Prestimulus hippocampal activity predicts later recollection

Functional magnetic resonance imaging (fMRI) was used to address the question whether medial temporal lobe (MTL) activity prior to a stimulus event is predictive of whether the event will be successfully encoded in an incidental study task. Participants were scanned while making pleasantness judgments on words presented either in written or spoken form. A cue presented at a variable interval before the onset of each word signaled the modality of the upcoming item. Following the study phase, a surprise recognition memory test was administered that required items to be endorsed as “Remembered,” “Known,” or “New.” Activity in the MTL, including the hippocampus, differed during the cue‐item interval according to whether the item was later endorsed as Remembered rather than judged as Known or New. Thus, the level of hippocampal activity prior to the onset of an event predicts whether the event will be successfully encoded into episodic memory. © 2009 Wiley‐Liss, Inc.     

Selective and shared contributions of the hippocampus and perirhinal cortex to episodic item and associative encoding

Although the general role of the medial-temporal lobe (MTL) in episodic memory is well established, controversy surrounds the precise division of labor between distinct MTL subregions. The perirhinal cortex (PrC) has been hypothesized to support nonassociative item encoding that contributes to later familiarity, whereas the hippocampus supports associative encoding that selectively contributes to later recollection. However, because previous paradigms have predominantly used recollection of the item context as a measure of associative encoding, it remains unclear whether recollection of different kinds of episodic detail depends on the same or different MTL encoding operations. In our current functional magnetic resonance imaging study, we devised a subsequent memory paradigm that assessed successful item encoding in addition to the encoding of two distinct episodic details: an item-color and an item-context detail. Hippocampal encoding activation was selectively enhanced during trials leading to successful recovery of either an item-color or item-context association. Moreover, the magnitude of hippocampal activation correlated with the number, and not the kind, of associated details successfully bound, providing strong evidence for a role of the hippocampus in domain-general associative encoding. By contrast, PrC encoding activation correlated with both nonassociative item encoding as well as associative item-color binding, but not with item-context binding. This pattern suggests that the PrC contributions to memory encoding may be domain-specific and limited to the binding of items with presented item-related features. Critically, together with a separately conducted behavioral study, these data raise the possibility that PrC encoding operations -- in conjunction with hippocampal mechanisms -- contribute to later recollection of presented item details.     

The relationship between task‐related and subsequent memory effects

The primary aim of this fMRI study was to assess the proposal that negative subsequent memory effects—greater activity for later forgotten relative to later remembered study items—are localized to regions demonstrating task‐negative effects, and hence to potential components of the default mode network. Additionally, we assessed whether positive subsequent memory effects overlapped with regions demonstrating task‐positive effects. Eighteen participants were scanned while they made easy or difficult relational judgments on visually presented word pairs. Easy and hard task blocks were interleaved with fixation‐only rest periods. In the later unscanned test phase, associative recognition judgments were required on intact word pairs (studied pairs), rearranged pairs (pairs formed from words presented on different study trials) and new pairs. Subsequent memory effects were identified by contrasting the activity elicited by study pairs that went on to be correctly endorsed as intact versus incorrectly endorsed as rearranged. Task effects were identified by contrasting all study items and rest blocks. Both task‐negative and task‐positive effects were evident in widespread cortical regions and negative and positive subsequent memory effects were generally confined to task‐negative and task‐positive regions respectively. However, subsequent memory effects could be identified in only a fraction of task‐sensitive voxels and, unlike task effects, were insensitive to the difficulty manipulation. The findings for the negative subsequent memory effects are consistent with recent proposals that the default mode network is functionally heterogeneous, and suggest that these effects are not accurately characterized as reflections of the modulation of the network as a whole. Hum Brain Mapp 35:3687–3700, 2014. © 2013 Wiley Periodicals, Inc .     

Recollection‐related hippocampal activity during continuous recognition: A high‐resolution fMRI study

We used high‐resolution functional magnetic resonance imaging to investigate whether successful recollection during continuous recognition is associated with relative enhancement of hippocampal activity, consistent with prior findings from experiments employing separate study and test phases. While being scanned, subjects discriminated between new and repeated pictures. Each picture, which was repeated once after an interval of between 10 and 30 items, was surrounded by a frame that was colored gray, blue, or orange. When an item repeated, its frame color determined the correct response. Repeated items surrounded by a gray frame always required an “old” judgment. A repeated item surrounded by a blue or an orange frame required a different response depending whether it was represented in the same (Target) or a different (Nontarget) color from the first presentation. Consistent with the results from previous continuous recognition experiments, robust new > old effects were found in bilateral hippocampus. In addition, an across‐subjects correlational analysis identified a cluster of voxels in right hippocampus where recollection‐related activity (operationalized by the contrast between correctly vs. incorrectly judged Nontargets) was positively correlated with recollection performance. Thus, successful recollection during continuous recognition is associated with a relative enhancement of hippocampal activity. © 2010 Wiley‐Liss, Inc.     

