Evidence that neural information flow is reversed between object perception and object reconstruction from memory

Linde-Domingo, Juan; Treder, Matthias S.; Kerrén, Casper; Wimber, Maria

doi:10.1038/s41467-018-08080-2

Cited by 126 publications

(225 citation statements)

References 58 publications

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“…These observations make the prediction that initial drive from the hippocampus during memory retrieval should propagate backwards through the visual system. Electrophysiological recordings from the macaque (Naya et al, 2001) and human (Linde-Domingo et al, 2019;Dijkstra et al, 2019), as well as computational modeling (Horikawa & Kamitani, 2017) support this idea.We simulated such a process in a hierarchical network. While highly simplified, this simulation captured the dominant features of our data, providing a possible explanation for our observations.…”

mentioning

confidence: 87%

“…Memory reinstatement is hypothesized to begin with the hippocampus, a region bidirectionally connected to high-level visual areas in ventral temporal cortex (Felleman & Essen, 1991). Reinstated activity is then thought to propagate backwards through visual cortex (Linde-Domingo et al, 2019;Dijkstra et al, 2019). Here, we explored whether a simple hierarchical model could be adapted to account for both our perception and memory results.…”

Section: Perception and Memory Responses Can Be Simulated With A Bidimentioning

confidence: 99%

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Perception and memory have distinct spatial tuning properties in human visual cortex

Favila

Kuhl

Winawer

2019

Preprint

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Neural activity evoked during perception is thought to be reactivated during later memory retrieval. While many studies have found evidence for memory reactivation in visual cortex, few have characterized differences between stimulus-driven and mnemonic activation. Here, we leveraged population receptive field (pRF) models to quantify spatial activity in the human visual system during perception and long-term memory retrieval. We found that mnemonic activity, like perceptual activity, was precisely retinotopically mapped. However, we also observed large, systematic differences between perceptual and mnemonic activity in measures of amplitude and precision. The magnitude of these differences varied according to position in the visual hierarchy, with the largest differences observed in early areas. These differences could not be accounted for by the fact that memory data had reduced signal-to-noise or the possibility that it contained a mixture of successful and failed retrieval trials. Finally, we explore predictions from several models, showing that a simple hierarchical model with reciprocal feedforward and feedback connections accounts for many of our observations. Our results reveal novel distinctions between perceptual and mnemonic activity in visual cortex and provide insight into the computational constraints governing memory reactivation. 1/21visual cortex during perception (Kay et al., 2013b). Using these models to quantify memory-triggered activity in the visual system offers the opportunity to precisely model reactivation in visual cortex and its relationship to visual perception. In particular, the fact that pRF models are stimulus-referred may aid in interpreting differences between perception and memory activation patterns by projecting these differences onto a small number of physical dimensions.Here, we used pRF models to characterize the properties of mnemonic activity in human visual cortex. We first trained human subjects to associate spatially localized stimuli with colored fixation cues. We then measured stimulus-triggered and memory-triggered activity in visual cortex using fMRI. Separately, we fit pRF models to independent fMRI data, which allowed us to estimate receptive field location and size within multiple visual field maps for each subject. Using pRF-based analyses, we quantified the location, amplitude, and precision of activity throughout these visual field maps during perception and memory retrieval. Finally, we explored what kind of cortical computations could account for our observations by simulating responses using a stimulus-referred pRF model and a simple hierarchical model of neocortex. Results BehaviorPrior to being scanned, subjects participated in a behavioral training session. During this session, subjects learned to associate four colored fixation dot cues with four stimuli. The four stimuli were unique radial frequency patterns presented at 45, 135, 225, or 315 degrees of polar angle and 2 degrees of eccentricity ( Fig. 1a,b). Subjects alternated between study and test ...

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confidence: 87%

Section: Perception and Memory Responses Can Be Simulated With A Bidimentioning

confidence: 99%

Perception and memory have distinct spatial tuning properties in human visual cortex

Favila

Kuhl

Winawer

2019

Preprint

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“…The EEG pattern classifier approach has been successfully adopted to differentiate between the retrieval of perceptual and semantic information of an episodic memory (Linde-Domingo et al, 2019) and in different mechanisms of memory (Jafarpour, Horner, Fuentemilla, Penny, & Duzel, 2013). The timing of the retrieval of an autobiographical memory has been shown to occur between 400 and 600 ms even when it is only spontaneously recalled (Addante, 2015;Hebscher, Ibrahim, & Gilboa, 2019).…”

Section: Discussionmentioning

confidence: 99%

“…Recent neuroimaging studies showed that both incidental (Forkmann, Wiech, Sommer, & Bingel, 2015) and voluntary (Fairhurst, Fairhurst, Berna, & Tracey, 2012) reinstatement of autobiographical pain involves partial reinstatement of activity in the brain areas that processed the perception of nociceptive stimuli. Recent advances in multivariate pattern analysis methods showed that brain activity patterns can be tracked during the encoding of new episodes and can be observed also during the retrieval of those episodes (Chen et al, 2017;Johnson, McDuff, Rugg, & Norman, 2009;Linde-Domingo, Treder, Kerrén, & Wimber, 2019;Michelmann, Bowman, & Hanslmayr, 2016;Staresina, Henson, Kriegeskorte, & Alink, 2012). Using this approach, we sought the first direct evidence for online reactivation of autobiographical memories when participants are required to empathize with others' physical pain.…”

