopus (0) Google Scholar] (see Outstanding Questions). Given the extent of the structural and functional connectivity of the PPC not only with the hippocampus [108Wang J.X. et al.Targeted enhancement of cortical–hippocampal brain networks and associative memory.Science. 2014; 345: 1054-1057Crossref PubMed Scopus (0) Google Scholar] but also with a wide network of high-level cortical regions [109Raichle M.E. et al.A default mode of brain function.Proc. Natl Acad. Sci. U. S. A. 2001; 98: 676-682Crossref PubMed Scopus (0) Google Scholar, 110Schmahmann J.D. et al.Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography.Brain. 2007; 130: 630-653Crossref PubMed Scopus (658) Google Scholar, 111Silson E.H. et al.Distinct subdivisions of human medial parietal cortex support recollection of people and places.Elife. 2019; 8: e47391Crossref PubMed Scopus (0) Google Scholar], this region might be thought of as an additional, third layer in the multiplexed index for memory reinstatement (hippocampus → EC → PPC). This notion is corroborated by a recent MEG study showing enhanced connectivity between the MTL and precuneus during autobiographical memory retrieval [85Hebscher M. et al.A causal role for the precuneus in network-wide theta and gamma oscillatory activity during complex memory retrieval.Elife. 2019; 8: e43114Crossref PubMed Scopus (0) Google Scholar]. Experimental disruption of the precuneus via continuous theta burst stimulation diminished both MTL–cortical coupling and memory vividness, pointing to a potential role of the PPC in maintaining hippocampal–cortical communication in the service of successful recall. Neuroimaging work has consistently shown engagement of the medial and lateral posterior parietal cortex (PPC) in episodic memory retrieval [94Hutchinson J.B. et al.Posterior parietal cortex and episodic retrieval: convergent and divergent effects of attention and memory.Learn. Mem. 2009; 16: 343-356Crossref PubMed Scopus (168) Google Scholar]. Although beyond the scope of the current review, it deserves mention that the PPC comprises structurally and functionally distinct subregions [95Nelson S.M. et al.A parcellation scheme for human left lateral parietal cortex.Neuron. 2010; 67: 156-170Abstract Full Text Full Text PDF PubMed Scopus (250) Google Scholar, 96Sestieri C. et al.The contribution of the human posterior parietal cortex to episodic memory.Nat. Rev. Neurosci. 2017; 18: 183Crossref PubMed Scopus (59) Google Scholar, 97Wagner A.D. et al.Parietal lobe contributions to episodic memory retrieval.Trends Cogn. Sci. 2005; 9: 445-453Abstract Full Text Full Text PDF PubMed Scopus (1005) Google Scholar, 98Sestieri C. et al.Attention to memory and the environment: functional specialization and dynamic competition in human posterior parietal cortex.J. Neurosci. 2010; 30: 8445-8456Crossref PubMed Scopus (71) Google Scholar]. Recall/reinstatement effects in the PPC seem to differ qualitatively from those in occipitotemporal regions [99Xiao X. et al.Transformed neural pattern reinstatement during episodic memory retrieval.J. Neurosci. 2017; 37: 2986-2998Crossref PubMed Scopus (13) Google Scholar, 100Favila S.E. et al.Parietal representations of stimulus features are amplified during memory retrieval and flexibly aligned with top-down goals.J. Neurosci. 2018; 38: 7809-7821Crossref PubMed Scopus (3) Google Scholar] and prominent views hold that parts of the PPC serve as an amodal episodic buffer [97Wagner A.D. et al.Parietal lobe contributions to episodic memory retrieval.Trends Cogn. Sci. 2005; 9: 445-453Abstract Full Text Full Text PDF PubMed Scopus (1005) Google Scholar, 101Baddeley A. The episodic buffer: a new component of working memory?.Trends Cogn. Sci. 2000; 4: 417-423Abstract Full Text Full Text PDF PubMed Scopus (3318) Google Scholar] or are deployed for working with memories in a goal-directed fashion once they are recalled [89Cabeza R. et al.The parietal cortex and episodic memory: an attentional account.Nat. Rev. Neurosci. 2008; 9: 613Crossref PubMed Scopus (679) Google Scholar, 96Sestieri C. et al.The contribution of the human posterior parietal cortex to episodic memory.Nat. Rev. Neurosci. 