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

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.

[1]  Karl J. Friston,et al.  Attention, Uncertainty, and Free-Energy , 2010, Front. Hum. Neurosci..

[2]  Michael W. Cole,et al.  Early-Course Unmedicated Schizophrenia Patients Exhibit Elevated Prefrontal Connectivity Associated with Longitudinal Change , 2015, The Journal of Neuroscience.

[3]  G. Meredith,et al.  Effect of Instructional Conditions on Rate of Binocular Rivalry , 1962, Perceptual and motor skills.

[4]  N. Logothetis,et al.  Multistable phenomena: changing views in perception , 1999, Trends in Cognitive Sciences.

[5]  W. PEDDIE,et al.  Helmholtz's Treatise on Physiological Optics , 1926, Nature.

[6]  Wolf Singer,et al.  Interhemispheric Connections Shape Subjective Experience of Bistable Motion , 2011, Current Biology.

[7]  Lyes Kadem,et al.  Visualization of an imploding circular wave front and the formation of a central vertical jet , 2011, J. Vis..

[8]  R. Blake,et al.  Neural bases of binocular rivalry , 2006, Trends in Cognitive Sciences.

[9]  John Rinzel,et al.  Neuromechanistic Model of Auditory Bistability , 2015, PLoS Comput. Biol..

[10]  C. Clifford Binocular rivalry , 2009, Current Biology.

[11]  Israel Nelken,et al.  Auditory Streaming as an Online Classification Process with Evidence Accumulation , 2015, PloS one.

[12]  Brian C J Moore,et al.  Multistability in perception: binding sensory modalities, an overview , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  E. Yuliwati,et al.  A Review , 2019, Current Trends and Future Developments on (Bio-) Membranes.

[14]  Duje Tadin,et al.  Understanding Attentional Modulation of Binocular Rivalry: A Framework Based on Biased Competition , 2011, Front. Hum. Neurosci..

[15]  Michael A. Pitts,et al.  Right parietal brain activity precedes perceptual alternation during binocular rivalry , 2011, Human brain mapping.

[16]  Theodor Landis,et al.  Right parietal brain activity precedes perceptual alternation of bistable stimuli. , 2009, Cerebral cortex.

[17]  Geraint Rees,et al.  Variability of perceptual multistability: from brain state to individual trait , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[18]  Makio Kashino,et al.  Separability and commonality of auditory and visual bistable perception. , 2012, Cerebral cortex.

[19]  R. Edden,et al.  In vivo magnetic resonance spectroscopy of GABA: a methodological review. , 2012, Progress in nuclear magnetic resonance spectroscopy.

[20]  Sabine Windmann,et al.  Role of the Prefrontal Cortex in Attentional Control over Bistable Vision , 2006 .

[21]  G. J. Brouwer,et al.  Voluntary control and the dynamics of perceptual bi-stability , 2005, Vision Research.

[22]  W. Levelt,et al.  The ‘laws’ of binocular rivalry: 50 years of Levelt’s propositions , 2015, Vision Research.

[23]  John Rinzel,et al.  Noise and adaptation in multistable perception: noise drives when to switch, adaptation determines percept choice. , 2014, Journal of vision.

[24]  Philipp Sterzer,et al.  A neural basis for inference in perceptual ambiguity , 2007, Proceedings of the National Academy of Sciences.

[25]  J. Hupé,et al.  Bistability for audiovisual stimuli: Perceptual decision is modality specific. , 2008, Journal of vision.

[26]  T. Kochiyama,et al.  Individual differences in visual motion perception and neurotransmitter concentrations in the human brain , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  J. Rauschecker,et al.  Perceptual Organization of Tone Sequences in the Auditory Cortex of Awake Macaques , 2005, Neuron.

[28]  J. Rauschecker,et al.  The role of auditory cortex in the formation of auditory streams , 2007, Hearing Research.

[29]  G. Rees,et al.  The Neural Bases of Multistable Perception , 2022 .

[30]  E. Adelson,et al.  Phenomenal coherence of moving visual patterns , 1982, Nature.

[31]  R. van Ee,et al.  Percept-choice sequences driven by interrupted ambiguous stimuli: a low-level neural model. , 2007, Journal of vision.

[32]  Susan L. Denham,et al.  Computational Models of Auditory Scene Analysis: A Review , 2016, Front. Neurosci..

[33]  K. Fujii,et al.  Visualization for the analysis of fluid motion , 2005, J. Vis..

[34]  Theodoros N. Arvanitis,et al.  A constrained least‐squares approach to the automated quantitation of in vivo 1H magnetic resonance spectroscopy data , 2011, Magnetic resonance in medicine.

[35]  Rainer Goebel,et al.  Activity patterns in human motion-sensitive areas depend on the interpretation of global motion , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[36]  P. Christiaan Klink,et al.  General Validity of Levelt's Propositions Reveals Common Computational Mechanisms for Visual Rivalry , 2008, PloS one.

[37]  Karl J. Friston,et al.  Canonical Microcircuits for Predictive Coding , 2012, Neuron.

[38]  M. Lankheet,et al.  Unraveling adaptation and mutual inhibition in perceptual rivalry. , 2006, Journal of vision.

