The Role of the Hippocampus in Prediction and Imagination

Howard Hughes Medical Institute at Harvard University, Cambridge, Massachusetts 02138, USA.
Annual Review of Psychology (Impact Factor: 21.81). 01/2010; 61(1):27-48, C1-8. DOI: 10.1146/annurev.psych.60.110707.163508
Source: PubMed


Traditionally, the hippocampal system has been studied in relation to the goal of retrieving memories about the past. Recent work in humans and rodents suggests that the hippocampal system may be better understood as a system that facilitates predictions about upcoming events. The hippocampus and associated cortical structures are active when people envision future events, and damage that includes the hippocampal region impairs this ability. In rats, hippocampal ensembles preplay and replay event sequences in the absence of overt behavior. If strung together in novel combinations, these sequences could provide the neural building blocks for simulating upcoming events during decision-making, planning, and when imagining novel scenarios. Moreover, in both humans and rodents, the hippocampal system is spontaneously active during task-free epochs and sleep, further suggesting that the system may use idle moments to derive new representations that set the context for future behaviors.

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    • "In humans, functional magnetic resonance imaging studies suggest that the hippocampus is strongly activated by episodic memory retrieval but is activated to an even greater degree when imagining the future than remembering the past (Addis & Schacter 2011, Buckner 2010). Because memories are used for constructing imaginary events, and because imagined events (and the experience of imagining them) likely are then stored in memory for future use, imagining and remembering are almost intractably intertwined and at the very least difficult to separate in an experimental paradigm. "
    • "In addition, given that predictive processes are inherently sequential and given that language comprehension usually deals with sequential input, we assumed that more domaingeneral systems responsible for various types of prediction and sequential processing (such as e.g., the hippocampal system, cf. Addis, Cheng, Roberts, & Schacter, 2011; Buckner, 2010; Fortin, Agster, & Eichenbaum, 2002; Gaesser, Spreng, McLelland, Addis, & Schacter, 2013; Lisman & Redish, 2009) contribute to linguistic predictions as well. "
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    ABSTRACT: DOWNLOAD FULL-TEXT: It is widely agreed upon that linguistic predictions are an integral part of language comprehension. Yet, experimental proof of their existence remains challenging. Here, we introduce a new predictive eye gaze reading task combining eye tracking and functional magnetic resonance imaging (fMRI) that allows us to infer the existence and timing of linguistic predictions via anticipatory eye-movements. Participants read different types of word sequences (i.e., regular sentences, meaningless jabberwocky sentences, non-word lists) up to the pre-final word. The final target word was displayed with a temporal delay and its screen position was dependent on the syntactic word category (nouns vs verbs). During the delay, anticipatory eye-movements into the correct target word area were indicative of linguistic predictions. For fMRI analysis, the predictive sentence conditions were contrasted to the non-word condition, with the anticipatory eye-movements specifying differences in timing across conditions. A conjunction analysis of both sentence conditions revealed the neural substrate of word category prediction, namely a distributed network of cortical and subcortical brain regions including language systems, basal ganglia, thalamus, and hippocampus. Direct contrasts between the regular sentence condition and the jabberwocky condition indicate that prediction of word category in meaningless jabberwocky sentences relies on classical left-hemispheric language systems involving Brodman's area 44/45 in the left inferior frontal gyrus, left superior temporal areas, and the dorsal caudate nucleus. Regular sentences, in contrast, allowed for the prediction of specific words. Word-specific predictions were specifically associated with more widely distributed temporal and parietal cortical systems, most prominently in the right hemisphere. Our results support the presence of linguistic predictions during sentence processing and demonstrate the validity of the predictive eye gaze paradigm for measuring syntactic and semantic aspects of linguistic predictions, as well as for investigating their neural substrates. Copyright © 2015 Elsevier Ltd. All rights reserved.
    Cortex 04/2015; DOI:10.1016/j.cortex.2015.04.011 · 5.13 Impact Factor
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    • "Generating a visual image (in the absence of sensory input) depends on imagination which relies on imaging (Conway 2009). As discussed earlier, imagining the future relies on imaginative re-association of past events (Szpunar, Watson et al. 2007; Addis, Pan et al. 2009; Addis and Schacter 2011) and such re-association enables predictions (Buckner 2010). "
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    ABSTRACT: This article argues both rapid eye movement (REM) and non-rapid eye movement (NREM) sleep contribute to overnight episodic memory processes but their roles differ. Episodic memory may have evolved from memory for spatial navigation in animals and humans. Equally, mnemonic navigation in world and mental space may rely on fundamentally equivalent processes. Consequently, the basic spatial network characteristics of pathways which meet at omnidirectional nodes or junctions may be conserved in episodic brain networks. A pathway is formally identified with the unidirectional, sequential phases of an episodic memory. In contrast, the function of omnidirectional junctions is not well understood. In evolutionary terms, both animals and early humans undertook tours to a series of landmark junctions, to take advantage of resources (food, water and shelter), whilst trying to avoid predators. Such tours required memory for emotionally significant landmark resource-place-danger associations and the spatial relationships amongst these landmarks. In consequence, these tours may have driven the evolution of both spatial and episodic memory. The environment is dynamic. Resource-place associations are liable to shift and new resource-rich landmarks may be discovered, these changes may require re-wiring in neural networks. To realise these changes, REM may perform an associative, emotional encoding function between memory networks, engendering an omnidirectional landmark junction which is instantiated in the cortex during NREM Stage 2. In sum, REM may preplay associated elements of past episodes (rather than replay individual episodes), to engender an unconscious representation which can be used by the animal on approach to a landmark junction in wake. Copyright © 2015. Published by Elsevier Inc.
    Neurobiology of Learning and Memory 04/2015; 122. DOI:10.1016/j.nlm.2015.04.005 · 3.65 Impact Factor
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