Inhibition-excitation balance in the parietal cortex modulates volitional control for auditory and visual multistability

Abstract

Perceptual organisation must select one interpretation from several alternatives to guide behaviour. Computational models suggest that this could be achieved through an interplay between inhibition and excitation across competing types of neural population coding for each interpretation. Here, to test for such models, we used magnetic resonance spectroscopy to measure non-invasively the concentrations of inhibitory γ-aminobutyric acid (GABA) and excitatory glutamate-glutamine (Glx) in several brain regions. Human participants first performed auditory and visual multistability tasks that produced spontaneous switching between percepts. Then, we observed that longer percept durations during behaviour were associated with higher GABA/Glx ratios in the sensory area coding for each modality. When participants were asked to voluntarily modulate their perception, a common factor across modalities emerged: the GABA/Glx ratio in the posterior parietal cortex tended to be positively correlated with the amount of effective volitional control. Our results provide direct evidence implicating that the balance between neural inhibition and excitation within sensory regions resolves perceptual competition. This powerful computational principle appears to be leveraged by both audition and vision, implemented independently across modalities, but modulated by an integrated control process.

Ensemble modeling of auditory streaming reveals potential sources of bistability across the perceptual hierarchy

“…First, it is consistent with the overall trend from a number of studies of resting state activity [86,87], showing a coarser outcome: they reveal greater variability in regions of the brain associated with more cognitive processing, than regions associated with perceptual processing. Second, it is consistent with studies of perceptual bistability indicating that there may be greater individual variability in the balance of excitation and inhibition in regions associated with more cognitive processing [27,29,85]. Third, it is consistent with the prevalence of evidence supporting the role of more general, higher-level processing stages during perceptual bistability [4,7,20,33,[51][52][53][54][55][56][57][58]; if these higher-level sources play a more dominant role in perceptual bistability, this could be due to the greater variety of configurations at later stages of analysis that can generate perceptual bistability.…”

“…These findings are especially interesting in light of the existing evidence that there are substantial individual differences in perceptual bistability [21][22][23][24][25][26][27][28][29]. The implication is that (1) perceptual bistability is pervasive and can emerge across many levels of the auditory hierarchy and (2) there may be greater individual variation in the higher level stages of auditory scene analysis, and less variation at the earliest stages, at least in terms of the magnitude of adaptation and inhibition.…”

“…These behavioral differences lead to patterns of perceptual switching that differ more across listeners than across sessions of the same listener [22]. Second, these switching patterns can be accounted for using differences in the dynamics of adaptation, inhibition and noise [5,7,18,29,38,[42][43][44][45]84]. Third, there are a number of neural correlates of these behavioral signatures in the balance of excitation and inhibition, as measured by magnetic resonance spectroscopy (MRS) [27,29,85].…”

“…Furthermore, the range of levels of adaptation and inhibition that generate a plausible form of bistability is much larger at the highest stage of this hierarchy (Object), while a much more precise tuning of adaptation and inhibition is required at the earliest stage of analysis (Peripheral)-and the Central-analysis parameter tuning is somewhere in-between these extremes. These differences in parameter sensitivity across the model hierarchy raise an interesting possibility, given the evidence for considerable variability across listeners during bistable perception [21][22][23][24][25][26][27][28][29]. It may be that these individual differences across human listeners originate primarily from later stages of the perceptual hierarchy, while earlier stages have a more precise tuning of adaptation and inhibition.…”

“…The study of perceptual bistability, and the more general phenomena of multistability, has the potential to shed light on a number of fundamental principles of perception, as evidenced by four properties. First, its manifestation is characterized by substantial individual variation [21][22][23][24][25][26][27][28][29] providing a potential means for understanding how perceptual function differs across individuals. Second, it is a quite general phenomenon, as there are many forms of ambiguous stimuli that can generate perceptual bistability or multistability [1][2][3][4]6].…”