Spectral hallmark of auditory-tactile interactions in the mouse somatosensory cortex

To synthesize a coherent representation of the external world, the brain must integrate inputs across different types of stimuli. Yet the mechanistic basis of this computation at the level of neuronal populations remains obscure. Here, we investigate tactile-auditory integration using two-photon Ca 2+ imaging in the mouse primary (S1) and secondary (S2) somatosensory cortices. Pairing sound with whisker stimulation modulates tactile responses in both S1 and S2, with the most prominent modulation being robust inhibition in S2. The degree of inhibition depends on tactile stimulation frequency, with lower frequency responses the most severely attenuated. Alongside these neurons, we identify sound-selective neurons in S2 whose responses are inhibited by high tactile frequencies. These results are consistent with a hypothesized local mutually-inhibitory S2 circuit that spectrally selects tactile versus auditory inputs. Our findings enrich mechanistic understanding of multisensory integration and suggest a key role for S2 in combining auditory and tactile information. Manning Zhang et al. investigate how the mouse brain makes sense of multiple sensory types, such as sound and touch using two-photon Ca 2+ imaging in the somatosensory cortex while exposing the mouse to sound and whisker simulation. They identify a potential mutually-inhibitory circuit between sound and touch that depends on the relative frequencies of the different stimuli.

[1]  Kenneth D. Harris,et al.  Effects of Arousal on Mouse Sensory Cortex Depend on Modality , 2018, Cell reports.

[2]  Lin Tian,et al.  Activity in motor-sensory projections reveals distributed coding in somatosensation , 2012, Nature.

[3]  J. Dörfl The innervation of the mystacial region of the white mouse: A topographical study. , 1985, Journal of anatomy.

[4]  F. Ebner,et al.  Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus , 1992, The Journal of comparative neurology.

[5]  John J. Foxe,et al.  Auditory-somatosensory multisensory processing in auditory association cortex: an fMRI study. , 2002, Journal of neurophysiology.

[6]  E. Ahissar,et al.  Muscle Architecture in the Mystacial Pad of the Rat , 2010, Anatomical record.

[7]  Manuel Guizar-Sicairos,et al.  Efficient subpixel image registration algorithms. , 2008, Optics letters.

[8]  Brenda C. Shields,et al.  Thy1-GCaMP6 Transgenic Mice for Neuronal Population Imaging In Vivo , 2014, PloS one.

[9]  John J. Foxe,et al.  The case for feedforward multisensory convergence during early cortical processing , 2005, Neuroreport.

[10]  A. Brombas,et al.  Activity-Dependent Modulation of Layer 1 Inhibitory Neocortical Circuits by Acetylcholine , 2014, The Journal of Neuroscience.

[11]  Robert A Jacobs,et al.  Bayesian integration of visual and auditory signals for spatial localization. , 2003, Journal of the Optical Society of America. A, Optics, image science, and vision.

[12]  Rogelio Luna,et al.  Do Sensory Cortices Process More than One Sensory Modality during Perceptual Judgments? , 2010, Neuron.

[13]  Benjamin D. Haeffele,et al.  Multiscale mapping of frequency sweep rate in mouse auditory cortex , 2017, Hearing Research.

[14]  Yong-Di Zhou,et al.  Somatosensory cell response to an auditory cue in a haptic memory task , 2004, Behavioural Brain Research.

[15]  Stefan R. Pulver,et al.  Ultra-sensitive fluorescent proteins for imaging neuronal activity , 2013, Nature.

[16]  J. F. Dammann,et al.  Temporal Frequency Channels Are Linked across Audition and Touch , 2009, Current Biology.

[17]  G. Fishell,et al.  A disinhibitory circuit mediates motor integration in the somatosensory cortex , 2013, Nature Neuroscience.

[18]  S. Lederman Auditory Texture Perception , 1979, Perception.

[19]  Conor Liston,et al.  Projections from neocortex mediate top-down control of memory retrieval , 2015, Nature.

[20]  J. Marth,et al.  Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. , 2001, Genes & development.

[21]  S. E. Kwon,et al.  Sensory and decision-related activity propagate in a cortical feedback loop during touch perception , 2016, Nature Neuroscience.

