Scientific Understanding of Consciousness
Hippocampal Place-Cell Episodic Memory Context Basis for Recollection
Science 29 November 2013: Vol. 342 no. 6162 pp. 1111-1114
Neural Activity in Human Hippocampal Formation Reveals the Spatial Context of Retrieved Memories
Jonathan F. Miller, Markus Neufang, Alec Solway, Armin Brandt, Michael Trippe, Irina Mader, Stefan Hefft, Max Merkow, Sean M. Polyn, Joshua Jacobs, Michael J. Kahana, Andreas Schulze-Bonhage
Drexel University, Philadelphia, PA 19104, USA.
Epilepsy Center, University Medical Center, Freiburg, Germany.
University of Pennsylvania, Philadelphia, PA 19104, USA.
In many species, spatial navigation is supported by a network of place cells that exhibit increased firing whenever an animal is in a certain region of an environment. Does this neural representation of location form part of the spatiotemporal context into which episodic memories are encoded? We recorded medial temporal lobe neuronal activity as epilepsy patients performed a hybrid spatial and episodic memory task. We identified place-responsive cells active during virtual navigation and then asked whether the same cells activated during the subsequent recall of navigation-related memories without actual navigation. Place-responsive cell activity was reinstated during episodic memory retrieval. Neuronal firing during the retrieval of each memory was similar to the activity that represented the locations in the environment where the memory was initially encoded.
When one encounters an old friend and remembers the time they last met, often the place of meeting and surrounding circumstances come to mind. This is the hallmark of episodic memory: the capacity to store and later retrieve memories that are bound to a particular place and time. Theories of episodic memory posit that the brain supports this ability by continually maintaining an updated representation of the current spatiotemporal context, which is a neural representation of space, time, and other aspects of one’s current cognitive milieu. When the brain forms a new episodic memory, these theories predict that the content of the experience becomes associated with the current spatial and temporal context. When the memory is retrieved, this prior context is partially reinstated, focusing one’s thoughts on the time and place of the remembered episode. This reinstatement not only provides the phenomenological experience of remembering, but also helps to cue other memories experienced within the same or related contexts.
Although it is well established that the hippocampus and surrounding medial-temporal-lobe (MTL) structures play a central role in the formation and retrieval of context-mediated memories, we know far less about how these memory processes manifest in the activities of individual MTL neurons. Much of what is known about the neural coding properties of hippocampal and MTL neurons comes from studies of rodent spatial navigation, where individual neurons respond preferentially at specific locations within a given contextually defined spatial environment. Similar neuronal responses have also been identified in the human hippocampus during virtual spatial navigation. The context-dependent firing of these neurons and their dependence on the animal’s goal state or past history of experienced cues have led some to speculate that the neural representation of space in the hippocampus is part of a broader network of neurons that encode episodic memories more generally. This hypothesis suggests that the same neural structures and computations that enable the learning of a spatial layout via place-cell activity also facilitate the encoding of episodic memories. However, according to a prominent alternative account, the spatial coding functions of the hippocampus are part of a context module that operates independently of the computations that encode the content of a memory
Because human neural recordings are rarely possible, little is known about the neural substrates of spontaneous verbal recall. Nonetheless, several recent studies have established the general phenomena of content reinstatement, whereby the attributes of an item at encoding become reinstated just before recall. This has been shown for human hippocampal neurons that are selective for taxonomic categories, or possibly individual items, and also for distributed patterns of intracranial electroencephalography and hemodynamic activity. Reinstatement is not specific to an individual item but also activates neighboring items, as would be expected if those neighboring items provide an abstract temporal context for the recalled item. Such a temporal context signal may be reflected in the recent discovery of individual neurons in the rodent hippocampus that appear to encode the relative times of behaviorally important events.
Our finding that spontaneous recall of an item reactivates its spatial context provides direct neural evidence for theories of episodic memory that postulate context reinstatement as the basis for recollection. This result also implies that the spatial coding identified with the hippocampal place-cell system is part of a more general engine of episodic memory in which items become associated with their spatiotemporal contexts, and retrieval of items reinstates those contexts to help cue other context-appropriate memories.
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