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Symposium Session 4 - Hippocampus and sequential behaviors across different timescales and memory domains in humans

Chair: Genevieve Albouy¹; ¹University of Utah
Presenters: Eyiyemisi Damisah, Hannah Tarder-Stoll, Katja Kornysheva, Ainsley Temudo

The goal of this symposium is to examine the capacity of the hippocampus to represent the sequential order of learned information across different timescales and memory domains. First, Dr. Damisah will provide a fine-grained characterization of time representation in the hippocampus using intra-cranial EEG recorded in epileptic patients viewing sequences of visual scenes. She will show that the hippocampus extracts topological features of experiences to add temporal continuity to sensory memories. The presentation of Dr. Tarder-Stoll will then focus on memories for temporally extended sequences of environments in immersive virtual reality. Her fMRI data show that the hippocampus integrates representations of connected sequences and that these representations predict the ability to update predictions in sequential behavior. Next, the talk of Dr. Kornysheva will focus on hippocampal sequencing function in the motor memory domain. She will present fMRI data acquired during the execution of learned motor sequences and will show how hippocampal activity increases during movement planning and predicts the order of upcoming motor sequences. Last, Ainsley Temudo will present fMRI data showing that the hippocampus represents the temporal order of sequential information similarly in both the declarative and the motor memory domains. She proposes that the hippocampus provides a cognitive framework for sequential behaviors irrespective of their nature. This symposium is important as it provides experimental support for the hippocampal sequencing hypothesis (Buzsaki and Tingley, 2018) which proposes that the hippocampus is a general sequence generator that carries content-limited ordinal information and tiles the gap between events to be linked.

Presentations

Representation of visual sequences in the tuning and topology of neuronal activity in the human hippocampus

Eyiyemisi Damisah¹; ¹Yale University

The hippocampus plays a critical role in the representation of time, yet the underlying coding principles are poorly understood. We hypothesized that hippocampal neurons selective for specific visual stimuli adjust their tuning to encode sequence structure, smoothly combining sensory and temporal codes. In epilepsy patients who underwent clinical monitoring with intracranial EEG, we recorded neuronal activity from the hippocampus and control brain regions as they viewed looping sequences of visual scenes in structured (repeating) or random orders. The firing rates of hippocampal neurons to individual scenes were modulated by temporal distance from their preferred scene in structured sequences, increasing for nearby scenes and decreasing for distant scenes; this modulation was absent in random sequences and control regions. Analysis of population activity in local field potentials revealed that the looping sequence structure was embedded in a high-dimensional ring shape representing the serial order of the scenes. These findings show that human hippocampal neurons encode sequence structure in their representational geometry, extracting topological features of experience to add temporal continuity to sensory memories.

The hippocampus rapidly integrates sequence representations during novel multistep predictions

Hannah Tarder-Stoll¹; ¹York University

Memories for temporally extended sequences can be used adaptively to predict future events on multiple timescales, a function that relies on the hippocampus. For such predictions to be useful, they should be updated when the environment changes. Here, we investigated how and when new learning shapes hippocampal representations of temporally extended sequences, and how this updating relates to flexible predictions about future events. Participants first learned sequences of environments in immersive virtual reality and then learned novel environment transitions connecting previously separate sequences. During subsequent fMRI, participants predicted multiple steps into the future in both the newly connected sequence and control sequences that remained separate. Results show that the hippocampus integrated representations of the connected sequence, such that activity patterns became more similar across trials for the connected sequence vs. the unconnected sequences. These integrated sequence representations in the hippocampus incorporated representations of the initial sequences as well as new activity patterns not previously present in either sequence, and predicted participants’ ability to update their predictions in behavior. Together, these results advance our understanding of how the hippocampus contributes to the dynamic emergence of structured knowledge in service of adaptive behavior.

The hippocampus preorders movements for skilled action sequences

Katja Kornysheva¹; ¹University of Birmingham

Plasticity in the subcortical motor basal ganglia-thalamo-cerebellar network plays a key role in the acquisition and the long-term retention of new procedural skills. However, recent findings demonstrate the involvement of a wider cortical and subcortical brain network in the acquisition and consolidation of well-trained actions, including a brain region traditionally associated with declarative memory-the hippocampus. Here, we probe which role these subcortical areas play in skilled motor sequence control, from sequence feature selection during planning to their integration during sequence execution. fMRI data (N = 24; 14 females) was collected after participants learnt to produce four finger press sequences entirely from memory with high movement and timing accuracy over several days. We examined both changes in BOLD activity and its informational content in subcortical regions of interest. Although there was a widespread activity increase in task-relevant regions such as the striatum, the thalamus, and the cerebellum, in particular during sequence execution, the associated activity did not contain information on the motor sequence identity. In contrast, hippocampal activity increased during planning and predicted the order of the upcoming sequence of movements. Our findings suggest that the hippocampus preorders movements for learned sequences, thus contributing to the higher-order control of skilled movements that require flexible retrieval. These findings challenge the traditional taxonomy of episodic and procedural memory and have implications for the rehabilitation of individuals with neurodegenerative disorders.

The capacity of the hippocampus to represent memory items in their temporal position in a sequence is domain-general

Ainsley Temudo¹; ¹University of Utah

Memory systems in humans are less segregated than initially thought as learning tasks from different memory domains (e.g., declarative versus procedural) can recruit similar brain areas such as the hippocampus. However, it remains unclear whether the functional role of these overlapping brain regions is domain-general. Here, we test the hypothesis that the hippocampus encodes and preserves the temporal order of sequential information irrespective of the nature of that information. We used multivariate pattern analyses (MVPA) of functional magnetic resonance imaging (fMRI) data acquired during the execution of learned sequences of movements and objects to assess brain patterns related to procedural and declarative memory processes, respectively. We also tested whether the hippocampus represents information about temporal order of items (here movements and objects in the motor and declarative domains, respectively) in a learned sequence irrespective of their nature. Our results suggest that hippocampal multivoxel activation patterns do not carry information about specific items or temporal position in a random series of objects or movements. Rather, this region codes for the representation of items in their learned temporal position in sequences irrespective of their nature (i.e., item-position coding). These findings indicate that the hippocampus represents the temporal order of sequential information similarly in both the declarative and the motor memory domains and might contribute to the development of item-position maps that provide a cognitive framework for sequential behaviors irrespective of their nature.