The interplay of hippocampus and ventromedial prefrontal cortex in memory-based decision making

Episodic memory and value-based decision making are two central and intensively studied research domains in cognitive neuroscience, but we are just beginning to understand how they interact to enable memory-based decisions. The two brain regions that have been associated with episodic memory and value-based decision making are the hippocampus and the ventromedial prefrontal cortex, respectively. In this review article, we first give an overview of these brain–behavior associations and then focus on the mechanisms of potential interactions between the hippocampus and ventromedial prefrontal cortex that have been proposed and tested in recent neuroimaging studies. Based on those possible interactions, we discuss several directions for future research on the neural and cognitive foundations of memory-based decision making

Content representation in the human medial temporal lobe

The transformation of sensory inputs into complex memory representations is fundamental to human experience; yet, little is known about how this crucial process is achieved. When you meet your friend at the new cafe in town, what part of the brain encodes this novel scene into long term memory? What part encoded your friend’s favorite t-shirt, so that the sight of it gives you a feeling of familiarity rather than surprise? It is well-established that the medial temporal lobe (MTL) is crucial to both processes, but the MTL is not a single homogeneous region. In fact, it is composed of several anatomically distinct subregions including hippocampus, perirhinal cortex (PRC) and parahippocampal cortex (PHC). However, the computations performed by each subregion to encode individual events is still unclear. The present research tests the central hypothesis that different forms of event content are transformed into memory by distinct subregions within the MTL. A critical barrier in the study of content representation thus far has been its focus on comparing univariate peak activations in a region to different stimulus materials. To go beyond this limited approach, we employed multivariate statistical analyses that takes into account how event content is represented by distributed activity in MTL subregions. First, we examine the content-specific contributions of MTL subregions to episodic encoding and retrieval. Then, we demonstrate how these distributed representations support memory-based prediction to resolve ambiguities in our environment.Neuroscienc

There is more to memory than recollection and familiarity.

Theoretical models of memory retrieval have focused on processes of recollection and familiarity. Research suggests that there are still other processes involved in memory reconstruction, leading to experiences of knowing and inferring the past. Understanding these experiences, and the cognitive processes that give rise to them, seems likely to further expand our understanding of the neural substrates of memory

Prediction and memory: A predictive coding account

The hippocampus is crucial for episodic memory, but it is also involved in online prediction. Evidence suggests that a unitary hippocampal code underlies both episodic memory and predictive processing, yet within a predictive coding framework the hippocampal-neocortical interactions that accompany these two phenomena are distinct and opposing. Namely, during episodic recall, the hippocampus is thought to exert an excitatory influence on the neocortex, to reinstate activity patterns across cortical circuits. This contrasts with empirical and theoretical work on predictive processing, where descending predictions suppress prediction errors to ‘explain away’ ascending inputs via cortical inhibition. In this hypothesis piece, we attempt to dissolve this previously overlooked dialectic. We consider how the hippocampus may facilitate both prediction and memory, respectively, by inhibiting neocortical prediction errors or increasing their gain. We propose that these distinct processing modes depend upon the neuromodulatory gain (or precision) ascribed to prediction error units. Within this framework, memory recall is cast as arising from fictive prediction errors that furnish training signals to optimise generative models of the world, in the absence of sensory data

When the brain, but not the person, remembers: Cortical reinstatement is modulated by retrieval goal in developmental amnesia

Developmental amnesia (DA) is associated with early hippocampal damage and subsequent episodic amnesia emerging in childhood alongside age-appropriate development of semantic knowledge. We employed fMRI to assess whether patients with DA show evidence of 'cortical reinstatement', a neural correlate of episodic memory, despite their amnesia. At study, 23 participants (5 patients) were presented with words overlaid on a scene or a scrambled image for later recognition. Scene reinstatement was indexed by scene memory effects (greater activity for previously presented words paired with a scene rather than scrambled images) that overlapped with scene perception effects. Patients with DA demonstrated scene reinstatement effects in the parahippocampal and retrosplenial cortex that were equivalent to those shown by healthy controls. Behaviourally, however, patients with DA showed markedly impaired scene memory. The data indicate that reinstatement can occur despite hippocampal damage, but that cortical reinstatement is insufficient to support accurate memory performance. Furthermore, scene reinstatement effects were diminished during a retrieval task in which scene information was not relevant for accurate responding, indicating that strategic mnemonic processes operate normally in DA. The data suggest that cortical reinstatement of trial-specific contextual information is decoupled from the experience of recollection in the presence of severe hippocampal atrophy

Neural reactivation in parietal cortex enhances memory for episodically linked information.