[39]  E. Finn,et al.  Ketamine-Induced Hallucinations , 2015, Psychopathology.

[40]  Sue L. Denham,et al.  Modelling the Emergence and Dynamics of Perceptual Organisation in Auditory Streaming , 2013, PLoS Comput. Biol..

[41]  M. Garwood,et al.  Simultaneous in vivo spectral editing and water suppression , 1998, NMR in biomedicine.

[42]  Mitchell Steinschneider,et al.  Neural correlates of auditory stream segregation in primary auditory cortex of the awake monkey , 2001, Hearing Research.

[43]  G. Rees,et al.  Neural correlates of perceptual rivalry in the human brain. , 1998, Science.

[44]  Caleb F. Davis,et al.  Genetic Disruption of Cortical Interneuron Development Causes Region- and GABA Cell Type-Specific Deficits, Epilepsy, and Behavioral Dysfunction , 2003, The Journal of Neuroscience.

[45]  Katsumi Aoki,et al.  Recent development of flow visualization , 2004, J. Vis..

[46]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[47]  Tomas Knapen,et al.  GABA Shapes the Dynamics of Bistable Perception , 2013, Current Biology.

[48]  Chris L. E. Paffen,et al.  Attentional Modulation of Binocular Rivalry , 2011, Front. Hum. Neurosci..

[49]  R. Blake,et al.  Negligible fronto-parietal BOLD activity accompanying unreportable switches in bistable perception , 2015, Nature Neuroscience.

[50]  J. Rinzel,et al.  Noise-induced alternations in an attractor network model of perceptual bistability. , 2007, Journal of neurophysiology.

[51]  Makio Kashino,et al.  Functional brain networks underlying perceptual switching: auditory streaming and verbal transformations , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[52]  Tomohisa Asai,et al.  Auditory multistability and neurotransmitter concentrations in the human brain , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[53]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[54]  I. Winkler,et al.  The role of predictive models in the formation of auditory streams , 2006, Journal of Physiology-Paris.

[55]  Ying Ding,et al.  Altered Glutamate Protein Co-Expression Network Topology Linked to Spine Loss in the Auditory Cortex of Schizophrenia , 2015, Biological Psychiatry.

[56]  Rhodri Cusack,et al.  The Intraparietal Sulcus and Perceptual Organization , 2005, Journal of Cognitive Neuroscience.

[57]  Raymond J. Dolan,et al.  Precision and neuronal dynamics in the human posterior parietal cortex during evidence accumulation , 2015, NeuroImage.

[58]  J. Lisman Excitation, inhibition, local oscillations, or large-scale loops: what causes the symptoms of schizophrenia? , 2012, Current Opinion in Neurobiology.

[59]  Makio Kashino,et al.  Involvement of the Thalamocortical Loop in the Spontaneous Switching of Percepts in Auditory Streaming , 2009, The Journal of Neuroscience.

[60]  L. T. Troland Helmholtz's Treatise on Physiological Optics , 1926 .

[61]  D G Pelli,et al.  Pixel independence: measuring spatial interactions on a CRT display. , 1997, Spatial vision.

[62]  J. Hupé,et al.  Temporal Dynamics of Auditory and Visual Bistability Reveal Common Principles of Perceptual Organization , 2006, Current Biology.

[63]  Geraint Rees,et al.  Energy landscape and dynamics of brain activity during human bistable perception , 2014, Nature Communications.

[64]  Rainer Goebel,et al.  On the functional relevance of frontal cortex for passive and voluntarily controlled bistable vision. , 2011, Cerebral cortex.

[65]  F. Tong,et al.  Can attention selectively bias bistable perception? Differences between binocular rivalry and ambiguous figures. , 2004, Journal of vision.

[66]  Karl J. Friston,et al.  Cerebral hierarchies: predictive processing, precision and the pulvinar , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[67]  Karl J. Friston,et al.  Predictive coding under the free-energy principle , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[68]  J. Kawahara,et al.  Differential Contributions of GABA Concentration in Frontal and Parietal Regions to Individual Differences in Attentional Blink , 2016, The Journal of Neuroscience.

[69]  David J. Heeger,et al.  Pattern-motion responses in human visual cortex , 2002, Nature Neuroscience.

[70]  C. Schroeder,et al.  Role of cortical N-methyl-D-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[71]  J. Hohwy The Predictive Mind , 2013 .

[72]  N. Logothetis What we can do and what we cannot do with fMRI , 2008, Nature.

[73]  Takashi Hanakawa,et al.  Dissociable Neural Activations of Conscious Visibility and Attention , 2012, Journal of Cognitive Neuroscience.

[74]  Hugh R Wilson,et al.  Computational evidence for a rivalry hierarchy in vision , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[75]  C. Lüscher,et al.  Epilepsy, Hyperalgesia, Impaired Memory, and Loss of Pre- and Postsynaptic GABAB Responses in Mice Lacking GABAB(1) , 2001, Neuron.

[76]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .

[77]  Nava Rubin,et al.  The dynamics of bi-stable alternation in ambiguous motion displays: a fresh look at plaids , 2003, Vision Research.