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Research Articles, Behavioral/Cognitive

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

Jessica Emily Antono, Shilpa Dang, Ryszard Auksztulewicz and Arezoo Pooresmaeili
Journal of Neuroscience 8 September 2023, JN-RM-0355-23; DOI: https://doi.org/10.1523/JNEUROSCI.0355-23.2023
Jessica Emily Antono
1Perception and Cognition Lab, European Neuroscience Institute Goettingen- A Joint Initiative of the University Medical Center Goettingen and the Max-Planck-Society, Germany, Grisebachstrasse 5, 37077 Goettingen, Germany
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Shilpa Dang
1Perception and Cognition Lab, European Neuroscience Institute Goettingen- A Joint Initiative of the University Medical Center Goettingen and the Max-Planck-Society, Germany, Grisebachstrasse 5, 37077 Goettingen, Germany
2School of Artificial Intelligence and Data Science, Indian Institute of Technology Jodhpur, Hauz Khas, New Delhi-110016, India
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Ryszard Auksztulewicz
3Center for Cognitive Neuroscience Berlin, Free University Berlin, Habelschwerdter Allee 45, 14195 Berlin, Germany
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Arezoo Pooresmaeili
1Perception and Cognition Lab, European Neuroscience Institute Goettingen- A Joint Initiative of the University Medical Center Goettingen and the Max-Planck-Society, Germany, Grisebachstrasse 5, 37077 Goettingen, Germany
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Abstract

Past reward associations may be signalled 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.

Footnotes

  • The authors declare no competing interests.

  • 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.

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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
Jessica Emily Antono, Shilpa Dang, Ryszard Auksztulewicz, Arezoo Pooresmaeili
Journal of Neuroscience 8 September 2023, JN-RM-0355-23; DOI: 10.1523/JNEUROSCI.0355-23.2023

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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
Jessica Emily Antono, Shilpa Dang, Ryszard Auksztulewicz, Arezoo Pooresmaeili
Journal of Neuroscience 8 September 2023, JN-RM-0355-23; DOI: 10.1523/JNEUROSCI.0355-23.2023
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