Remembering is a complex process that involves recalling specific details, such as who you were with when you celebrated your last birthday, as well as contextual information, such as the place where you celebrated. It is well established that the act of remembering enhances long-term retention of the retrieved information, but the neural and cognitive mechanisms that drive memory enhancement are not yet understood. One possibility is that the process of remembering results in reactivation of the broader episodic context. Consistent with this idea, in two experiments, we found that multiple retrieval attempts enhanced long-term retention of both the retrieved object and the nontarget object that shared scene context, compared with a restudy control. Using representational similarity analysis of fMRI data in experiment 2, we found that retrieval resulted in greater neural reactivation of both the target objects and contextually linked objects compared with restudy. Furthermore, this reactivation occurred in a network of medial and lateral parietal lobe regions that have been linked to episodic recollection. The results demonstrate that retrieving a memory can enhance retention of information that is linked in the broader event context and the hippocampus and a posterior medial network of parietal cortical areas (also known as the Default Network) play complementary roles in supporting the reactivation of episodically linked information during retrieval

Content Tuning in the Medial Temporal Lobe Cortex: Voxels that Perceive, Retrieve.

How do we recall vivid details from our past based only on sparse cues? Research suggests that the phenomenological reinstatement of past experiences is accompanied by neural reinstatement of the original percept. This process critically depends on the medial temporal lobe (MTL). Within the MTL, perirhinal cortex (PRC) and parahippocampal cortex (PHC) are thought to support encoding and recall of objects and scenes, respectively, with the hippocampus (HC) serving as a content-independent hub. If the fidelity of recall indeed arises from neural reinstatement of perceptual activity, then successful recall should preferentially draw upon those neural populations within content-sensitive MTL cortex that are tuned to the same content during perception. We tested this hypothesis by having eighteen human participants undergo functional MRI (fMRI) while they encoded and recalled objects and scenes paired with words. Critically, recall was cued with the words only. While HC distinguished successful from unsuccessful recall of both objects and scenes, PRC and PHC were preferentially engaged during successful versus unsuccessful object and scene recall, respectively. Importantly, within PRC and PHC, this content-sensitive recall was predicted by content tuning during perception: Across PRC voxels, we observed a positive relationship between object tuning during perception and successful object recall, while across PHC voxels, we observed a positive relationship between scene tuning during perception and successful scene recall. Our results thus highlight content-based roles of MTL cortical regions for episodic memory and reveal a direct mapping between content-specific tuning during perception and successful recall

Cortical circuits underlying flexible learning

Animals survive and compete in their environment by making adaptive memories of the situations they have encountered. Flexible learning then allows to adjust to the great variety of possible environmental changes. This requires comparison of past and present values of rewards and costs associated with behaviour in order to make a decision whether the default course of behaviour needs to be adjusted to the new circumstances. This complex behaviour involves a variety of brain functions, such as detection of the salience of stimuli and its changes, memory of the history of reinforcement, and cognitive control of behaviour. These functions have most consistently been associated with the subdivisions of medium prefrontal cortex and limbic areas of the brain. Within this context, the anterior cingulate cortex (ACC), a prefrontal area, is of special interest due to its specific position within prefrontal and limbic brain systems. ACC has recently been a focus of extensive research in humans, primates and rodents. However, despite a wealth of descriptive data, and numerous theories about the role of ACC in sensory, motor and cognitive processes, it has not yet been possible to combine current views on the function of ACC in cognition into a coherent model. In my thesis, I explore the role of mouse ACC in flexible learning. I use chemogenetic silencing to locally interfere with the acquisition and consolidation of memory in order to investigate the role of ACC in Pavlovian and non-Pavlovian forms of learning. First, I address the role of ACC in attention set-shifting tasks, which represent a close analogue to the foraging paradigms that have mainly been explored in monkeys. Second, I compare the function of ACC in acquisition and consolidation of single-trial and multi-trial versions of contextual fear conditioning (cFC) learning. By utilising newly available genetic tools, which allow us to selectively silence the group of cells projecting to the area of interest and further manipulate it, I then proceed to a more in-depth study of ACC function within the wider brain network. To this end, I describe in detail the connectivity of ACC with other brain areas, and then address the role of those ACC-based networks in acquisition, consolidation and modification of learning. My results reveal how the function of ACC in supporting flexible learning is embedded dynamically within a specific network of systems, within which specific areas are associated with different forms of subsequent learning. This study provides a comprehensive view of how ACC and the structures monosynaptically connected to it are implicated in the formation of adjustable memories