Reflections on Conversations and Memory

The study of memory and remembering has traditionally either stripped meaning away from acts of remembering to reveal the “raw material of memory” or explored how meaning guides the reconstruction of the past. In reflecting on the contributions to this topic, there appears to be an emerging “third‐way,” which holds that there is an inextricable relation between conversations and remembering. The articles in this volume exemplify how conversing is often an act of remembering and represent approaches to memory that might not otherwise be taken if one were to study memory as a within‐individual phenomenon. The implications of this approach are far‐ranging and present the opportunity to pose new questions about the nature of remembering as it unfolds in conversation. The contributing articles have expanded the scope of what memory researchers can study by adopting a relatively straightforward assumption about the sociality of remembering and the role of the conversation in the social process.     

Faces are special but not too special: Spared face recognition in amnesia is based on familiarity

Most current theories of human memory are material-general in the sense that they assume that the medial temporal lobe (MTL) is important for retrieving the details of prior events, regardless of the specific type of materials. Recent studies of amnesia have challenged the material-general assumption by suggesting that the MTL may be necessary for remembering words, but is not involved in remembering faces. We examined recognition memory for faces and words in a group of amnesic patients, which included hypoxic patients and patients with extensive left or right MTL lesions. Recognition confidence judgments were used to plot receiver operating characteristics (ROCs) in order to more fully quantify recognition performance and to estimate the contributions of recollection and familiarity. Consistent with the extant literature, an analysis of overall recognition accuracy showed that the patients were impaired at word memory but had spared face memory. However, the ROC analysis indicated that the patients were generally impaired at high confidence recognition responses for faces and words, and they exhibited significant recollection impairments for both types of materials. Familiarity for faces was preserved in all patients, but extensive left MTL damage impaired familiarity for words. These results show that face recognition may appear to be spared because performance tends to rely heavily on familiarity, a process that is relatively well preserved in amnesia. In addition, the findings challenge material-general theories of memory, and suggest that both material and process are important determinants of memory performance in amnesia.     

Prefrontal cortex activity associated with source monitoring in a working memory task

Using functional magnetic resonance imaging (fMRI), we investigated prefrontal cortex (PFC) activity during remembering specific source information (format, location judgments) versus remembering that could be based on undifferentiated information, such as familiarity (old/new recognition [ON], recency judgments). A working memory (WM) paradigm with an immediate test yielded greater activation in the lateral PFC for format and location source memory (SM) tasks than ON recognition; this SM-related activity was left lateralized. The same regions of PFC were recruited in Experiment 2 when information was tested immediately and after a filled delay. Substituting recency for location judgments (Experiment 3) resulted in an overall shift in task context that produced greater right PFC activity associated with ON and recency tasks compared to the format task, in addition to left SM-related activity. These data extend to WM previous findings from long-term memory (LTM) indicating that the left and right PFC may be differentially involved in memory attributions depending on the specificity of information evaluated. The findings also provide evidence for the continuity of evaluative processes recruited in WM and LTM.     

Early episodic memory impairments in Alzheimer's disease

Patients with Alzheimer's disease (AD) show early episodic memory impairments. Such deficits reflect specific impairments affecting one or several stages of encoding, storage and retrieval processes. However, AD patients not only have great difficulty retrieving memories and information but also suffer from distortions of memory, as intrusions and false recognitions. Intrusions can be defined as the unintentional recall of inappropriate information in a laboratory-learning tasks such as word-list recall and story recall. False recognition refers to the erroneous recognition of information that was not previously presented. The first objective of this review is to present studies from the literature that allowed a better understanding of the nature of episodic memory deficits in AD, and to examine recent research on false memories. The second part of this review is aimed at presenting recent research conducted on prospective memory (PM) in Alzheimer's disease. Prospective memory situations involve forming intentions and then realizing those intentions at some appropriate time in the future. Everyday examples of prospective memory include remembering to buy bread on the way home from work, remembering to give friends a message upon next encountering them, and remembering to take medication. Patients suffering from AD show difficulties in performing prospective tasks in daily life, according to the complaints of their care givers, and these difficulties are massively present at the first stages of the disease. Nevertheless, very few studies have been dedicated to this subject, although the evaluation of PM could be helpful for the early diagnosis of AD.     