Intracranial EEG correlates of implicit relational inference within the hippocampus

Drawing inferences from past experiences enables adaptive behavior in future situations. Inference has been shown to depend on hippocampal processes. Usually, inference is considered a deliberate and effortful mental act which happens during retrieval, and requires the focus of our awareness. Recent fMRI studies hint at the possibility that some forms of hippocampus‐dependent inference can also occur during encoding and possibly also outside of awareness. Here, we sought to further explore the feasibility of hippocampal implicit inference, and specifically address the temporal evolution of implicit inference using intracranial EEG. Presurgical epilepsy patients with hippocampal depth electrodes viewed a sequence of word pairs, and judged the semantic fit between two words in each pair. Some of the word pairs entailed a common word (e.g., “winter–red,” “red–cat”) such that an indirect relation was established in following word pairs (e.g., “winter–cat”). The behavioral results suggested that drawing inference implicitly from past experience is feasible because indirect relations seemed to foster “fit” judgments while the absence of indirect relations fostered “do not fit” judgments, even though the participants were unaware of the indirect relations. A event‐related potential (ERP) difference emerging 400 ms post‐stimulus was evident in the hippocampus during encoding, suggesting that indirect relations were already established automatically during encoding of the overlapping word pairs. Further ERP differences emerged later post‐stimulus (1,500 ms), were modulated by the participants' responses and were evident during encoding and test. Furthermore, response‐locked ERP effects were evident at test. These ERP effects could hence be a correlate of the interaction of implicit memory with decision‐making. Together, the data map out a time‐course in which the hippocampus automatically integrates memories from discrete but related episodes to implicitly influence future decision making. © 2015 Wiley Periodicals, Inc.     

Novelty preference in patients with developmental amnesia

To re‐examine whether or not selective hippocampal damage reduces novelty preference in visual paired comparison (VPC), we presented two different versions of the task to a group of patients with developmental amnesia (DA), each of whom sustained this form of pathology early in life. Compared with normal control participants, the DA group showed a delay‐dependent reduction in novelty preference on one version of the task and an overall reduction on both versions combined. Because VPC is widely considered to be a measure of incidental recognition, the results appear to support the view that the hippocampus contributes to recognition memory. A difficulty for this conclusion, however, is that according to one current view the hippocampal contribution to recognition is limited to task conditions that encourage recollection of an item in some associated context, and according to another current view, to recognition of an item with the high confidence judgment that reflects a strong memory. By contrast, VPC, throughout which the participant remains entirely uninstructed other than to view the stimuli, would seem to lack such task conditions and so would likely lead to recognition based on familiarity rather than recollection or, alternatively, weak memories rather than strong. However, before concluding that the VPC impairment therefore contradicts both current views regarding the role of the hippocampus in recognition memory, two possibilities that would resolve this issue need to be investigated. One is that some variable in VPC, such as the extended period of stimulus encoding during familiarization, overrides its incidental nature, and, because this condition promotes either recollection‐ or strength‐based recognition, renders the task hippocampal‐dependent. The other possibility is that VPC, rather than providing a measure of incidental recognition, actually assesses an implicit, information‐gathering process modulated by habituation, for which the hippocampus is also partly responsible, independent of its role in recognition. © 2010 Wiley Periodicals, Inc.     

