Abstract

Cross-modal effects provide a model framework for investigating hierarchical inter-areal processing, particularly, under conditions where unimodal cortical areas receive contextual feedback from other modalities. Here, using complementary behavioral and brain imaging techniques, we investigated the functional networks participating in face and voice processing during gender perception, a high-level feature of voice and face perception. Within the framework of a signal detection decision model, Maximum likelihood conjoint measurement (MLCM) was used to estimate the contributions of the face and voice to gender comparisons between pairs of audio-visual stimuli in which the face and voice were independently modulated. Top–down contributions were varied by instructing participants to make judgments based on the gender of either the face, the voice or both modalities (N = 12 for each task). Estimated face and voice contributions to the judgments of the stimulus pairs were not independent; both contributed to all tasks, but their respective weights varied over a 40-fold range due to top–down influences. Models that best described the modal contributions required the inclusion of two different top–down interactions: (i) an interaction that depended on gender congruence across modalities (i.e., difference between face and voice modalities for each stimulus); (ii) an interaction that depended on the within modalities’ gender magnitude. The significance of these interactions was task dependent. Specifically, gender congruence interaction was significant for the face and voice tasks while the gender magnitude interaction was significant for the face and stimulus tasks. Subsequently, we used the same stimuli and related tasks in a functional magnetic resonance imaging (fMRI) paradigm (N = 12) to explore the neural correlates of these perceptual processes, analyzed with Dynamic Causal Modeling (DCM) and Bayesian Model Selection. Results revealed changes in effective connectivity between the unimodal Fusiform Face Area (FFA) and Temporal Voice Area (TVA) in a fashion that paralleled the face and voice behavioral interactions observed in the psychophysical data. These findings explore the role in perception of multiple unimodal parallel feedback pathways.

Highlights

  • Hierarchical processing has long played a prominent role in understanding cortical organization and function (Hubel and Wiesel, 1962, 1965; Rockland and Pandya, 1979; Felleman and Van Essen, 1991; Ferster et al, 1996; Angelucci et al, 2002; Angelucci and Bressloff, 2006)

  • Dynamic Causal Modeling To explore the neural substrate of the multi-modal integration revealed by the psychophysical experiments, we performed a series of functional imaging experiments in which we evaluated the effective connectivity between areas implicated in processing face and voice stimuli

  • When subjects were focusing on the gender of the stimulus, there was evidence of the gender magnitude interaction observed in the psychophysical analyses, and evidence for modulation of the effective connectivity from Fusiform Face Area (FFA) to Temporal Voice Area (TVA) in response to face gender information

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Summary

INTRODUCTION

Hierarchical processing has long played a prominent role in understanding cortical organization and function (Hubel and Wiesel, 1962, 1965; Rockland and Pandya, 1979; Felleman and Van Essen, 1991; Ferster et al, 1996; Angelucci et al, 2002; Angelucci and Bressloff, 2006). Despite spectacular conceptual progress in the context of predictive coding that conceives of feedforward pathways as transmitting prediction errors and feedback pathways predictions (Clark, 2013), Jean Bullier’s question “What is fed back” (Bullier, 2006) remains as urgent today as it was when he formulated it This is largely because experimentally it is considerably more difficult to invasively manipulate the top–down processes that come under the banner of predictions than it is to record the consequences of changes in the sensorium on bottom-up processes (Zagha, 2020; Vezoli et al, 2021). While Watson et al (2013) were able to detect cross-modal effects, they were unable to describe the rules by which voice and face cues are combined qualitatively and quantitatively We can obviate these problems by using the psychophysical method of maximum likelihood conjoint measurement (MLCM) that links gender comparisons to a signal detection model of the decision process. In order to clarify the neural correlates of the perceptual processes, we employ functional imaging to elucidate the effective connectivity underlying the behavioral responses

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