2017; 18: 183Crossref PubMed Scopus (59) Google Scholar]. Common to these accounts is that the PPC responds to a bottom-up mnemonic signal, and as reviewed in the main text, the most likely candidate to generate this signal is the hippocampus. By varying the interval of maintenance of a recalled episodic detail, fMRI data suggest that hippocampal engagement during successful recall is transient, whereas PPC engagement is sustained and covaries in time with the maintenance interval [102Vilberg K.L. Rugg M.D. The neural correlates of recollection: transient versus sustained fMRI effects.J. Neurosci. 2012; 32: 15679-15687Crossref PubMed Scopus (54) Google Scholar]. Moreover, a recent fMRI study found that mnemonic decodability in the PPC correlated with that in MTL regions [103Guidotti R. et al.Choice-predictive activity in parietal cortex during source memory decisions.Neuroimage. 2019; 189: 589-600Crossref PubMed Scopus (0) Google Scholar]. Both of these results are consistent with the notion that a hippocampal memory signal precedes and influences PPC engagement, although it is difficult to infer the exact temporal relationship between these regions based solely on fMRI dynamics. One recent study used fMRI in conjunction with source-reconstructed EEG/MEG and revealed a recall effect in the left precuneus from 600 to 1600 ms after cue onset [104Bergström Z.M. et al.Multimodal imaging reveals the spatiotemporal dynamics of recollection.Neuroimage. 2013; 68: 141-153Crossref PubMed Scopus (21) Google Scholar]. Human intracranial recordings from parietal regions are relatively rare compared with MTL coverage. Besides two studies using simple old/new recognition memory paradigms [29Rutishauser U. et al.Representation of retrieval confidence by single neurons in the human medial temporal lobe.Nat. Neurosci. 2015; 18: 1041Crossref PubMed Scopus (43) Google Scholar, 105Gonzalez A. et al.Electrocorticography reveals the temporal dynamics of posterior parietal cortical activity during recognition memory decisions.Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 11066-11071Crossref PubMed Scopus (0) Google Scholar], one study [106Foster B.L. et al.Neural populations in human posteromedial cortex display opposing responses during memory and numerical processing.Proc. Natl. Acad. Sci. U. S. A. 2012; 109: 15514-15519Crossref PubMed Scopus (37) Google Scholar] used an autobiographical memory task, more strongly reliant on recall processes. Pronounced engagement of the PPC was observed (high-gamma signal; 70–180 Hz), with an average onset of the parietal response at 600 ms. Together these studies suggest that PPC contributions unfold after the hippocampal recall process has begun. We speculate that there might be a push–pull relationship between the hippocampus and PPC. In particular, the hippocampus initiates cortical reinstatement in a bottom-up, holistic fashion [64Horner A.J. et al.Evidence for holistic episodic recollection via hippocampal pattern completion.Nat. Commun. 2015; 6: 7462Crossref PubMed Google Scholar], whereas the PPC aids and refines recall by deploying working memory/attentional resources to recover the task-relevant mnemonic features [107Kuhl B.A. et al.Dissociable neural mechanisms for goal-directed versus incidental memory reactivation.J. Neurosci. 2013; 33: 16099-16109Crossref PubMed Scopus (0) Google Scholar] (see Outstanding Questions). Given the extent of the structural and functional connectivity of the PPC not only with the hippocampus [108Wang J.X. et al.Targeted enhancement of cortical–hippocampal brain networks and associative memory.Science. 2014; 345: 1054-1057Crossref PubMed Scopus (0) Google Scholar] but also with a wide network of high-level cortical regions [109Raichle M.E. et al.A default mode of brain function.Proc. Natl Acad. Sci. U. S. A. 2001; 98: 676-682Crossref PubMed Scopus (0) Google Scholar, 110Schmahmann J.D. et al.Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography.Brain. 2007; 130: 630-653Crossref PubMed Scopus (658) Google Scholar, 111Silson E.H. et al.Distinct subdivisions of human medial parietal cortex support recollection of people and places.Elife. 2019; 8: e47391Crossref PubMed Scopus (0) Google Scholar], this region might be thought of as an additional, third layer in the multiplexed index for memory reinstatement (hippocampus → EC → PPC). This notion is corroborated by a recent MEG study showing enhanced connectivity between the MTL and precuneus during autobiographical memory retrieval [85Hebscher M. et al.A causal role for the precuneus in network-wide theta and gamma oscillatory activity during complex memory retrieval.Elife. 