Neural correlates of encoding within- and across-domain inter-item associations

The neural correlates of the encoding of associations between pairs of words, pairs of pictures, and word-picture pairs were compared. The aims were to determine, first, whether the neural correlates of associative encoding vary according to study material and, second, whether encoding of across- versus within-material item pairs is associated with dissociable patterns of hippocampal and perirhinal activity, as predicted by the "domain dichotomy" hypothesis of medial temporal lobe function. While undergoing fMRI scanning, subjects (n = 24) were presented with the three classes of study pairs, judging which of the denoted objects fit into the other. Outside of the scanner, subjects then undertook an associative recognition task, discriminating between intact study pairs, rearranged pairs comprising items that had been presented on different study trials, and unstudied item pairs. The neural correlates of successful associative encoding--subsequent associative memory effects--were operationalized as the difference in activity between study pairs correctly judged intact versus pairs incorrectly judged rearranged on the subsequent memory test. Pair type-independent subsequent memory effects were evident in the left inferior frontal gyrus (IFG) and the hippocampus. Picture-picture pairs elicited material-selective effects in regions of fusiform cortex that were also activated to a greater extent on picture trials than on word trials, whereas word-word pairs elicited material-selective subsequent memory effects in left lateral temporal cortex. Contrary to the domain-dichotomy hypothesis, neither hippocampal nor perirhinal subsequent memory effects differed depending on whether they were elicited by within- versus across-material study pairs. It is proposed that the left IFG plays a domain-general role in associative encoding, that associative encoding can also be facilitated by enhanced processing in material-selective cortical regions, and that the hippocampus and perirhinal cortex contribute equally to the formation of inter-item associations, regardless of whether the items belong to the same or to different processing domains.     

Fractionation of the component processes underlying successful episodic encoding: a combined fMRI and divided-attention study

Considerable evidence suggests that attentional resources are necessary for the encoding of episodic memories, but the nature of the relationship between attention and neural correlates of encoding is unclear. Here we address this question using functional magnetic resonance imaging and a divided-attention paradigm in which competition for different types of attentional resources was manipulated. Fifteen volunteers were scanned while making animacy judgments to visually presented words and concurrently performing one of three tasks on auditorily presented words: male/female voice discrimination (control task), 1-back voice comparison (1-back task), or indoor/outdoor judgment (semantic task). The 1-back and semantic tasks were designed to compete for task-generic and task-specific attentional resources, respectively. Using the "remember/know" procedure, memory for the study words was assessed after 15 min. In the control condition, subsequent memory effects associated with later recollection were identified in the left dorsal inferior frontal gyrus and in the left hippocampus. These effects were differentially attenuated in the two more difficult divided-attention conditions. The effects of divided attention seem, therefore, to reflect impairments due to limitations at both task-generic and task-specific levels. Additionally, each of the two more difficult divided-attention conditions was associated with subsequent memory effects in regions distinct from those showing effects in the control condition. These findings suggest the engagement of alternative encoding processes to those engaged in the control task. The overall pattern of findings suggests that divided attention can impact later memory in different ways, and accordingly, that different attentional resources, including task-generic and task-specific resources, make distinct contributions to successful episodic encoding.     

Neural bases of autobiographical support for episodic recollection of faces

Incidental retrieval of autobiographical knowledge can provide rich contextual support for episodic recollection of a recent event. We examined the neural bases of these two processes by performing fMRI scanning during a recognition memory test for faces that were unfamiliar, famous, or personally known. The presence of pre‐experimental knowledge of a face was incidental to the task, but nonetheless resulted in improved performance. Two distinct networks of activation were associated with correct recollection of a face's prior presentation (recollection hits vs. correct rejections) on one hand, and with pre‐experimental knowledge about it (famous or personally known vs. unfamiliar faces) on the other. The former included mid/posterior cingulate cortex, precuneus, and ventral striatum. The latter included bilateral hippocampus, retrosplenial, and ventromedial prefrontal cortices. Anterior and medial thalamic activations showed an interaction between both effects, driven by increased activation for recollection of unfamiliar faces. When recollecting the presentation of a famous or personally known face, hippocampal activation increased with participants' ratings of how well they felt they knew the person shown. Ventromedial prefrontal cortex showed significantly greater activation for personally known than famous faces. Our results indicate a dissociation between the involvement of retrosplenial vs. mid/posterior cingulate and precuneus in memory tasks. They also indicate that, during recognition memory experiments, the hippocampus supports incidental retrieval of pre‐experimental knowledge about the stimuli presented. This type of knowledge likely underlies the additional recollection found for prior presentation of well known stimuli compared with novel ones and may link hippocampal activation at encoding to subsequent memory performance more generally. © 2009 Wiley‐Liss, Inc.     

