Jessica Robin

Functional connectivity of hippocampal and prefrontal networks during episodic and spatial memory based on real‐world environments

Several recent studies have compared episodic and spatial memory in neuroimaging paradigms in order to understand better the contribution of the hippocampus to each of these tasks. In the present study, we build on previous findings showing common neural activation in default network areas during episodic and spatial memory tasks based on familiar, real‐world environments (Hirshhorn et al. (2012) Neuropsychologia 50:3094–3106). Following previous demonstrations of the presence of functionally connected sub‐networks within the default network, we performed seed‐based functional connectivity analyses to determine how, depending on the task, the hippocampus and prefrontal cortex differentially couple with one another and with distinct whole‐brain networks. We found evidence for a medial prefrontal‐parietal network and a medial temporal lobe network, which were functionally connected to the prefrontal and hippocampal seeds, respectively, regardless of the nature of the memory task. However, these two networks were functionally connected with one another during the episodic memory task, but not during spatial memory tasks. Replicating previous reports of fractionation of the default network into stable sub‐networks, this study also shows how these sub‐networks may flexibly couple and uncouple with one another based on task demands. These findings support the hypothesis that episodic memory and spatial memory share a common medial temporal lobe‐based neural substrate, with episodic memory recruiting additional prefrontal sub‐networks.

The spatial scaffold: The effects of spatial context on memory for events.

Events always unfold in a spatial context, leading to the claim that it serves as a scaffold for encoding and retrieving episodic memories. The ubiquitous co-occurrence of spatial context with events may induce participants to generate a spatial context when hearing scenarios of events in which it is absent. Spatial context should also serve as an excellent cue for memory retrieval. To test these predictions, participants read event scenarios involving a highly familiar or less familiar spatial context, or person, which they were asked to imagine and remember. At recall, locations were more effective memory cues than people, and both were better when they were highly familiar. Most importantly, when no locations were specified at study, participants exhibited a spontaneous tendency to generate a spatial context for the scenarios, while rarely generating a person. Events with spatial context were remembered more vividly and described in more detail than those without. Together, the results favor the view that spatial context plays a leading role in remembering events.

The Effects of Spatial Contextual Familiarity on Remembered Scenes, Episodic Memories, and Imagined Future Events

Several recent studies have explored the effect of contextual familiarity on remembered and imagined events. The aim of this study was to examine the extent of this effect by comparing the effect of cuing spatial memories, episodic memories, and imagined future events with spatial contextual cues of varying levels of familiarity. We used real-world landmark cues that had all been previously visited by the participants, and we measured the retrieval time, detail-richness, and vividness of remembered scenes, events, and imagined future events based on these cues. Participants consistently rated scenes and events based on more familiar cues as more detailed and more vivid, and they took less time to retrieve them. When the types of details were examined, it was revealed that the effects of increased contextual familiarity carry over to non-spatial details in the case of remembered events but possibly not in imagined events. This study provides evidence regarding how episodic memory and imagination are reliant on spatial context and possibly the process of scene construction.

Details, gist and schema: hippocampal–neocortical interactions underlying recent and remote episodic and spatial memory

Memories are complex and dynamic, continuously transforming with time and experience. In this paper, we review evidence of the neural basis of memory transformation for events and environments with emphasis on the role of hippocampal–neocortical interactions. We argue that memory transformation from detail-rich representations to gist-like and schematic representation is accompanied by corresponding changes in their neural representations. These changes can be captured by a model based on functional differentiation along the long-axis of the hippocampus, and its functional connectivity to related posterior and anterior neocortical structures, especially the ventromedial prefrontal cortex (vmPFC). In particular, we propose that perceptually detailed, highly specific representations are mediated by the posterior hippocampus and neocortex, gist-like representations by the anterior hippocampus, and schematic representations by vmPFC. These representations can co-exist and the degree to which each is utilized is determined by its availability and by task demands.

Familiar Real-World Spatial Cues Provide Memory Benefits in Older and Younger Adults.

Episodic memory, future thinking, and memory for scenes have all been proposed to rely on the hippocampus, and evidence suggests that these all decline in healthy aging. Despite this age-related memory decline, studies examining the effects of context reinstatement on episodic memory have demonstrated that reinstating elements of the encoding context of an event leads to better memory retrieval in both younger and older adults. The current study was designed to test whether more familiar, real-world contexts, such as locations that participants visited often, would improve the detail richness and vividness of memory for scenes, autobiographical events, and imagination of future events in young and older adults. The predicted age-related decline in internal details across all 3 conditions was accompanied by persistent effects of contextual familiarity, in which a more familiar spatial context led to increased detail and vividness of remembered scenes, autobiographical events, and, to some extent, imagined future events. This study demonstrates that autobiographical memory, imagination of the future, and scene memory are similarly affected by aging, and all benefit from being associated with more familiar (real-world) contexts, illustrating the stability of contextual reinstatement effects on memory throughout the life span.

