Dataset Information

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 ?-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.

SUBMITTER: Kondo HM

PROVIDER: S-EPMC6162284 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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

Kondo Hirohito M HM Pressnitzer Daniel D Shimada Yasuhiro Y Kochiyama Takanori T Kashino Makio M

Scientific reports 20180928 1

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 br ...[more]

PMID: 30267021

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Project description:In multistability, a constant stimulus induces alternating perceptual interpretations. For many forms of visual multistability, the transition from one interpretation to another ("perceptual switch") is accompanied by a dilation of the pupil. Here we ask whether the same holds for auditory multistability, specifically auditory streaming. Two tones were played in alternation, yielding four distinct interpretations: the tones can be perceived as one integrated percept (single sound source), or as segregated with either tone or both tones in the foreground. We found that the pupil dilates significantly around the time a perceptual switch is reported ("multistable condition"). When participants instead responded to actual stimulus changes that closely mimicked the multistable perceptual experience ("replay condition"), the pupil dilated more around such responses than in multistability. This still held when data were corrected for the pupil response to the stimulus change as such. Hence, active responses to an exogeneous stimulus change trigger a stronger or temporally more confined pupil dilation than responses to an endogenous perceptual switch. In another condition, participants randomly pressed the buttons used for reporting multistability. In Study 1, this "random condition" failed to sufficiently mimic the temporal pattern of multistability. By adapting the instructions, in Study 2 we obtained a response pattern more similar to the multistable condition. In this case, the pupil dilated significantly around the random button presses. Albeit numerically smaller, this pupil response was not significantly different from the multistable condition. While there are several possible explanations-related, e.g., to the decision to respond-this underlines the difficulty to isolate a purely perceptual effect in multistability. Our data extend previous findings from visual to auditory multistability. They highlight methodological challenges in interpreting such data and suggest possible approaches to meet them, including a novel stimulus to simulate the experience of perceptual switches in auditory streaming.

Project description:To encode specific sensory inputs, cortical neurons must generate selective responses for distinct stimulus features. In principle, a variety of factors can contribute to the response selectivity of a cortical neuron: the tuning and strength of excitatory1-3 and inhibitory synaptic inputs4-6, dendritic nonlinearities7-9 and spike threshold10,11. Here we use a combination of techniques including in vivo whole-cell recording, synaptic- and cellular-resolution in vivo two-photon calcium imaging, and GABA (?-aminobutyric acid) neuron-selective optogenetic manipulation to dissect the factors that contribute to the direction-selective responses of layer 2/3 neurons in ferret visual cortex (V1). Two-photon calcium imaging of dendritic spines12,13 revealed that each neuron receives a mixture of excitatory synaptic inputs selective for the somatic preferred or null direction of motion. The relative number of preferred- and null-tuned excitatory inputs predicted a neuron's somatic direction preference, but failed to account for the degree of direction selectivity. By contrast, in vivo whole-cell patch-clamp recordings revealed a notable degree of direction selectivity in subthreshold responses that was significantly correlated with spiking direction selectivity. Subthreshold direction selectivity was predicted by the magnitude and variance of the response to the null direction of motion, and several lines of evidence, including conductance measurements, demonstrate that differential tuning of excitation and inhibition suppresses responses to the null direction of motion. Consistent with this idea, optogenetic inactivation of GABAergic neurons in layer 2/3 reduced direction selectivity by enhancing responses to the null direction. Furthermore, by optogenetically mapping connections of inhibitory neurons in layer 2/3 in vivo, we find that layer 2/3 inhibitory neurons make long-range, intercolumnar projections to excitatory neurons that prefer the opposite direction of motion. We conclude that intracortical inhibition exerts a major influence on the degree of direction selectivity in layer 2/3 of ferret V1 by suppressing responses to the null direction of motion.

Dataset Information

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

Publications

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

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