Electrophysiological signature of working and long‐term memory interaction in the human hippocampus

Recent findings indicate that the hippocampus is not only crucial for long‐term memory (LTM) encoding, but plays a role for working memory (WM) as well. In particular, it has been shown that the hippocampus is important for WM maintenance of multiple items or associations between item features. Previous studies using intracranial electroencephalography recordings from the hippocampus of patients with epilepsy revealed slow positive potentials during maintenance of a single item and during LTM encoding, but slow negative potentials during maintenance of multiple items. These findings predict that WM maintenance of multiple items interferes with LTM encoding, because these two processes are associated with slow potentials of opposing polarities in the hippocampus. Here, we tested this idea in a dual‐task paradigm involving a LTM encoding task nested into a WM Sternberg task with either a low (one item) or a high (three items) memory load. In the high WM load condition, LTM encoding was significantly impoverished, and slow hippocampal potentials were more negative than in the low WM load condition. Time‐frequency analysis revealed that a reduction of slow hippocampal activity in the delta frequency range supported LTM formation in the low load condition, but not during high WM load. Together, these findings indicate that multi‐item WM and LTM encoding interfere within the hippocampus.     

Spatial reconstruction by patients with hippocampal damage is dominated by relational memory errors

Hippocampal damage causes profound yet circumscribed memory impairment across diverse stimulus types and testing formats. Here, within a single test format involving a single class of stimuli, we identified different performance errors to better characterize the specifics of the underlying deficit. The task involved study and reconstruction of object arrays across brief retention intervals. The most striking feature of patients' with hippocampal damage performance was that they tended to reverse the relative positions of item pairs within arrays of any size, effectively “swapping” pairs of objects. These “swap errors” were the primary error type in amnesia, almost never occurred in healthy comparison participants, and actually contributed to poor performance on more traditional metrics (such as distance between studied and reconstructed location). Patients made swap errors even in trials involving only a single pair of objects. The selectivity and severity of this particular deficit creates serious challenges for theories of memory and hippocampus. © 2013 Wiley Periodicals, Inc.     

fMRI evidence for separable and lateralized prefrontal memory monitoring processes

Source memory research suggests that attempting to remember specific contextual aspects surrounding prior stimulus encounters results in greater left prefrontal cortex (PFC) activity than simple item-based old/new recognition judgments. Here, we tested a complementary hypothesis that predicts increases in the right PFC with tasks requiring close monitoring of item familiarity. More specifically, we compared a judgment of frequency (JOF) task to an item memory task, in which the former required estimating the number of previous picture encounters and the latter required discriminating old from new exemplars of previously seen items. In comparison to standard old/new recognition, both source memory and the JOF task examined here require more precise mnemonic judgments. However, in contrast to source memory, cognitive models suggest the JOF task relies heavily upon item familiarity, not specific contextual recollections. Event-related fMRI demonstrated greater recruitment of right, not left, dorsolateral and frontopolar PFC regions during the JOF compared to item memory task. These data suggest a role for right PFC in the close monitoring of the familiarity of objects, which becomes critical when contextual recollection is ineffective in satisfying a memory demand.     

Recognition memory for single items and for associations in amnesic patients

Recognition memory performance reflects two distinct processes or types of memory referred to as recollection and familiarity. According to theoretical claims about the two types of memory, single item and associative recognition tasks can be used as an experimental method to distinguish recollection and familiarity processes. Associative recognition decisions can be used as an index of recollection while memory for single items is mostly based on familiarity judgement. We employed this procedure to examine a possible dissociation in the memory performance of amnesic patients between spared single item and impaired associative recognition. Twelve amnesic patients, six with damage confined to the hippocampus proper, and six with damage elsewhere in the brain, were recruited for the present study. The findings showed that hippocampal amnesics exhibit relative sparing of single item learning but are consistently deficient in the learning of all kinds of between-item associations. These results are consistent with the view that hippocampal formation contributes differently to declarative tasks that require recollective or familiarity processes.     

A role for perirhinal cortex in memory for novel object-context associations

It is debated whether functional divisions between structures in the medial temporal lobe (MTL), in particular the perirhinal cortex (PrC) and hippocampus (HC), are best conceptualized according to memory process (Diana et al., 2007; Ranganath, 2010; Wixted et al., 2010) or stimulus category (Graham et al., 2010). In the former account, PrC is critical for item familiarity but not recollection of associations between items and their contexts (which is instead dependent upon the HC; Ranganath et al., 2004). In the latter theory, complex object representations in PrC are capable of supporting memory for objects as well as for object-context associations, particularly when there is a demand to discriminate between highly visually similar objects (Cowell et al., 2010). To adjudicate between these accounts, human participants were scanned while making two different judgments about visually presented objects (is the object common or uncommon, or does the object have more edges or curves). In a subsequent, unscanned, retrieval phase, participants made item (old/new) followed by context (encoding task) judgments about previously seen and novel objects. Neural activity at encoding was separated according to the accuracy of the retrieval judgments. PrC activity predicted successful item-context judgments, a result that remained when item-memory strength was equated across objects for which the context was remembered or forgotten. These data imply that the function of PrC goes beyond processing item-based memory information, contributing additionally to memory for item-context associations when the stimuli are objects (Graham et al., 2010).     