More than accuracy: nonverbal dialects modulate the time course of vocal emotion recognition across cultures

Using a gating paradigm, this study investigated the nature of the in-group advantage in vocal emotion recognition by comparing 2 distinct cultures. Pseudoutterances conveying 4 basic emotions, expressed in English and Hindi, were presented to English and Hindi listeners. In addition to hearing full utterances, each stimulus was gated from its onset to construct 5 processing intervals to pinpoint when the in-group advantage emerges, and whether this differs when listening to a foreign language (English participants judging Hindi) or a second language (Hindi participants judging English). An index of the mean emotion identification point for each group and unbiased measures of accuracy at each time point was calculated. Results showed that in each language condition, native listeners were faster and more accurate than non-native listeners to recognize emotions. The in-group advantage emerged in both conditions after processing 400 ms to 500 ms of acoustic information. In the bilingual Hindi group, greater oral proficiency in English predicted faster and more accurate recognition of English emotional expressions. Consistent with dialect theory, our findings provide new evidence that nonverbal dialects impede both the accuracy and the efficiency of vocal emotion processing in cross-cultural settings, even when individuals are highly proficient in the out-group target language.

Long-term consolidation switches goal proximity coding from hippocampus to retrosplenial cortex

Recent research indicates the hippocampus may code the distance to the goal during navigation of newly learned environments. It is unclear however, whether this also pertains to highly familiar environments where extensive systems-level consolidation is thought to have transformed mnemonic representations. Here we recorded fMRI while University College London and Imperial College London students navigated virtual simulations of their own familiar campus (> 2 years of exposure) and the other campus learned days before scanning. Posterior hippocampal activity tracked the proximity to the goal in the newly learned campus, but not in the familiar campus. By contrast retrosplenial cortex tracked the distance to the goal in the familiar campus, but not in the recently learned campus. These responses were abolished when participants were guided to their goal by external cues. These results open new avenues of research on navigation and consolidation of spatial information and help advance models of how neural circuits support navigation in novel and highly familiar environments. Significance Statement Historically, research on the hippocampal formation has focused on its role in long-term memory and navigation – often in isolation. No study to date has directly compared realistic navigation within familiar with recently learned environments, nor has it been explored how the neural substrates, along with computational codes, may change. In this study, we show for the first time, a shift from hippocampal to cortical coding of distance to a goal during active navigation. This study bridges the gap between memory consolidation and navigation, and paves the way for more functional and realistic understanding of the hippocampus.

Selective scene perception deficits in a case of topographical disorientation

Topographical disorientation (TD) is a neuropsychological condition characterized by an inability to find ones way, even in familiar environments. One common contributing cause of TD is landmark agnosia, a visual recognition impairment specific to scenes and landmarks. Although many cases of TD with landmark agnosia have been documented, little is known about the perceptual mechanisms which lead to selective deficits in recognizing scenes. In the present study, we test LH, a man who exhibits TD and landmark agnosia, on measures of scene perception that require selectively attending to either the configural or surface properties of a scene. Compared to healthy controls, LH demonstrates perceptual impairments when attending to the configuration of a scene, but not when attending to its surface properties, such as the pattern of the walls or whether the ground is sand or grass. In contrast, when focusing on objects instead of scenes, LH demonstrates intact perception of both geometric and surface properties. This study demonstrates that in a case of TD and landmark agnosia, the perceptual impairments are selective to the layout of scenes, providing insight into the mechanism of landmark agnosia and scene-selective perceptual processes.

The Primacy of Spatial Context in the Neural Representation of Events

Some theories of episodic memory hypothesize that spatial context plays a fundamental role in episodic memory, acting as a scaffold on which episodes are constructed. A prediction based on this hypothesis is that spatial context should play a primary role in the neural representation of an event. To test this hypothesis in humans, male and female participants imagined events, composed of familiar locations, people, and objects, during an fMRI scan. We used multivoxel pattern analysis to determine the neural areas in which events could be discriminated based on each feature. We found that events could be discriminated according to their location in areas throughout the autobiographical memory network, including the parahippocampal cortex and posterior hippocampus, retrosplenial cortex, posterior cingulate cortex, precuneus, and medial prefrontal cortex. Events were also discriminable based on person and object features, but in fewer regions. Comparing classifier performance in regions involved in memory for scenes and events demonstrated that the location of an event was more accurately classified than the person or object involved. These results support theories that suggest that spatial context is a prominent defining feature of episodic memory. SIGNIFICANCE STATEMENT Remembered and imagined events are complex, consisting of many elements, including people, objects, and locations. In this study, we sought to determine how these types of elements differentially contribute to how the brain represents an event. Participants imagined events consisting of familiar locations, people, and objects (e.g., kitchen, mom, umbrella) while their brain activity was recorded with fMRI. We found that the neural patterns of activity in brain regions associated with spatial and episodic memory could distinguish events based on their location, and to some extent, based on the people and objects involved. These results suggest that the spatial context of an event plays an important role in how an event is represented in the brain.

Differential spatiotemporal representations along the hippocampal long axis in humans

Increased place field size and signal autocorrelation along the dorsoventral hippocampal axis in rodents are considered a fundamental aspect of hippocampal organization, yet such evidence is lacking in humans. Using fMRI, we report corresponding evidence of increasing neural similarity from posterior to anterior hippocampus (dorsoventral homologues) in humans. These findings help account for observed shifting in representational granularity, from global context (anterior) to local details (posterior), along the hippocampal axis.