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confidence: 99%

EEG and fMRI Evidence for Autobiographical Memory Reactivation in Empathy

Meconi¹,

Linde-Domingo²,

Ferreira³

et al. 2019

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Empathy relies on the ability to mirror and to explicitly infer others' inner states. Studies on healthy populations show consistent evidence supporting the idea that our memories play a role in empathy when building a representation of others' inner states (Buckner & Carroll, 2007a; Spreng & Grady, 2009a;Spreng, Mar, & Kim, 2009). However, direct evidence of a reactivation of autobiographical memories (AM) when it comes to empathizing with others' inner states is yet to be shown. To address this question, we conducted two experiments where we recorded electrophysiological (Exp 1) and hemodynamic activity (Exp2) from two independent samples of participants. In Exp 1, EEG was recorded from 28 participants who performed a classic empathy task, i.e. a pain decision task in which targets for empathy were depicted in painful scenes for which participants either did or did not have an AM, followed by a task that explicitly required memory retrieval of the AM and non-AM scenes. The retrieval task acted as a 'localizer' to extract the neural fingerprints of AM and non-AM scenes, which could then be used to probe data from the empathy task. A state-of-the-art EEG pattern classifier was trained and tested across tasks and showed evidence for AM reactivation when participants were preparing their judgement in the empathy task. Participants self-reported higher empathy for people depicted in situations they had experienced themselves (for which they would have an AM) as compared to situations they had not experienced. This behavioral result was replicated in a second fMRI Experiment, where hemodynamic responses were measured from an independent sample of 28 participants. Furthermore, fMRI results showed activation in the brain networks that have been extensively shown in previous studies to underlie both AM retrieval and empathy (study reports behavioral, electrophysiological and fMRI evidence that robustly supports the involvement of autobiographical memory reactivation in empathy. Significance statementHuman empathy is at the basis of our ability to bond with other people and interact in a meaningful way. Since we cannot fully experience what someone else is feeling, a big challenge in psychology is to understand how empathy occurs. We might use our own mind and experience as a model to represent others' inner states. To shed new light onto this debate, we used established and novel paradigms and analysis tools in the fields of social and cognitive neuroscience. In two experiments, we present compelling evidence that shows that participants reactivate AMs when asked to empathize with another person. The current study has the potential to increase scientific knowledge to ultimately impact a wide range of professions working with people in need in the health and social sectors.

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“…Brain organization is thought to be grossly hierarchical [92]. As a first approximation, we can ignore feedback circuits and consider the processing of information at each level from the prior processing stage [27,51]. We have previously hypothesized, and demonstrated in a model, that proper information processing at each stage requires a balance between information flow-through and information from the area itself, related to local resonance properties [61].…”

Section: Why Is Information Flow Important?mentioning

confidence: 99%

In silicohippocampal modeling for multi-target pharmacotherapy in schizophrenia

Sherif

Neymotin

Lytton

2019

Preprint

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Background: Treatment of schizophrenia has had limited success in treating core cognitive symptoms. The evidence of multi-gene involvement suggests that multi-target therapy may be needed. Meanwhile, the complexity of schizophrenia pathophysiology and psychopathology, coupled with the species-specificity of much of the symptomatology, places limits on analysis via animal models, in vitro assays, and patient assessment. Multiscale computer modeling complements these traditional modes of study.Methods: Using a hippocampal CA3 computer model with 1200 neurons, we examined the effects of alterations in NMDAR, HCN (I h current), and GABA A R on information flow (measured with normalized transfer entropy), and in gamma activity in local field potential (LFP).Results: Altering NMDARs, GABA A R, I h , individually or in combination, modified information flow in an inverted-U shape manner, with information flow reduced at low and high levels of these parameters. The strong information flow seen at the peaks were associated with an intermediate level of synchrony, seen as an intermediate level of gamma activity in the LFP, and an intermediate level of pyramidal cell excitability.Conclusions: Our results are consistent with the idea that overly low or high gamma power is associated with pathological information flow and information processing. These data suggest the need for careful titration of schizophrenia pharmacotherapy to avoid extremes that alter information flow in different ways. These results also identify gamma power as a potential biomarker for monitoring pathology and multi-target pharmacotherapy.

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Evidence that neural information flow is reversed between object perception and object reconstruction from memory

Cited by 126 publications

References 58 publications

Perception and memory have distinct spatial tuning properties in human visual cortex

Perception and memory have distinct spatial tuning properties in human visual cortex

EEG and fMRI Evidence for Autobiographical Memory Reactivation in Empathy

In silicohippocampal modeling for multi-target pharmacotherapy in schizophrenia

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