Memory
memory representation
Flexible codes and loci of visual working memory
Neural correlates of visual working memory have been found in early visual, parietal, and prefrontal regions. These findings have spurred fruitful debate over how and where in the brain memories might be represented. Here, I will present data from multiple experiments to demonstrate how a focus on behavioral requirements can unveil a more comprehensive understanding of the visual working memory system. Specifically, items in working memory must be maintained in a highly robust manner, resilient to interference. At the same time, storage mechanisms must preserve a high degree of flexibility in case of changing behavioral goals. Several examples will be explored in which visual memory representations are shown to undergo transformations, and even shift their cortical locus alongside their coding format based on specifics of the task.
Drifting assemblies for persistent memory: Neuron transitions and unsupervised compensation
Change is ubiquitous in living beings. In particular, the connectome and neural representations can change. Nevertheless behaviors and memories often persist over long times. In a standard model, associative memories are represented by assemblies of strongly interconnected neurons. For faithful storage these assemblies are assumed to consist of the same neurons over time. We propose a contrasting memory model with complete temporal remodeling of assemblies, based on experimentally observed changes of synapses and neural representations. The assemblies drift freely as noisy autonomous network activity or spontaneous synaptic turnover induce neuron exchange. The exchange can be described analytically by reduced, random walk models derived from spiking neural network dynamics or from first principles. The gradual exchange allows activity-dependent and homeostatic plasticity to conserve the representational structure and keep inputs, outputs and assemblies consistent. This leads to persistent memory. Our findings explain recent experimental results on temporal evolution of fear memory representations and suggest that memory systems need to be understood in their completeness as individual parts may constantly change.
Extrinsic control and autonomous computation in the hippocampal CA1 circuit
In understanding circuit operations, a key issue is the extent to which neuronal spiking reflects local computation or responses to upstream inputs. Because pyramidal cells in CA1 do not have local recurrent projections, it is currently assumed that firing in CA1 is inherited from its inputs – thus, entorhinal inputs provide communication with the rest of the neocortex and the outside world, whereas CA3 inputs provide internal and past memory representations. Several studies have attempted to prove this hypothesis, by lesioning or silencing either area CA3 or the entorhinal cortex and examining the effect of firing on CA1 pyramidal cells. Despite the intense and careful work in this research area, the magnitudes and types of the reported physiological impairments vary widely across experiments. At least part of the existing variability and conflicts is due to the different behavioral paradigms, designs and evaluation methods used by different investigators. Simultaneous manipulations in the same animal or even separate manipulations of the different inputs to the hippocampal circuits in the same experiment are rare. To address these issues, I used optogenetic silencing of unilateral and bilateral mEC, of the local CA1 region, and performed bilateral pharmacogenetic silencing of the entire CA3 region. I combined this with high spatial resolution recording of local field potentials (LFP) in the CA1-dentate axis and simultaneously collected firing pattern data from thousands of single neurons. Each experimental animal had up to two of these manipulations being performed simultaneously. Silencing the medial entorhinal (mEC) largely abolished extracellular theta and gamma currents in CA1, without affecting firing rates. In contrast, CA3 and local CA1 silencing strongly decreased firing of CA1 neurons without affecting theta currents. Each perturbation reconfigured the CA1 spatial map. Yet, the ability of the CA1 circuit to support place field activity persisted, maintaining the same fraction of spatially tuned place fields, and reliable assembly expression as in the intact mouse. Thus, the CA1 network can maintain autonomous computation to support coordinated place cell assemblies without reliance on its inputs, yet these inputs can effectively reconfigure and assist in maintaining stability of the CA1 map.
Distributed and stable memory representations may lead to serial dependence
Perception and action are biased by our recent experiences. Even when a sequence of stimuli are randomly presented, responses are sometimes attracted toward the past. The mechanism of such bias, recently termed serial dependence, is still under investigation. Currently, there is mixed evidence indicating that such bias could be either from a sensory and perceptual origin or occurring only at decisional stages. In this talk, I will present recent findings from our group showing that biases are decreased when disrupting the memory trace in a premotor region in a simple visuomotor task. In addition, we have shown that this bias is stable over periods of up to 8 s. At the end, I will show ongoing analysis of a recent experiment and argue that serial dependence may rely on distributed memory representations of stimuli and task relevant features.
Flexible codes and loci of visual working memory
Neural correlates of visual working memory have been found in early visual, parietal, and prefrontal regions. These findings have spurred fruitful debate over how and where in the brain memories might be represented. Here, I will present data from multiple experiments to demonstrate how a focus on behavioral requirements can unveil a more comprehensive understanding of the visual working memory system. Specifically, items in working memory must be maintained in a highly robust manner, resilient to interference. At the same time, storage mechanisms must preserve a high degree of flexibility in case of changing behavioral goals. Several examples will be explored in which visual memory representations are shown to undergo transformations, and even shift their cortical locus alongside their coding format based on specifics of the task.