2019; 8: e43114Crossref PubMed Scopus (0) Google Scholar]. Experimental disruption of the precuneus via continuous theta burst stimulation diminished both MTL–cortical coupling and memory vividness, pointing to a potential role of the PPC in maintaining hippocampal–cortical communication in the service of successful recall. The question of how a simple cue can trigger recall of a past experience has a long history in computational models of memory. Following the seminal discovery that intact episodic memory critically relies on the hippocampus [1Scoville W.B. Milner B. Loss of recent memory after bilateral hippocampal lesions.J. Neurol. Neurosurg. Psychiatry. 1957; 20: 11-21Crossref PubMed Google Scholar], theoretical work has tried to link this region’s unique physiological properties to its putative role in coordinating memory recall [2Marr D. Simple memory: a theory for archicortex.Philos. Trans. R. Soc. Lond. B Biol. Sci. 1971; 262: 23-81Crossref PubMed Google Scholar, 3McNaughton B.L. Morris R.G. 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Hippocampal–neocortical interaction: a hierarchy of associativity.Hippocampus. 2000; 10: 420-430Crossref PubMed Scopus (0) Google Scholar]. Together, these properties put the hippocampus in a privileged position to orchestrate cued recall. Specifically, it is thought that during the initial experience, a particular set of hippocampal neurons coactivates with and is thereby linked to the cortical sites representing the constituents of the experience. The specific configuration of cortical sites (participating regions and activation profiles) forms the so-called engram [7Tonegawa S. et al.Memory engram cells have come of age.Neuron. 2015; 87: 918-931Abstract Full Text Full Text PDF PubMed Google Scholar]. As the cortical sites disengage/reconfigure to process new incoming information, the reciprocal link between hippocampal neurons and the cortical engram lives on in the form of strengthened synaptic weights, also referred to as the hippocampal index [5Teyler T.J. DiScenna P. The hippocampal memory indexing theory.Behav. Neurosci. 1986; 100: 147-154Crossref PubMed Google Scholar]. Later presentation of a subset of the engram (i.e., a partial cue) again propagates into the hippocampus, where the entire index is activated via autoassociative processes, thereby reinstating the complete cortical engram. A number of recent fMRI studies on cued recall have provided some empirical evidence for these computational accounts of hippocampal pattern completion and cortical reinstatement. Particularly, the advent of multivariate pattern analyses (MVPA) [8Norman K.A. et al.Beyond mind-reading: multi-voxel pattern analysis of fMRI data.Trends Cogn. Sci. 2006; 10: 424-430Abstract Full Text Full Text PDF PubMed Scopus (1328) Google Scholar], including representational similarity analysis and machine learning approaches, has yielded great progress in the assessment of memory-guided reinstatement. Not only have these methods consistently shown that cortical reinstatement is stronger during successful relative to unsuccessful recall, but activation levels in the hippocampus predict the extent of cortical reinstatement [9Bosch S.E. et al.Reinstatement of associative memories in early visual cortex is signaled by the hippocampus.J. Neurosci. 2014; 34: 7493-7500Crossref PubMed Scopus (49) Google Scholar, 10Gordon A.M. et al.Cortical reinstatement mediates the relationship between content-specific encoding activity and subsequent recollection decisions.Cereb. Cortex. 2013; 24: 3350-3364Crossref PubMed Scopus (46) Google Scholar, 11Ritchey M. et al.Neural similarity between encoding and retrieval is related to memory via hippocampal interactions.Cereb. Cortex. 2012; 23: 2818-2828Crossref PubMed Scopus (89) Google Scholar, 12Staresina B.P. et al.Episodic reinstatement in the medial temporal lobe.J. Neurosci. 2012; 32: 18150-18156Crossref PubMed Scopus (89) Google Scholar]. Regarding pattern completion in the hippocampus, fMRI evidence is scarcer, but a recent high-resolution fMRI study showed enhanced similarity of hippocampal encoding and retrieval activation patterns for successful versus unsuccessful cued recall [13Tompary A. et al.High-resolution investigation of memory-specific reinstatement in the hippocampus and perirhinal cortex.Hippocampus. 