Age-related declines in prospective memory: behavioral and electrophysiological evidence

Prospective remembering reflects the ability of an individual to form and later realize intentions that must be delayed over minutes, hours, or days. A substantial body of literature, primarily based upon the findings of behavioral studies, indicates that there are robust declines in the efficiency of prospective remembering in later adulthood. However, the cognitive and neural mechanisms mediating age-related deficits in prospective remembering are not well understood. In this review we consider evidence from recent behavioral and electrophysiological studies indicating that decreases in the efficiency of prospective memory in older adults results from age-related differences in those neural mechanisms supporting the encoding of intentions into memory and the detection of prospective memory cues in the environment.     

Memorial familiarity remains intact for pictures but not for words in patients with amnestic mild cognitive impairment

Understanding how memory breaks down in the earliest stages of Alzheimer's disease (AD) process has significant implications, both clinically and with respect to intervention development. Previous work has highlighted a robust picture superiority effect in patients with amnestic mild cognitive impairment (aMCI). However, it remains unclear as to how pictures improve memory compared to words in this patient population. In the current study, we utilized receiver operating characteristic (ROC) curves to obtain estimates of familiarity and recollection for pictures and words in patients with aMCI and healthy older controls. Analysis of accuracy shows that even when performance is matched between pictures and words in the healthy control group, patients with aMCI continue to show a significant picture superiority effect. The results of the ROC analysis showed that patients demonstrated significantly impaired recollection and familiarity for words compared controls. In contrast, patients with aMCI demonstrated impaired recollection, but intact familiarity for pictures, compared to controls. Based on previous work from our lab, we speculate that patients can utilize the rich conceptual information provided by pictures to enhance familiarity, and perceptual information may allow for post-retrieval monitoring or verification of the enhanced sense of familiarity. Alternatively, the combination of enhanced conceptual and perceptual fluency of the test item might drive a stronger or more robust sense of familiarity that can be accurately attributed to a studied item.     

NEREC,an effective brain mapping protocol for combined language and long-term memory functions

Temporal lobe epilepsy can induce functional plasticity in temporoparietal networks involved in language and long-term memory processing. Previous studies in healthy subjects have revealed the relative difficulty for this network to respond effectively across different experimental designs, as compared to more reactive regions such as frontal lobes. For a protocol to be optimal for clinical use, it has to first show robust effects in a healthy cohort. In this study, we developed a novel experimental paradigm entitled NEREC, which is able to reveal the robust participation of temporoparietal networks in a uniquely combined language and memory task, validated in an fMRI study with healthy subjects. Concretely, NEREC is composed of two runs: (a) an intermixed language-memory task (confrontation naming associated with encoding in nonverbal items, NE) to map language (i.e., word retrieval and lexico-semantic processes) combined with simultaneous long-term verbal memory encoding (NE items named but also explicitly memorized) and (b) a memory retrieval task of items encoded during NE (word recognition, REC) intermixed with new items. Word recognition is based on both perceptual-semantic familiarity (feeling of ‘know’) and accessing stored memory representations (remembering). In order to maximize the remembering and recruitment of medial temporal lobe structures, we increased REC difficulty by changing the modality of stimulus presentation (from nonverbal during NE to verbal during REC). We report that (a) temporoparietal activation during NE was attributable to both lexico-semantic (language) and memory (episodic encoding and semantic retrieval) processes; that (b) encoding activated the left hippocampus, bilateral fusiform, and bilateral inferior temporal gyri; and that (c) task recognition (recollection) activated the right hippocampus and bilateral but predominant left fusiform gyrus. The novelty of this protocol consists of (a) combining two tasks in one (language and long-term memory encoding/recall) instead of applying isolated tasks to map temporoparietal regions, (b) analyzing NE data based on performances recorded during REC, (c) double-mapping networks involved in naming and in long-term memory encoding and retrieval, (d) focusing on remembering with hippocampal activation and familiarity judgment with lateral temporal cortices activation, and (e) short duration of examination and feasibility. These aspects are of particular interest in patients with TLE, who frequently show impairment of these cognitive functions. Here, we show that the novel protocol is suited for this clinical evaluation.     