Medial temporal lobe function and recognition memory: a novel approach to separating the contribution of recollection and familiarity

Human neuroimaging studies of recognition memory have often been interpreted to mean that the hippocampus supports recollection but not familiarity. This interpretation is complicated by the fact that recollection-based decisions are typically associated with stronger memories than familiarity-based decisions. Some studies of source memory controlled for this difference in memory strength and found that hippocampal activity during learning predicted subsequent item memory strength while recollection-based memory (performance on source memory questions) was held at chance. This result suggests that the hippocampus is important for familiarity. However, a difficulty with this approach is that when source memory is assessed by asking specific, task-relevant source memory questions, participants who fail to answer the prescribed questions might nevertheless have available other (task-irrelevant) source information. Accordingly, successful item memory could still be associated with recollection. The present study used a novel method to assess item memory and source memory. Instead of responding to specific source questions, participants rated their source memory strength based on any information about the learning episode that was available to them. When subsequent source memory strength was held constant at the lowest possible level, we identified regions bilaterally in hippocampus, as well as in perirhinal cortex, where activity during learning increased as subsequent item memory increased in strength. In addition, activity in cortical regions (including prefrontal cortex) was related to source memory success independently of item memory strength. These findings suggest that activity in the hippocampus is related to the encoding of familiarity-based item memory, independent of subsequent recollection-based success.     

Memory orientation and success: separable neurocognitive components underlying episodic recognition

Episodic recognition can be based on recollection of contextual details, on a sense of recent encounter, or some combination of the two. According to several cognitive models, selectively attending to these distinct aspects of memory may require different retrieval orientations and result in different neural responses depending upon whether or not retrieval is successful. Using event-related fMRI, we examined retrieval orientation by having subjects discriminate between two test words in one of two manners. During source recollection, they selected the member of the pair previously associated with a particular encoding task. In contrast, recency judgment required selection of the most recently encountered item of the pair, regardless of how it had been encoded. Furthermore, successful and unsuccessful trials within each retrieval task were contrasted to determine whether retrieval success effects occurred in overlapping or dissimilar neural populations compared to those associated with each retrieval orientation. The results revealed distinct lateral prefrontal and parietal activations that distinguished attempted source recollection from judgments of relative recency; these orientation effects were largely independent of retrieval success. In contrast, medial temporal lobe structures (hippocampus and parahippocampal gyrus) were differentially more active during successful recollection of encoding context, showing similar reduced responses during failed source recollection and judgments of recency. These results indicate that different memory orientations recruit distinct prefrontal and parietal networks and that the recovery of episodic context is associated with the hippocampus and surrounding medial temporal cortices.     

Hippocampal Theta Oscillations Support Successful Associative Memory Formation

Models of memory formation posit that episodic memory formation depends critically on the hippocampus, which binds features of an event to its context. For this reason, the contrast between study items that are later recollected with their associative pair versus those for which no association is made fails should reveal electrophysiological patterns in the hippocampus selectively involved in associative memory encoding. Extensive data from studies in rodents support a model in which theta oscillations fulfill this role, but results in humans have not been as clear. Here, we used an associative recognition memory procedure to identify hippocampal correlates of successful associative memory encoding and retrieval in patients (10 females and 9 males) undergoing intracranial EEG monitoring. We identified a dissociation between 2–5 Hz and 5–9 Hz theta oscillations, by which power increases in 2–5 Hz oscillations were uniquely linked with successful associative memory in both the anterior and posterior hippocampus. These oscillations exhibited a significant phase reset that also predicted successful associative encoding and distinguished recollected from nonrecollected items at retrieval, as well as contributing to relatively greater reinstatement of encoding-related patterns for recollected versus nonrecollected items. Our results provide direct electrophysiological evidence that 2–5 Hz hippocampal theta oscillations preferentially support the formation of associative memories, although we also observed memory-related effects in the 5–9 Hz frequency range using measures such as phase reset and reinstatement of oscillatory activity.SIGNIFICANCE STATEMENT Models of episodic memory encoding predict that theta oscillations support the formation of interitem associations. We used an associative recognition task designed to elicit strong hippocampal activation to test this prediction in human neurosurgical patients implanted with intracranial electrodes. The findings suggest that 2–5 Hz theta oscillatory power and phase reset in the hippocampus are selectively associated with associative memory judgments. Furthermore, reinstatement of oscillatory patterns in the hippocampus was stronger for successful recollection. Collectively, the findings support a role for hippocampal theta oscillations in human associative memory.     

