Integrative and distinctive coding of visual and conceptual object features in the ventral visual stream

Martin, Chris B.; Douglas, Danielle; Newsome, Rachel N.; Man, Louisa Ly; Barense, Morgan D.

doi:10.7554/elife.31873

Cited by 185 publications

(173 citation statements)

References 99 publications

(159 reference statements)

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“…This is in line with theories on hierarchical message passing in the brain (26)(27)(28). Complex objects are known to be represented in the MTL, such as in perirhinal cortex (31,32), areas known to have direct reciprocal connections with the hippocampus (17,21). Therefore, the hippocampus is ideally positioned to supply complex shape predictions to its immediate cortical neighbours.…”

Section: Discussionsupporting

confidence: 80%

“…For instance, V2 may supply V1 with predictions about the locations of short line elements making up longer lines (26,29). Visual processing in areas of the medial temporal lobe (MTL) most directly connected to the hippocampus, such as perirhinal and parahippocampal cortices, is dominated by high-level objects and scenes, respectively (30)(31)(32), as well as their spatial, temporal, and associative relations (33)(34)(35).…”

Section: Introductionmentioning

confidence: 99%

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Content-based dissociation of hippocampal involvement in prediction

Kok

Rait

Turk‐Browne

2019

Preprint

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Significance StatementTo deal with the noisy and ambiguous sensory signals received by our brain, it is crucial to use prior knowledge of the world to guide perception. Previous research suggests that the hippocampus is involved in predicting upcoming visual stimuli based on prior knowledge. In the current study, we show that hippocampal prediction is specific to expectations of complex objects, whereas for simple features the hippocampus generates an opposite prediction error signal instead. These findings demonstrate that the computational role of the hippocampus can be content-sensitive and refine our understanding of the involvement of memory systems in predictive processing.

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Section: Discussionsupporting

confidence: 80%

Section: Introductionmentioning

confidence: 99%

Content-based dissociation of hippocampal involvement in prediction

Kok

Rait

Turk‐Browne

2019

Preprint

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“…In a recent model of PRC and PHC function (Burke et al, ), we argued that older adults’ object memory improves when objects are embedded in a rich, semantically related context, due to relatively preserved PHC function during aging (see also, Gutchess, Ieuji, & Federmeier, ). Prior studies have also demonstrated greater PHC activation when an object is semantically bound to a particular context (e.g., a hairdryer in a bathroom; Bar & Aminoff, ; Bar, Aminoff, & Schacter, ; Martin, Douglas, Newsome, Man, & Barense, ). In the current study, all objects were strongly semantically related to the context in which they were observed, and each object and scene pairing was unique.…”

Section: Resultsmentioning

confidence: 96%

Visual integration of objects and scenes increases recollection‐based responding despite differential MTL recruitment in young and older adults

Memel¹,

Ryan

2018

Hippocampus

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Unitization, the process of encoding previously independent units as one coherent representation, improves associative memory in both young and older adults, or in some cases, differentially benefits older adults. Unitization of verbal associative pairs may reduce reliance on the hippocampus (HC) for successful encoding and recognition by shifting to familiarity-based processing mediated by perirhinal cortex (PRC). However, this shift was not observed in a recent study of visual associative memory, with equivalent activation in HC and PRC during encoding of visually integrated (unitized) and nonintegrated object and scene pairs. Furthermore, behavioral findings from this study suggested an increase in recollection rather than familiarity during recognition of visually integrated pairs. The present study extends our previous work by focusing on the influence of visual integration on fMRI activation during associative recognition, rather than encoding and these patterns between young and older adults. In contrast to our findings from encoding, visual integration reduced HC and PRC activation during retrieval of object and scene associative pairs across both age groups. However, visual integration increased the correlation between bilateral HC and left parahippocampal (PHC) activation and behavioral performance among older adults, consistent with an increased reliance on recollection. In contrast, visual integration reduced the correlation between HC activation and behavioral performance in young adults, more consistent with findings from the verbal unitization literature. Taken together, these results suggest that associative memory for visually integrated pairs may involve differential recruitment of medial temporal regions in young and older adults.

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“…Another brain structure playing a crucial role in memory of disgust was PRC. Other findings support complex multi-modal item representations in this region 54,55 , such as integration of novel odors with visual category information 56 , or integration of visual with conceptual object features 57 . PRC was also shown to reflect semantic similarity between words 58 , yet here we found no difference in the semantic coherence of word pairs between disgust and fear.…”

Section: Differences In Memory Modulation By Disgust and Fearmentioning

confidence: 81%

Distinct medial-temporal lobe mechanisms of encoding and amygdala-mediated memory reinstatement for disgust and fear

Riegel

Wierzba

Wypych

et al. 2019

Preprint

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Many associative memory traces are charged with emotion that can either impair or enhance subsequent retrieval. Various factors may influence such emotion effects, including the nature of associations and type of emotions. We show that long-term recognition memory of very close verbal associations was enhanced for emotionally charged material, and these effects differed between two negative emotion categories matched for arousal level. Specifically, memory was better for word pairs related to disgust than word pairs related to fear. Furthermore, these two emotions distinctively modulated neural processes during encoding and its relationship with retrieval, regardless of arousal evoked by word pairs. Amygdala and perirhinal cortex activity were associated with enhanced memory for disgust-related unitizations, whereas better memory for fear-related unitizations engaged parahippocampal cortex and hippocampus. Finally, the magnitude of amygdala activation during encoding was related to the subsequent fidelity of hippocampal activity patterns during retrieval. These results show that dissociable neural pathways and reinstatement mechanisms are involved in associative memory for different emotion categories and that arousal alone cannot fully explain emotional influences on associative memory.individually control for the effects of valence and arousal dimensions. Most importantly, this paradigm enabled us to compare the encoding-retrieval similarity of brain activation patterns elicited across two different emotion categories and determine which brain regions promoted this measure of neural reinstatement.We found a memory enhancement effect due to emotion. Moreover, word pairs related to disgust were remembered better than word pairs related to fear, and this effect could not be explained by differences in arousal. We found distinctive neural pathways preferentially engaged in encoding modulation by disgust or fear. Specifically, the left AMY and left PRC were more activated during successful encoding of disgust-related unitized word pairs, whereas right PHC and HC were more activated for fear-related unitized word pairs, even when the level of arousal was regressed out from the analysis. Moreover, during successful encoding of disgust-compared to fearrelated word pairs, we observed an increase in functional connectivity between AMY, PRC and PHC. Finally, for disgusting compared to fearful word pairs, the left AMY encoding activation was found to be critical for the level of trial-by-trial encodingretrieval similarity of brain activation patterns.Altogether, the results show that behavioural and neuronal mechanisms of long-term associative memory can be differently modulated by basic emotion categories, over and above of valence and arousal dimensions. For the first time, we revealed that due to AMY and PRC engagement, disgust as opposed to fear has a strong influence on reinstatement and recognition memory of unitized word pairs, which is in line with its distinctive and perhaps evolutionary-driven role in memorizing ...

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Integrative and distinctive coding of visual and conceptual object features in the ventral visual stream

Cited by 185 publications

References 99 publications

Content-based dissociation of hippocampal involvement in prediction

Content-based dissociation of hippocampal involvement in prediction

Visual integration of objects and scenes increases recollection‐based responding despite differential MTL recruitment in young and older adults

Distinct medial-temporal lobe mechanisms of encoding and amygdala-mediated memory reinstatement for disgust and fear

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