Recollection and familiarity make independent contributions to memory judgments

Recognition memory can be supported by the processes of recollection and familiarity. Recollection is recovery of qualitative information about a prior event. Familiarity is a scalar strength signal that permits judgments of prior occurrence. There is vigorous debate about how these processes are conceptualized, how they contribute to memory judgments, and which brain regions support them. One popular method for investigating these questions is the Remember/Know procedure, where subjects give a Remember response to studied stimuli for which they can recover contextual details of the study encounter, and a Know response when details are not recovered but subjects nevertheless believe that a stimulus was studied. According to one model, Remember responses are strong memories that are typically associated with relatively high levels of recollection and familiarity. Know responses are weaker memories and are typically associated with lower levels of both processes. Data inconsistent with this account were obtained in this experiment, where magnetoencephalographic (MEG) measures of neural activity were acquired in the test phase of a verbal memory task where healthy human volunteers made Remember, Know, or New judgments to studied and unstudied words. An MEG index of the process of recollection was larger for Remember than Know judgments, whereas the reverse was true for a MEG index of familiarity. Critically, this result is predicted by a model where recollection and familiarity make independent contributions to Remember and Know judgments, and provides a powerful constraint when mapping memory processes onto their neural substrates.     

Aging reduces veridical remembering but increases false remembering: Neuropsychological test correlates of remember-know judgments

In 1985 Tulving introduced the remember-know procedure, whereby subjects are asked to distinguish between memories that involve retrieval of contextual details (remembering) and memories that do not (knowing). Several studies have been reported showing age-related declines in remember hits, which has typically been interpreted as supporting dual-process theories of cognitive aging that align remembering with a recollection process and knowing with a familiarity process. Less attention has been paid to remember false alarms, or their relation to age. We reviewed the literature examining aging and remember/know judgments and show that age-related increases in remember false alarms, i.e., false remembering, are as reliable as age-related decreases in remember hits, i.e., veridical remembering. Moreover, a meta-analysis showed that the age effect size for remember hits and false alarms are similar, and larger than age effects on know hits and false alarms. We also show that the neuropsychological correlates of remember hits and false alarms differ. Neuropsychological tests of medial-temporal lobe functioning were related to remember hits, but tests of frontal-lobe functioning and age were not. By contrast, age and frontal-lobe functioning predicted unique variance in remember false alarms, but MTL functioning did not. We discuss various explanations for these findings and conclude that any comprehensive explanation of recollective experience will need to account for the processes underlying both remember hits and false alarms.     

Electromagnetic correlates of recognition memory processes.

Recognition memory is critically dependent on a hierarchically organized network of brain areas including the visual ventral stream, medial temporal lobe structures, frontal and parietal cortices. In recent years, cognitive theories of recognition memory have been helpful to further our understanding of the functional organization of this network. A prominent, although not unchallenged, set of theories proposes that recognition memory is not a unitary phenomenon, but can be based on the recollection of contextual information about events or on familiarity in the absence of recollection. A number of hemodynamic and electromagnetic studies have been undertaken to relate recollection and familiarity to neuronal substrates both in healthy subjects as well as in patients with brain lesions. Today, it is evident that both event-related potential and event-related field (ERP/ERF) data as well as data of oscillatory brain activity (e.g., theta oscillations) are necessary to fully understand the neural dynamics of recollection and familiarity and their relationship to functional anatomy. Ultimately, such data are required from patients with isolated brain injuries to designated components of the networks (such as the hippocampus) to obtain converging evidence for functional relationships between recollection and familiarity and respective neuroanatomic substrates. The complexity of this task is highlighted by findings indicating that recognition memory can already be affected by preparatory processes prior to stimulus onset.     

Familiarity in source memory

Familiarity and recollection are thought to be separate processes underlying recognition memory. Event-related potentials (ERPs) dissociate these processes, with an early (approximately 300-500ms) frontal effect relating to familiarity (the FN400) and a later (500-800ms) parietal old/new effect relating to recollection. It has been debated whether source information for a studied item (i.e., contextual associations from when the item was previously encountered) is only accessible through recollection, or whether familiarity can contribute to successful source recognition. It has been shown that familiarity can assist in perceptual source monitoring when the source attribute is an intrinsic property of the item (e.g., an object's surface color), but few studies have examined its contribution to recognizing extrinsic source associations. Extrinsic source associations were examined in three experiments involving memory judgments for pictures of common objects. In Experiment 1, source information was spatial and results suggested that familiarity contributed to accurate source recognition: the FN400 ERP component showed a source accuracy effect, and source accuracy was above chance for items judged to only feel familiar. Source information in Experiment 2 was an extrinsic color association; source accuracy was at chance for familiar items and the FN400 did not differ between correct and incorrect source judgments. Experiment 3 replicated the results using a within-subjects manipulation of spatial vs. color source. Overall, the results suggest that familiarity's contribution to extrinsic source monitoring depends on the type of source information being remembered.     