Visual working memory representations are distorted by their use in perceptual comparisons
Visual working memory (VWM) allows us to maintain a small amount of task-relevant information in mind so that we can use them to guide our behavior. Although past studies have successfully characterized its capacity limit and representational quality during maintenance, the consequence of its usage for task-relevant behaviors has been largely unknown. In this talk, I will demonstrate that VWM representations get distorted when they are used for perceptual comparisons with new visual inputs, especially when the inputs are subjectively similar to the VWM representations. Furthermore, I will show that this similarity-induced memory bias (SIMB) occurs for both simple (e.g. , color, shape) and complex stimuli (e.g., real world objects, faces) that are perceptually encoded and retrieved from long-term memory. Given the observed versatility of the SIMB, its implication for other memory distortion phenomena (e.g., distractor-induced distortion, misinformation effect) will be discussed.
Imaging memory consolidation in wakefulness and sleep
New memories are initially labile and have to be consolidated into stable long-term representations. Current theories assume that this is supported by a shift in the neural substrate that supports the memory, away from rapidly plastic hippocampal networks towards more stable representations in the neocortex. Rehearsal, i.e. repeated activation of the neural circuits that store a memory, is thought to crucially contribute to the formation of neocortical long-term memory representations. This may either be achieved by repeated study during wakefulness or by a covert reactivation of memory traces during offline periods, such as quiet rest or sleep. My research investigates memory consolidation in the human brain with multivariate decoding of neural processing and non-invasive in-vivo imaging of microstructural plasticity. Using pattern classification on recordings of electrical brain activity, I show that we spontaneously reprocess memories during offline periods in both sleep and wakefulness, and that this reactivation benefits memory retention. In related work, we demonstrate that active rehearsal of learning material during wakefulness can facilitate rapid systems consolidation, leading to an immediate formation of lasting memory engrams in the neocortex. These representations satisfy general mnemonic criteria and cannot only be imaged with fMRI while memories are actively processed but can also be observed with diffusion-weighted imaging when the traces lie dormant. Importantly, sleep seems to hold a crucial role in stabilizing the changes in the contribution of memory systems initiated by rehearsal during wakefulness, indicating that online and offline reactivation might jointly contribute to forming long-term memories. Characterizing the covert processes that decide whether, and in which ways, our brains store new information is crucial to our understanding of memory formation. Directly imaging consolidation thus opens great opportunities for memory research.
Exploring Memories of Scenes
State-of-the-art machine vision models can predict human recognition memory for complex scenes with astonishing accuracy. In this talk I present work that investigated how memorable scenes are actually remembered and experienced by human observers. We found that memorable scenes were recognized largely based on recollection of specific episodic details but also based on familiarity for an entire scene. I thus highlight current limitations in machine vision models emulating human recognition memory, with promising opportunities for future research. Moreover, we were interested in what observers specifically remember about complex scenes. We thus considered the functional role of eye-movements as a window into the content of memories, particularly when observers recollected specific information about a scene. We found that when observers formed a memory representation that they later recollected (compared to scenes that only felt familiar), the overall extent of exploration was broader, with a specific subset of fixations clustered around later to-be-recollected scene content, irrespective of the memorability of a scene. I discuss the critical role that our viewing behavior plays in visual memory formation and retrieval and point to potential implications for machine vision models predicting the content of human memories.
The When, Where and What of visual memory formation
The eyes send a continuous stream of about two million nerve fibers to the brain, but only a fraction of this information is stored as visual memories. This talk will detail three neurocomputational models that attempt an understanding how the visual system makes on-the-fly decisions about how to encode that information. First, the STST family of models (Bowman & Wyble 2007; Wyble, Potter, Bowman & Nieuwenstein 2011) proposes mechanisms for temporal segmentation of continuous input. The conclusion of this work is that the visual system has mechanisms for rapidly creating brief episodes of attention that highlight important moments in time, and also separates each episode from temporally adjacent neighbors to benefit learning. Next, the RAGNAROC model (Wyble et al. 2019) describes a decision process for determining the spatial focus (or foci) of attention in a spatiotopic field and the neural mechanisms that provide enhancement of targets and suppression of highly distracting information. This work highlights the importance of integrating behavioral and electrophysiological data to provide empirical constraints on a neurally plausible model of spatial attention. The model also highlights how a neural circuit can make decisions in a continuous space, rather than among discrete alternatives. Finally, the binding pool (Swan & Wyble 2014; Hedayati, O’Donnell, Wyble in Prep) provides a mechanism for selectively encoding specific attributes (i.e. color, shape, category) of a visual object to be stored in a consolidated memory representation. The binding pool is akin to a holographic memory system that layers representations of select latent representations corresponding to different attributes of a given object. Moreover, it can bind features into distinct objects by linking them to token placeholders. Future work looks toward combining these models into a coherent framework for understanding the full measure of on-the-fly attentional mechanisms and how they improve learning.
Learning orthogonal working memory representations protects from interference in a dual task
COSYNE 2023
Volatile working memory representations crystallize with practice
COSYNE 2025
Drifting memories: Sleep stages play opposite roles in reshaping memory representations
FENS Forum 2024
Sensory cues bind memory representations facilitating consolidation
FENS Forum 2024