Reinstatement of Associative Memories in Early Visual Cortex Is Signaled by the Hippocampus

Bosch, Sander; Jehee, Janneke; Fernández, Guillén; Doeller, Christian F.

doi:10.1523/jneurosci.0805-14.2014

Cited by 150 publications

(151 citation statements)

References 65 publications

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“…Furthermore, fMRI studies have revealed predictive signals in the hippocampus (13,26,27), and Reddy et al (28) reported anticipatory firing to expected stimuli in the medial temporal lobe, including the hippocampus. One intriguing possibility is that predictive signals from the hippocampus are fed back to sensory cortex (13,29,30).…”

Section: Discussionmentioning

confidence: 99%

Prior expectations induce prestimulus sensory templates

Kok

Mostert

Lange

2017

Proc. Natl. Acad. Sci. U.S.A.

310

331

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Perception can be described as a process of inference, integrating bottom-up sensory inputs and top-down expectations. However, it is unclear how this process is neurally implemented. It has been proposed that expectations lead to prestimulus baseline increases in sensory neurons tuned to the expected stimulus, which in turn, affect the processing of subsequent stimuli. Recent fMRI studies have revealed stimulus-specific patterns of activation in sensory cortex as a result of expectation, but this method lacks the temporal resolution necessary to distinguish pre-from poststimulus processes. Here, we combined human magnetoencephalography (MEG) with multivariate decoding techniques to probe the representational content of neural signals in a time-resolved manner. We observed a representation of expected stimuli in the neural signal shortly before they were presented, showing that expectations indeed induce a preactivation of stimulus templates. The strength of these prestimulus expectation templates correlated with participants' behavioral improvement when the expected feature was task-relevant. These results suggest a mechanism for how predictive perception can be neurally implemented.prediction | perceptual inference | predictive coding | feature-based expectation | feature-based attention P erception is heavily influenced by prior knowledge (1-3). Accordingly, many theories cast perception as a process of inference, integrating bottom-up sensory inputs and top-down expectations (4-6). However, it is unclear how this integration is neurally implemented. It has been proposed that prior expectations lead to baseline increases in sensory neurons tuned to the expected stimulus (7-9), which in turn, leads to improved neural processing of matching stimuli (10, 11). In other words, expectations may induce stimulus templates in sensory cortex before the actual presentation of the stimulus. Alternatively, topdown influences in sensory cortex may exert their influence only after the bottom-up stimulus has been initially processed, and the integration of the two sources of information may become apparent only during later stages of sensory processing (12).The evidence necessary to distinguish between these hypotheses has been lacking. fMRI studies have revealed stimulusspecific patterns of activation in sensory cortex as a result of expectation (9, 13), but this method lacks the temporal resolution necessary to distinguish pre-from poststimulus periods. Here, we combined magnetoencephalography (MEG) with multivariate decoding techniques to probe the representational content of neural signals in a time-resolved manner (14-17). The experimental paradigm was virtually identical to the ones used in our previous fMRI studies that studied how expectations modulate stimulus-specific patterns of activity in the primary visual cortex (9, 11). We trained a forward model to decode the orientation of task-irrelevant gratings from the MEG signal (18,19) and applied this decoder to trials in which participants expected a grating of a pa...

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Section: Discussionmentioning

confidence: 99%

Prior expectations induce prestimulus sensory templates

Kok

Mostert

Lange

2017

Proc. Natl. Acad. Sci. U.S.A.

310

331

View full text Add to dashboard Cite

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“…It was found that stimulus-specific scene patterns were reactivated in the parahippocampal cortex when participants indicated they had recollected the target scene, but not when they indicated they had no recollection (Fig. 2) (Staresina et al 2012; see also, Ritchey et al 2008;Bosch et al 2014). This is an important step toward demonstrating that episodic reinstatement in the MTL can be observed at the level of individual memory representations.…”