Transcranial magnetic stimulation can measure and modulate learning and memory

The potential uses for Transcranial Magnetic Stimulation (TMS) in the study of learning and memory range from a method to map the topography and intensity of motor output maps during visuomotor learning to inducing reversible lesions that allow for the precise temporal and spatial dissection of the brain processes underlying learning and remembering. Single-pulse TMS appears to be adequate to examine motor output maps but repetitive TMS (rTMS) appears necessary to affect most cognitive processes in measurable ways. The results we have reviewed in this article indicate that rTMS may have a potential clinical application in patients with epilepsy in whom it is important to identify the lateralization of verbal memory. Single-pulse TMS can help identify changes in motor output maps during training, that may indicate improved or diminished learning and memory processes following a stroke or other neurological insult. Other evidence indicates that rTMS may even have the capability of facilitating various aspects of memory performance. From a research perspective. rTMS has demonstrated site- and time-specific effects primarily in interfering with explicit retrieval of episodic information from long-term memory. rTMS may also be able to modulate retrieval from semantic memory as evidenced by response-time and accuracy changes after rTMS. All these findings suggest that the use of transcranial magnetic stimulation in the study of learning and memory will increase in the future and that it is already a valuable tool in the cognitive neuroscientists' belt.     

Accelerated Long-Term Forgetting Limited to the Recollection Component of Recognition Memory in a Temporal Lobe Epileptic Patient

Accelerated long-term forgetting (ALF) is a frequent finding in patients with temporal lobe epilepsy (TLE). Here we report the case of a TLE patient who complained of marked difficulties in remembering personal events and information even though repeated neuropsychological assessments had failed to detect any deficit on common laboratory memory tests. The patient underwent an experimental investigation that involved estimating recollection and familiarity processes in the performance on verbal and visual recognition tests, over intervals ranging from 10 minutes to 7 days. Results showed accelerated forgetting confined to the recollection component only, which was particularly evident in the verbal test.     

On familiarity and recall of events by rats

Memory for a previously experienced event such as seeing a particular object can involve either a sense of familiarity for the object or of recall for seeing the object on a particular occasion. In humans, it has been claimed that recall and familiarity can be selectively impaired as they are based on dissociable neural systems. However, most tasks used to test memory in nonhuman animals use recognition memory tasks, in which successful performance can be based entirely on familiarity cues. Without the means to selectively investigate recall and familiarity in nonhuman animals, it has until recently proved difficult to dissociate the neural basis of these processes, and their very existence as separable entities has been questioned. Here we discuss a number of studies from our laboratory in which we have developed tasks that require recall and contrast these with recognition memory tasks that can be performed using familiarity alone. We use these tasks to begin to unravel familiarity and recall in the rat and the underlying neural bases of these processes.     

Dissociative contributions of medial temporal and frontal regions to prospective remembering

Prospective memory is memory of future intentions or plans in everyday life. Although some previous neuropsychological studies have stated that the prefrontal cortex and the medial temporal lobe are essential for successful prospective remembering, how the two regions contribute to prospective remembering remains unclear. We therefore used prospective memory training in the present study to investigate the neural mechanism of two components of prospective remembering: remembering to remember and remembering content. Two brain-damaged patients participated in this study: patient Y.O., who had lesions in the medial temporal lobe bilaterally, and patient T.K., who had a lesion in the basal forebrain and right medial frontal lobe. Both participants exhibited a severe anterograde amnesic syndrome and had normal IQ scores. Before the prospective memory training the participants underwent several index memory tests to examine their general memory and prospective memory performance. The training consisted of requesting the participants to perform an original mini-day task, in which they were first asked to memorize five simple daily actions with their times for execution, and then to recall the content of the actions when shown a drawing of a clock showing the proper time for execution. A training session was carried out once a week for 3 months. After completing training, the participants were again requested to take the same index memory tests. The results of the training task showed that Y.O.'s memory performance had gradually improved across all sessions of training, but T.K.'s improvement was not as marked. A more detailed analysis revealed that Y.O.'s memory performance was better for recalling time than for recalling content, whereas T.K.'s memory performance was better for recalling content than for recalling time. Furthermore, the results of the final index memory tests showed that the only improvement in Y.O.'s prospective memory was in remembering to remember, and that the only improvement in T.K.'s prospective memory was in remembering content. These results provide strong evidence that these two remembering components of prospective memory have independent neural bases, with the basal forebrain and right medial frontal lobe being required for remembering to remember, and the medial temporal lobe being required for remembering content. The results also suggest that memory training is an effective, means of improving everyday memory.     