Assessing recollection and familiarity of similar lures in a behavioral pattern separation task

The relationship between recollection‐mediated recognition memory and behavioral pattern separation is poorly understood. In two separate experiments, we modified a well‐validated object discrimination task with previously demonstrated sensitivity to neural pattern separation with instructions to assess recollection and familiarity. In the first experiment, we included a Remember/Know (R/K) judgment, and in the second we included a source memory judgment. We found that both “Remember” and correct source judgments were higher for lures labeled “similar” (where pattern separation is engaged) but also higher on lures called “old” (where pattern separation is absent), suggesting that false alarms in pattern separation tasks are frequently mediated by recollection. As one might expect, “Remember” judgments and correct source decisions increased with greater dissimilarity for “similar” responses and increased with greater similarity for “old” responses. This suggests that recollection can occur in the presence and in the absence of pattern separation and that false alarms to similar lures are not simply driven by familiarity. © 2013 Wiley Periodicals, Inc.     

Prediction of memory formation based on absolute electroencephalographic phases in rhinal cortex and hippocampus outperforms prediction based on stimulus‐related phase shifts

Absolute (i.e. measured) rhinal and hippocampal phase values are predictive for memory formation. It has been an open question, whether the capability of mediotemporal structures to react to stimulus presentation with phase shifts may be similarly indicative of successful memory formation. We analysed data from 27 epilepsy patients implanted with depth electrodes in the hippocampus and entorhinal cortex, who performed a continuous word recognition task. Electroencephalographic phase information related to the first presentation of repeatedly presented words was used for prediction of subsequent remembering vs. forgetting applying a support vector machine. The capability to predict successful memory formation based on stimulus‐related phase shifts was compared to that based on absolute phase values. Average hippocampal phase shifts were larger and rhinal phase shifts were more accumulated for later remembered compared to forgotten trials. Nevertheless, prediction based on absolute phase values clearly outperformed phase shifts and there was no significant increase in prediction accuracies when combining both measures. Our findings indicate that absolute rhinal and hippocampal phases and not stimulus‐related phase shifts are most relevant for successful memory formation. Absolute phases possibly affect memory formation via influencing neural membrane potentials and thereby controlling the timing of neural firing.     

Reconstructing relational information

Hippocampal involvement in learning and remembering relational information has an extensive history, often focusing specifically on spatial information. In humans, spatial reconstruction (SR) paradigms are a powerful tool for evaluating an individuals' spatial‐relational memory. In SR tasks, participants study locations of items in space and subsequently reconstruct the studied display after a short delay. Previous work has revealed that patients with hippocampal damage are impaired both in overall placement accuracy as well as on a specific measure of relational memory efficacy, “swaps” (i.e., when the relative location of two items is reversed). However, the necessity of the hippocampus for other types of spatial‐relational information involved in reconstruction behaviors (e.g., where in the environment and relative to which other items an item was located) have not yet been investigated systematically. In this work, three patients with hippocampal damage and nine healthy matched comparison participants performed an SR task. An analysis framework was developed to independently assess three first‐order types of relations: (1) memory for the binding of specific item identities to locations, (2) memory for arrangement of items in relation to each other or the environment bounds, regardless of memory for the item identity, and (3) higher‐order, compound relational errors (i.e., errors involving multiple pieces of relational information). Reconstruction errors were evaluated to determine the degree to which patients and comparisons differed (or not) on each type of spatial‐relational information. Data revealed that the primary group difference in performance was for identity‐location information. However, when the locations of items were evaluated without regarding the identities, no group difference was found in the number of item placements to studied locations. The present work provides a principled approach to analysis of SR data and clarifies our understanding of the types of spatial relations impaired in hippocampal damaged.