A Neural “Tuning Curve” for Multisensory Experience and Cognitive-Perceptual Schizotypy

Abstract

Our coherent perception of external events is enabled by the integration of inputs from different senses occurring within a range of temporal offsets known as the temporal binding window (TBW), which varies from person to person. A relatively wide TBW may increase the likelihood that stimuli originating from different environmental events are erroneously integrated and abnormally large TBW has been found in psychiatric disorders characterized by unusual perceptual experiences. Despite strong evidence of inter-individual differences in TBW, both within clinical and nonclinical populations, the neurobiological underpinnings of this variability remain unclear. We adopted an integrated strategy linking TBW to temporal dynamics in functional magnetic resonance imaging (fMRI)-resting-state activity and cortical excitation/inhibition (E/I) balance. E/I balance was indexed by glutamate/Gamma-AminoButyric Acid (GABA) concentrations and common variation in glutamate and GABA genes in a healthy sample. Stronger resting-state longrange temporal correlations, indicated by larger power law exponent (PLE), in the auditory cortex, robustly predicted narrower audio-tactile TBW, which was in turn associated with lower cognitive-perceptual schizotypy. Furthermore, PLE was highest and TBW narrowest for individuals with intermediate levels of E/I balance, with shifts towards either extreme resulting in reduced multisensory temporal precision and increased schizotypy, effectively forming a neural "tuning curve" for multisensory experience and schizophrenia risk. Our findings shed light on the neurobiological underpinnings of multisensory integration and its potentially clinically relevant inter-individual variability.

Audiovisual temporal integration and rapid temporal recalibration in adolescents and adults: Age‐related changes and its correlation with autistic traits

“…Individuals with neurodevelopmental disorders are less sensitive to large audiovisual asynchrony, and their wider TBW is correlated with impaired communicative and language skills [Kaganovich, ; Righi et al, ] and aberrant perceptual experiences [Stevenson et al, ]. Furthermore, altered multisensory temporal processing has been found to extend to subclinical populations with elevated levels of autistic [Donohue, Darling, & Mitroff, ] and schizotypal [Ferri et al, ; Ferri, Venskus, Fotia, Cooke, & Romei, ] traits. Compared with the width of the TBW, relatively few studies have examined temporal adaptation in clinical settings.…”

Mathematics and the brain –a category theoretic approach to go beyond the neural correlates of consciousness

“…Traditional models presuppose that stimulus-induced activity as related to external stimuli is simply added to and thus supervenes on the ongoing internal neuronal activitythis amounts to additive rest-stimulus interaction [3,6,34,35,36,96] In contrast, recent findings suggest nonadditive interaction between pre-and post-stimulus activity levels as based on EEG [43], fMRI [31,32,50,88],and computational modelling [84].…”

“…Instead, the level of pre-stimulus activity exerts a strong impact on the level of subsequent post-stimulus activity. In terms of the response amplitude, low pre-stimulus activity levels lead to relative higher post-stimulus activity levels than high prestimulus activity levels [32,50,51]. Importantly, recent studies in both MEG [11,66] and fMRI [51] demonstrate that pre-stimulus variance and its non-additive impact on post-stimulus amplitude/variance is related to conscious contents [2,11,66,93] and the level/state of consciousness [51].…”

Schizotypal Personality Traits and Multisensory Integration: An Investigation Using the McGurk Effect

“…In short, the more temporally and spatially coincident two sensory inputs are, the more likely they originated from the same external event, and thus the more likely that they should be integrated. Temporal processing abilities vary quite drastically between individuals in both clinical and nonclinical groups , and within these individual differences, multisensory temporal precision has been directly associated with the frequency and accuracy of multisensory integration (Ferri et al, 2017;Martin, Giersch, Huron, & van Wassenhove, 2013;Stevenson, Zemtsov, & Wallace, 2013).…”

“…Since multisensory temporal precision has been directly associated with the frequency and accuracy of multisensory integration (Ferri et al, 2017;Martin et al, 2013;Stevenson et al, 2013), it is not surprising that individuals with schizophrenia who have temporal deficits also have altered multisensory integration (de Jong, Hodiamont, Van den Stock, & de Gelder, 2009;White et al, 2014;Williams, Light, Braff, & Ramachandran, 2010, but see Martin et al, 2013;Romero et al, 2016). These multisensory integration deficits in schizophrenia have been found specifically in the realm of audiovisual speech integration (de Gelder et al, 2002;Pearl et al, 2009;Ross, Saint-Amour, Leavitt, Molholm, et al, 2007;Stekelenburg, Maes, Van Gool, Sitskoorn, & Vroomen, 2013, but see Surguladze et al, 2001).…”