2016; 26: 995-1007Crossref PubMed Google Scholar] (see also [14Kok P. Turk-Browne N.B. Associative prediction of visual shape in the hippocampus.J. Neurosci. 2018; 38: 6888-6899Crossref PubMed Scopus (2) Google Scholar, 15Grande X. et al.Holistic recollection via pattern completion involves hippocampal subfield CA3.J. Neurosci. 2019; 39: 8100-8111Crossref PubMed Scopus (0) Google Scholar]). Together these findings are consistent with a hippocampal pattern completion process geared toward orchestrating cortical reinstatement. However, given the temporal ambiguity of the blood-oxygenation level-dependent (BOLD) signal, most of these findings would also be compatible with hippocampal activity following cortical reinstatement. Thus, to establish whether hippocampal engagement during memory recall indeed initiates reinstatement, real-time (i.e., millisecond precision) temporal resolution is needed. The most widely used method to glean real-time insights into human cognitive processes is noninvasive electrophysiological recordings via electroencephalography (EEG) or magnetoencephalography (MEG). Most early EEG investigations focused on different forms of recognition memory rather than cued recall per se. Specifically, event-related potentials (ERPs) were used to distinguish between familiarity-based and recollection-based recognition [16Yonelinas A.P. The nature of recollection and familiarity: a review of 30 years of research.J. Mem. Lang. 2002; 46: 441-517Crossref Scopus (2212) Google Scholar], with the latter being more akin to cued recall. In brief, an early (300–500 ms) frontal ERP has been linked to familiarity-based recognition, whereas a later (>500 ms) posterior ERP has been linked to recollection-based recognition [17Rugg M.D. Curran T. Event-related potentials and recognition memory.Trends Cogn. Sci. 2007; 11: 251-257Abstract Full Text Full Text PDF PubMed Scopus (698) Google Scholar]. (Note that we hereafter refer to onset latencies of significant differences between memory conditions or changes from baseline where this information is available.) These data hint toward different mnemonic processes being discernible via human electrophysiological recordings, with recall-related processes unfolding ∼500 ms after the reminder. However, given the ambiguities about neural generators of surface electrical/magnetic fields, the underlying brain regions – and the link to hippocampal signals in particular – have remained largely unknown. One methodological approach that overcomes many of the abovementioned modality-specific limitations is direct invasive recordings from the hippocampus and cortical target sites in human epilepsy patients [intracranial EEG (iEEG)] [18Parvizi J. Kastner S. Promises and limitations of human intracranial electroencephalography.Nat. Neurosci. 2018; 21: 474Crossref PubMed Scopus (0) Google Scholar]. The first set of iEEG studies on memory employed simple old/new recognition tests, revealing an initial response peaking around 400 ms in the entorhinal cortex (EC)/perirhinal cortex and distinguishing correctly identified old from new stimuli (for a review see [19Fernández G. Tendolkar I. The rhinal cortex: ‘gatekeeper’ of the declarative memory system.Trends Cogn. 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However, the simple comparison of old versus new stimuli leaves open whether this response reflects a novelty signal or recall of episodic details associated with the old stimulus. An iEEG study designed to distinguish between old/new discrimination and associative retrieval (cued recall) indicated the latter. ERPs were derived for: (i) new items [correct rejection (CR)]; (ii) recognised old items without recalling associative details [item recognition (IR)]; and (iii) recognised old items and recalling associative details [associative recognition (AR)]. Hippocampal ERPs showed an associative recall effect (AR > IR) most pronounced between 500 and 1500 ms [23Staresina B.P. et al.Memory signals are temporally dissociated in and across human hippocampus and perirhinal cortex.Nat. Neurosci. 2012; 15: 1167Crossref PubMed Scopus (74) Google Scholar]. 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