Melissa C. Duff

The hippocampus and the flexible use and processing of language

Fundamental to all human languages is an unlimited expressive capacity and creative flexibility that allow speakers to rapidly generate novel and complex utterances. In turn, listeners interpret language “on-line,” incrementally integrating multiple sources of information as words unfold over time. A challenge for theories of language processing has been to understand how speakers and listeners generate, gather, integrate, and maintain representations in service of language processing. We propose that many of the processes by which we use language place high demands on and receive contributions from the hippocampal declarative memory system. The hippocampal declarative memory system is long known to support relational binding and representational flexibility. Recent findings demonstrate that these same functions are engaged during the real-time processes that support behavior in-the-moment. Such findings point to the hippocampus as a potentially key contributor to cognitive functions that require on-line integration of multiple sources of information, such as on-line language processing. Evidence supporting this view comes from findings that individuals with hippocampal amnesia show deficits in the use of language flexibly and on-line. We conclude that the relational binding and representational flexibility afforded by the hippocampal declarative memory system positions the hippocampus as a key contributor to language use and processing.

Declarative memory is critical for sustained advantageous complex decision-making

Previous studies have reported conflicting evidence concerning the contribution of declarative memory to advantageous decision-making on the Iowa Gambling Task (IGT). One study, in which the measurement of psychophysiology during the task necessitated a 10-s delay between card selections, found that six participants with amnesia due to hippocampal damage failed to develop a preference for advantageous decks over disadvantageous decks [Gutbrod, K., Krouzel, C., Hofer, H., Muri, R., Perrig, W., & Ptak, R. (2006). Decision-making in amnesia: Do advantageous decisions require conscious knowledge of previous behavioural choices? Neuropsychologia, 44(8), 1315-1324]. However, a single-case study (where psychophysiology was not measured and no delay between card selections occurred) showed that an amnesic patient developed normal preference for advantageous decks [Turnbull, O. H., & Evans, C. E. (2006). Preserved complex emotion-based learning in amnesia. Neuropsychologia, 44(2), 300-306]. We sought to resolve these discrepant findings by examining IGT performances in five patients with profound amnesia (WMS-III General Memory Index M=63) and bilateral hippocampal damage caused by anoxia (n=4) or herpes simplex encephalitis (n=1). In one administration of the IGT, psychophysiology measurements were utilized and a 6-s delay was interposed between card selections. In a second administration, no delay between card selections was interposed. While age-, sex-, and education-matched healthy comparison participants showed significant learning with a gradual preference for advantageous decks in both conditions, amnesic patients, irrespective of IGT administration condition and extent of medial temporal lobe damage, failed to develop this preference. These findings strongly discount the possibility that the delay between card selections explains why amnesic participants fail to learn in the IGT, and suggest instead a significant role for medial temporal lobe declarative memory systems in the type of complex decision-making tapped by the IGT.

The role of the hippocampus in flexible cognition and social behavior

Successful behavior requires actively acquiring and representing information about the environment and people, and manipulating and using those acquired representations flexibly to optimally act in and on the world. The frontal lobes have figured prominently in most accounts of flexible or goal-directed behavior, as evidenced by often-reported behavioral inflexibility in individuals with frontal lobe dysfunction. Here, we propose that the hippocampus also plays a critical role by forming and reconstructing relational memory representations that underlie flexible cognition and social behavior. There is mounting evidence that damage to the hippocampus can produce inflexible and maladaptive behavior when such behavior places high demands on the generation, recombination, and flexible use of information. This is seen in abilities as diverse as memory, navigation, exploration, imagination, creativity, decision-making, character judgments, establishing and maintaining social bonds, empathy, social discourse, and language use. Thus, the hippocampus, together with its extensive interconnections with other neural systems, supports the flexible use of information in general. Further, we suggest that this understanding has important clinical implications. Hippocampal abnormalities can produce profound deficits in real-world situations, which typically place high demands on the flexible use of information, but are not always obvious on diagnostic tools tuned to frontal lobe function. This review documents the role of the hippocampus in supporting flexible representations and aims to expand our understanding of the dynamic networks that operate as we move through and create meaning of our world.

