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Distinct patterns of connectivity between brain regions underlie the intra-modal and cross-modal value-driven modulations of the visual cortex

Distinct patterns of connectivity between brain regions underlie the intra-modal and cross-modal value-driven modulations of the visual cortex
Distinct patterns of connectivity between brain regions underlie the intra-modal and cross-modal value-driven modulations of the visual cortex

Past reward associations may be signaled from different sensory modalities; however, it remains unclear how different types of reward-associated stimuli modulate sensory perception. In this human fMRI study (female and male participants), a visual target was simultaneously presented with either an intra- (visual) or a cross-modal (auditory) cue that was previously associated with rewards. We hypothesized that, depending on the sensory modality of the cues, distinct neural mechanisms underlie the value-driven modulation of visual processing. Using a multivariate approach, we confirmed that reward-associated cues enhanced the target representation in early visual areas and identified the brain valuation regions. Then, using an effective connectivity analysis, we tested three possible patterns of connectivity that could underlie the modulation of the visual cortex: a direct pathway from the frontal valuation areas to the visual areas, a mediated pathway through the attention-related areas, and a mediated pathway that additionally involved sensory association areas. We found evidence for the third model demonstrating that the reward-related information in both sensory modalities is communicated across the valuation and attention-related brain regions. Additionally, the superior temporal areas were recruited when reward was cued cross-modally. The strongest dissociation between the intra- and cross-modal reward-driven effects was observed at the level of the feedforward and feedback connections of the visual cortex estimated from the winning model. These results suggest that, in the presence of previously rewarded stimuli from different sensory modalities, a combination of domain-general and domain-specific mechanisms are recruited across the brain to adjust the visual perception. SIGNIFICANCE STATEMENT Reward has a profound effect on perception, but it is not known whether shared or disparate mechanisms underlie the reward-driven effects across sensory modalities. In this human fMRI study, we examined the reward-driven modulation of the visual cortex by visual (intra-modal) and auditory (cross-modal) reward-associated cues. Using a model-based approach to identify the most plausible pattern of inter-regional effective connectivity, we found that higher-order areas involved in the valuation and attentional processing were recruited by both types of rewards. However, the pattern of connectivity between these areas and the early visual cortex was distinct between the intra- and cross-modal rewards. This evidence suggests that, to effectively adapt to the environment, reward signals may recruit both domain-general and domain-specific mechanisms.

fMRI, reward, sensory modality, value, visual perception
0270-6474
7361-7375
Antono, Jessica Emily
9e03e2d3-1d8d-4b08-bf00-cab5fb1cf8db
Dang, Shilpa
beaa809b-b64f-41a4-b134-48a42b5e97f8
Auksztulewicz, Ryszard
bac30103-5fb2-453c-8e15-ff249a970684
Pooresmaeili, Arezoo
319b6aed-8454-4ad2-b16e-8fadfdfd2e53
Antono, Jessica Emily
9e03e2d3-1d8d-4b08-bf00-cab5fb1cf8db
Dang, Shilpa
beaa809b-b64f-41a4-b134-48a42b5e97f8
Auksztulewicz, Ryszard
bac30103-5fb2-453c-8e15-ff249a970684
Pooresmaeili, Arezoo
319b6aed-8454-4ad2-b16e-8fadfdfd2e53

Antono, Jessica Emily, Dang, Shilpa, Auksztulewicz, Ryszard and Pooresmaeili, Arezoo (2023) Distinct patterns of connectivity between brain regions underlie the intra-modal and cross-modal value-driven modulations of the visual cortex. The Journal of Neuroscience, 43 (44), 7361-7375. (doi:10.1523/JNEUROSCI.0355-23.2023).

Record type: Article

Abstract

Past reward associations may be signaled from different sensory modalities; however, it remains unclear how different types of reward-associated stimuli modulate sensory perception. In this human fMRI study (female and male participants), a visual target was simultaneously presented with either an intra- (visual) or a cross-modal (auditory) cue that was previously associated with rewards. We hypothesized that, depending on the sensory modality of the cues, distinct neural mechanisms underlie the value-driven modulation of visual processing. Using a multivariate approach, we confirmed that reward-associated cues enhanced the target representation in early visual areas and identified the brain valuation regions. Then, using an effective connectivity analysis, we tested three possible patterns of connectivity that could underlie the modulation of the visual cortex: a direct pathway from the frontal valuation areas to the visual areas, a mediated pathway through the attention-related areas, and a mediated pathway that additionally involved sensory association areas. We found evidence for the third model demonstrating that the reward-related information in both sensory modalities is communicated across the valuation and attention-related brain regions. Additionally, the superior temporal areas were recruited when reward was cued cross-modally. The strongest dissociation between the intra- and cross-modal reward-driven effects was observed at the level of the feedforward and feedback connections of the visual cortex estimated from the winning model. These results suggest that, in the presence of previously rewarded stimuli from different sensory modalities, a combination of domain-general and domain-specific mechanisms are recruited across the brain to adjust the visual perception. SIGNIFICANCE STATEMENT Reward has a profound effect on perception, but it is not known whether shared or disparate mechanisms underlie the reward-driven effects across sensory modalities. In this human fMRI study, we examined the reward-driven modulation of the visual cortex by visual (intra-modal) and auditory (cross-modal) reward-associated cues. Using a model-based approach to identify the most plausible pattern of inter-regional effective connectivity, we found that higher-order areas involved in the valuation and attentional processing were recruited by both types of rewards. However, the pattern of connectivity between these areas and the early visual cortex was distinct between the intra- and cross-modal rewards. This evidence suggests that, to effectively adapt to the environment, reward signals may recruit both domain-general and domain-specific mechanisms.

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JNEUROSCI.0355-23.2023.full - Accepted Manuscript
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Accepted/In Press date: 26 August 2023
e-pub ahead of print date: 8 September 2023
Published date: 1 November 2023
Additional Information: Funding Information: We thank Tabea Hildebrand, Jana Znaniewitz, and Sanna Peter for their help with the data collection. We also thank Dr. Carsten Schmidt-Samoa and Dr. Peter Dechent for their technical assistance, and Prof. Melanie Wilke and Dr. Roberto Goya-Maldonado for their input and suggestions. This work was supported by an ERC Starting Grant (no: 716846) to AP. Publisher Copyright: © 2023 Society for Neuroscience. All rights reserved. Copyright © 2023 the authors.
Keywords: fMRI, reward, sensory modality, value, visual perception

Identifiers

Local EPrints ID: 484567
URI: http://eprints.soton.ac.uk/id/eprint/484567
ISSN: 0270-6474
PURE UUID: 716d8e7f-7e78-49f5-b430-8ba18c1aebf9
ORCID for Arezoo Pooresmaeili: ORCID iD orcid.org/0000-0002-4369-8838

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Date deposited: 16 Nov 2023 18:02
Last modified: 18 Mar 2024 04:10

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Contributors

Author: Jessica Emily Antono
Author: Shilpa Dang
Author: Ryszard Auksztulewicz
Author: Arezoo Pooresmaeili ORCID iD

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