The role of recollection and familiarity in the functional differentiation of the medial temporal lobes

The components of the medial temporal lobes (MTL) receive different kinds of input. The perirhinal cortex receives primarily object/item information, the parahippocampal cortex receives contextual information, and the hippocampus receives high-level inputs that include object/item, context, and other information. Critically, the perirhinal and parahippocampal cortices have similar cytoarchitectonics, which differ considerably from that of the hippocampus and suggest that these cortices process their inputs differently from the way that the hippocampus processes its inputs. Much evidence indicates that the hippocampus is designed to rapidly bind together pattern-separated representations that support recall/recollection well. In contrast, the newer MTL cortices rapidly create poorly pattern-separated memories that support familiarity well, but recall/recollection very poorly. For over a decade, there has been disagreement about whether recall/recollection is primarily mediated by the hippocampus and familiarity by the evolutionarily newer MTL cortices or whether the MTL mediates these kinds of memory in an integrated, homogeneous fashion. Common misconceptions about familiarity, recollection, item, and associative memory are discussed as are methodological problems with MTL lesion and functional imaging research. The possible confound of familiarity with weaker memory and recollection with stronger memory is discussed and the implications of the Montaldi et al. (2006) functional Magnetic Resonance Imaging (fMRI) study, which matched memory strength between strong familiarity and recollection, finding that only recollection activated the hippocampus, are discussed. A suggestion is made about how the long-running conflict of findings in the human hippocampal lesion literature may be resolved.     

Findings from animals concerning when interactions between perirhinal cortex, hippocampus and medial prefrontal cortex are necessary for recognition memory

Loss of recognition memory is a prominent feature of the human classical amnesic syndrome. Recognition memory requires judgments concerning prior occurrence. Such judgments can be made in a variety of ways using different types of information such as the relative familiarity of individual objects or locations, or the location of a previously encountered object, or when an object was previously encountered. We review findings of selective ablation studies which demonstrate that the perirhinal cortex, hippocampus and medial prefrontal cortex are differently involved in recognition memory processes involving these different types of information. This review also presents data from a series of disconnection analyses, which test whether the perirhinal cortex, hippocampus and medial prefrontal cortex form components of an integrated system for these recognition memory processes. These analyses reveal that it is necessary for the perirhinal cortex, medial prefrontal cortex and the hippocampus to interact, forming an integrated network, in recognition memory involving judgment of whether an object has been previously encountered in a particular place (object-in-place recognition memory) and in judging which of two objects was encountered longer ago (temporal order memory). In contrast, such interactions are not necessary when judgments are made concerning the prior occurrence of an individual item without positional information being necessary for the judgment (object memory) or concerning the prior occurrence of some item at a particular location without object information being necessary for the judgment (location memory).     

Perceptual fluency, semantic familiarity and recognition-related familiarity: an electrophysiological exploration

Scalp recorded event-related potentials (ERPs) were used to examine the neuronal activity associated with perceptual fluency, semantic familiarity and recognition-related familiarity. We assume that ERP differences between first and second presentations of non-famous faces in an implicit memory condition reflect perceptual fluency, ERP differences between first presentations of famous and non-famous faces reflect semantic familiarity (i.e., familiarity arising from semantic memory retrieval), and early ERP differences between first and second presentations of non-famous and famous faces in an explicit recognition memory task reflect recognition-related familiarity. Semantic familiarity elicited a broadly distributed effect between 200 and 300 ms after stimulus onset, possibly representing the activation of face recognition units. Between 300 and 450 ms, frontal effects were observed for semantic familiarity and recognition-related familiarity, while perceptual fluency was associated with a centro-parietally focused effect. Thus, familiarity arising from the retrieval of semantic information and recognition-related familiarity depend at least partly on the same neuronal circuits, while these are dissociable from those mediating perceptual fluency.     

Towards a functional organization of episodic memory in the medial temporal lobe

Here we describe a model of medial temporal lobe organization in which parallel "what" and "where" processing streams converge within the hippocampus to represent events in the spatio-temporal context in which they occurred; this circuitry also mediates the retrieval of context from event cues and vice versa, which are prototypes of episodic recall. Evidence from studies in animals are reviewed in support of this model, including experiments that distinguish characteristics of episodic recollection from familiarity, neuropsychological and recording studies that have identified a key role for the hippocampus in recollection and in associating events with the context in which they occurred, and distinct roles for parahippocampal region areas in separate "what" and "where" information processing that contributes to recollective and episodic memory.