Medial pfc damage abolishes the self-reference effect

Functional neuroimaging studies suggest that the medial PFC (mPFC) is a key component of a large-scale neural system supporting a variety of self-related processes. However, it remains unknown whether the mPFC is critical for such processes. In this study, we used a human lesion approach to examine this question. We administered a standard trait judgment paradigm [Kelley, W. M., Macrae, C. N., Wyland, C. L., Caglar, S., Inati, S., & Heatherton, T. F. Finding the self? An event-related fMRI study. Journal of Cognitive Neuroscience, 14, 785–794, 2002] to patients with focal brain damage to the mPFC. The self-reference effect (SRE), a memory advantage conferred by self-related processing, served as a measure of intact self-processing ability. We found that damage to the mPFC abolished the SRE. The results demonstrate that the mPFC is necessary for the SRE and suggest that this structure is important for self-referential processing and the neural representation of self.

Hippocampal amnesia disrupts creative thinking

Creativity requires the rapid combination and recombination of existing mental representations to create novel ideas and ways of thinking. The hippocampal system, through its interaction with neocortical storage sites, provides a relational database necessary for the creation, updating, maintenance, and juxtaposition of mental representations used in service of declarative memory. Given this functionality, we hypothesized that hippocampus would play a critical role in creative thinking. We examined creative thinking, as measured by verbal and figural forms of the torrance tests of creative thinking (TTCT), in a group of participants with hippocampal damage and severe declarative memory impairment as well as in a group of demographically matched healthy comparison participants. The patients with bilateral hippocampal damage performed significantly worse than comparison participants on both the verbal and figural portions of the TTCT. These findings suggest that hippocampus plays a role critical in creative thinking, adding to a growing body of work pointing to the diverse ways the hallmark processing features of hippocampus serve a variety of behaviors that require flexible cognition.

Sustained experience of emotion after loss of memory in patients with amnesia

Can the experience of an emotion persist once the memory for what induced the emotion has been forgotten? We capitalized on a rare opportunity to study this question directly using a select group of patients with severe amnesia following circumscribed bilateral damage to the hippocampus. The amnesic patients underwent a sadness induction procedure (using affectively-laden film clips) to ascertain whether their experience of sadness would persist beyond their memory for the sadness-inducing films. The experiment showed that the patients continued to experience elevated levels of sadness well beyond the point in time at which they had lost factual memory for the film clips. A second experiment using a happiness induction procedure yielded similar results, suggesting that both positive and negative emotional experiences can persist independent of explicit memory for the inducing event. These findings provide direct evidence that a feeling of emotion can endure beyond the conscious recollection for the events that initially triggered the emotion.

Differential contributions of hippocampus and medial prefrontal cortex to self-projection and self-referential processing

Converging evidence points to a neural network that supports a range of abilities including remembering the past, thinking about the future, and introspecting about oneself and others. Neuroimaging studies find hippocampal activation during event construction tasks, and patients with hippocampal amnesia are impaired in their ability to (re)construct events of the past and the future. Neuroimaging studies of constructed experiences similarly implicate the medial prefrontal cortex (mPFC), but it remains unknown whether the mPFC is critical for such processes. The current study compares performance of five patients with bilateral mPFC damage, six patients with bilateral hippocampal damage, and demographically matched comparison participants on an event construction task. Participants were given a neutral cue word and asked to (re)construct events across four time conditions: real past, imagined past, imagined present, and future. These event narratives were analyzed for the number of internal and external details to quantify the extent of episodic (re)experiencing. Given the literature on the involvement of the mPFC in self-referential processing, we also analyzed the event narratives for self-references. The patients with mPFC damage did not differ from healthy comparison participants in their ability to construct highly detailed episodic events across time periods but displayed disruptions in their incorporation of the self. Patients with hippocampal damage showed the opposite pattern; they were impaired in their ability to construct highly detailed episodic events across time periods but not in their incorporation of the self. The results suggest differential contributions of hippocampus and medial prefrontal cortex to the distributed neural network for various forms of self-projection.