Section: Multivariate Fmri and Connectivity Analyses Of Episodic Retrmentioning

confidence: 90%

Noninvasive Functional and Anatomical Imaging of the Human Medial Temporal Lobe

Brown

Staresina

Wagner

2015

Cold Spring Harb Perspect Biol

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The ability to remember life's events, and to leverage memory to guide behavior, defines who we are and is critical for everyday functioning. The neural mechanisms supporting such mnemonic experiences are multiprocess and multinetwork in nature, which creates challenges for studying them in humans and animals. Advances in noninvasive neuroimaging techniques have enabled the investigation of how specific neural structures and networks contribute to human memory at its many cognitive and mechanistic levels. In this review, we discuss how functional and anatomical imaging has provided novel insights into the types of information represented in, and the computations performed by, specific medial temporal lobe (MTL) regions, and we consider how interactions between the MTL and other cortical and subcortical structures influence what we learn and remember. By leveraging imaging, researchers have markedly advanced understanding of how the MTL subserves declarative memory and enables navigation of our physical and mental worlds.O ne of the central aims of cognitive neuroscience research is to understand how human brain function relates to the mnemonic experiences that define much of who we are as individuals. Recent advances in noninvasive human neuroimaging have given rise to novel insights about the neural foundations of human memory, and have allowed neuroscientists to draw important connections between human and nonhuman animal research. Although noninvasive imaging techniques remain limited in their spatial resolution (we cannot yet describe the behavior of individual neurons in the human brain without implanting electrodes in patients undergoing brain surgery), they also have important strengths that have allowed researchers to significantly advance mechanistic accounts of learning and memory. In this review, we begin with a historical perspective on noninvasive neuroimaging techniques and their application to the study of memory encoding. We then introduce more recent cutting-edge methodological approaches, as we discuss specific domains of memory theory that they have helped advance. Drawing on research examining the medial temporal lobe (MTL), we emphasize the power of such imaging techniques to allow scientists to make inferences about the types of mnemonic information represented by distinct brain areas, and to understand how the funcEditors: Eric R. Kandel, Yadin Dudai, and Mark R. Mayford Additional Perspectives on Learning and Memory available at

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“…On the other hand, only a few studies have addressed how content-general memory processes promote the distributed reactivation of stimulus-specific patterns during memory retrieval, and most studies have focused on a narrow subset of brain regions. For example, hippocampal activation has been shown to promote the cortical reinstatement of scene-specific (Ritchey et al, 2013) and categorical source information (such as faces vs. scenes; Gordon et al, 2013) and of low-level visual gratings (Bosch, Jehee, Fernandez, & Doeller, 2014).…”

Section: Introductionmentioning

confidence: 99%

Distributed Patterns of Reactivation Predict Vividness of Recollection

St-Laurent

Abdi

Buchsbaum

2015

Journal of Cognitive Neuroscience

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Abstract■ According to the principle of reactivation, memory retrieval evokes patterns of brain activity that resemble those instantiated when an event was first experienced. Intuitively, one would expect neural reactivation to contribute to recollection (i.e., the vivid impression of reliving past events), but evidence of a direct relationship between the subjective quality of recollection and multiregional reactivation of item-specific neural patterns is lacking. The current study assessed this relationship using fMRI to measure brain activity as participants viewed and mentally replayed a set of short videos. We used multivoxel pattern analysis to train a classifier to identify individual videos based on brain activity evoked during perception and tested how accurately the classifier could distinguish among videos during mental replay. Classification accuracy correlated positively with memory vividness, indicating that the specificity of multivariate brain patterns observed during memory retrieval was related to the subjective quality of a memory. In addition, we identified a set of brain regions whose univariate activity during retrieval predicted both memory vividness and the strength of the classifier's prediction irrespective of the particular video that was retrieved. Our results establish distributed patterns of neural reactivation as a valid and objective marker of the quality of recollection. ■

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Reinstatement of Associative Memories in Early Visual Cortex Is Signaled by the Hippocampus

Cited by 150 publications

References 65 publications

Prior expectations induce prestimulus sensory templates

Prior expectations induce prestimulus sensory templates

Noninvasive Functional and Anatomical Imaging of the Human Medial Temporal Lobe

Distributed Patterns of Reactivation Predict Vividness of Recollection

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