Hiding in plain view: Lesions of the medial temporal lobe impair online representation

The hippocampus is necessary for the normal formation of enduring declarative memories, but its role in cognitive processes spanning short intervals is less well understood. Within the last decade, several reports have described modest behavioral deficits in medial temporal lobe (MTL)‐lesion patients when they perform tasks that do not seem likely to rely on enduring memory. An intriguing but sparsely‐tested implication of such results is that the MTL is involved in the online representation of information, possibly of an associative/relational nature, irrespective of delay. We administered several tests that simultaneously presented all information necessary for accurate responses to a group of MTL‐lesion patients with severe declarative memory deficits but otherwise normal cognition, and to matched brain‐damaged and healthy comparison participants. MTL‐lesion patients performed less well than either comparison group in the Hooper Visual Organization Test, and several patients performed outside the normal range on the Overlapping Figures Test. A novel follow‐up borrowing characteristics of the Overlapping Figures Test revealed impaired identification of novel items by MTL‐lesion patients when target items were obscured by distracters, and two additional novel tests of fragmented object identification further implicated the hippocampus/MTL in the integration of information across very brief intervals. These findings suggest that MTL structures including the hippocampus contribute similarly to cognition irrespective of timescale.

Hippocampal amnesia disrupts verbal play and the creative use of language in social interaction

Background: While the neural substrates and cognitive components of creativity have received considerable attention in cognitive neuroscience, the creative use of language in social interaction has been less well studied. As part of a broader programme of research on language‐and‐memory‐in‐use in individuals with hippocampal amnesia, we analysed verbal play, a creative use of language that is pervasive in everyday communicative interaction. Aims: To identify instances of creative uses of language in the protocols of social and collaborative interactions, to characterise the qualitative nature, and to determine the frequency of these interactions initiated by participants with hippocampal amnesia vs comparison participants in order to ascertain whether amnesia impairs this aspect of social communication. Methods & Procedures: This study uses quantitative group comparisons and detailed discourse analysis to analyse verbal play in the interactional discourse sessions of four participants with hippocampal amnesia and four healthy (demographically matched) comparison participants, each interacting with a familiar partner while completing a collaborative referencing task and with a researcher between task trials. Outcomes & Results: All participants used verbal play. However, significantly fewer episodes were initiated in sessions with amnesia participants (312) and by participants with amnesia themselves (187) than in sessions with comparison participants (572) and by comparison participants (395). No significant group differences were observed for interactional forms, resources, or functions. Qualitative differences were also observed in amnesia sessions (e.g., more rotely produced episodes, lack of thematically linked episodes). Conclusions: These findings suggest that hippocampal amnesia disrupts the creative use of language in social interaction and accord with our previous work pointing to impairments in language‐and‐memory‐in‐use more broadly. These findings highlight the interdependence of language and memory especially in the interactional aspects of communication.

Mild traumatic brain injury (MTBI): assessment and treatment procedures used by speech-language pathologists (SLPs)

The purposes of this study were to identify how individuals with MTBI are assessed, to determine the referral process to and from speech-language pathologists (SLPs), to describe the frequency, structure, and nature of treatment, to identify how individuals with MTBI and their families are educated about the injury and counselled, and to assess current follow-up procedures. One-hundred and forty-three hospital and rehabilitation centre based SLPs from North Carolina and Illinois responded to a survey developed to address these areas of interest. Findings indicated current diagnostic tools used by SLPs lack the sensitivity to detect the subtle cognitive communication deficits associated with MTBI, referral and follow-up procedures are not sufficiently implemented in facilities to meet the growing needs of individuals with MTBI, and SLPs would benefit from increased training regarding the management of individuals with MTBI including educating and counselling patients and their families.