[22]  M. Andermann,et al.  Embodied Information Processing: Vibrissa Mechanics and Texture Features Shape Micromotions in Actively Sensing Rats , 2008, Neuron.

[23]  Denise M. Piscopo,et al.  Large-scale imaging of cortical dynamics during sensory perception and behavior. , 2016, Journal of neurophysiology.

[24]  Takao K. Hensch,et al.  Sensory Integration in Mouse Insular Cortex Reflects GABA Circuit Maturation , 2014, Neuron.

[25]  K. Svoboda,et al.  A Cellular Resolution Map of Barrel Cortex Activity during Tactile Behavior , 2015, Neuron.

[26]  Giuliano Iurilli,et al.  Sound-Driven Synaptic Inhibition in Primary Visual Cortex , 2012, Neuron.

[27]  D. Feldmeyer Excitatory neuronal connectivity in the barrel cortex , 2012, Front. Neuroanat..

[28]  T. Stanford,et al.  Evaluating the Operations Underlying Multisensory Integration in the Cat Superior Colliculus , 2005, The Journal of Neuroscience.

[29]  Cullen B. Owens,et al.  Anatomical Pathways Involved in Generating and Sensing Rhythmic Whisker Movements , 2011, Front. Integr. Neurosci..

[30]  G. DeAngelis,et al.  A Neural Signature of Divisive Normalization at the Level of Multisensory Integration in Primate Cortex , 2017, Neuron.

[31]  Barry E Stein,et al.  Neuron-specific response characteristics predict the magnitude of multisensory integration. , 2003, Journal of neurophysiology.

[32]  T. Harkany,et al.  Pyramidal cell communication within local networks in layer 2/3 of rat neocortex , 2003, The Journal of physiology.

[33]  H. Scheich,et al.  Nonauditory Events of a Behavioral Procedure Activate Auditory Cortex of Highly Trained Monkeys , 2005, The Journal of Neuroscience.

[34]  G. von Békésy,et al.  Similarities between hearing and skin sensations. , 1959, Psychological review.

[35]  N. Logothetis,et al.  Integration of Touch and Sound in Auditory Cortex , 2005, Neuron.

[36]  M. Stryker,et al.  Modulation of Visual Responses by Behavioral State in Mouse Visual Cortex , 2010, Neuron.

[37]  Kenneth O. Johnson,et al.  The roles and functions of cutaneous mechanoreceptors , 2001, Current Opinion in Neurobiology.

[38]  T. Stanford,et al.  Multisensory integration: current issues from the perspective of the single neuron , 2008, Nature Reviews Neuroscience.

[39]  H. Scheich,et al.  Multisensory processing via early cortical stages: Connections of the primary auditory cortical field with other sensory systems , 2006, Neuroscience.

[40]  Alexander S. Ecker,et al.  Population code in mouse V1 facilitates read-out of natural scenes through increased sparseness , 2014, Nature Neuroscience.

[41]  D. Simons,et al.  Biometric analyses of vibrissal tactile discrimination in the rat , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  Makoto Takemoto,et al.  Identification and characterization of an insular auditory field in mice , 2011, The European journal of neuroscience.

[43]  Rafael Yuste,et al.  Fast nonnegative deconvolution for spike train inference from population calcium imaging. , 2009, Journal of neurophysiology.

[44]  D. McCormick,et al.  Waking State: Rapid Variations Modulate Neural and Behavioral Responses , 2015, Neuron.

[45]  M. Carandini,et al.  Normalization as a canonical neural computation , 2011, Nature Reviews Neuroscience.

[46]  Christopher R Fetsch,et al.  Dynamic Reweighting of Visual and Vestibular Cues during Self-Motion Perception , 2009, The Journal of Neuroscience.

[47]  Nathan C. Klapoetke,et al.  Transgenic Mice for Intersectional Targeting of Neural Sensors and Effectors with High Specificity and Performance , 2015, Neuron.

[48]  B. Haeffele,et al.  Multiscale Optical Ca2+ Imaging of Tonal Organization in Mouse Auditory Cortex , 2014, Neuron.

[49]  David J. Freedman,et al.  A hierarchy of intrinsic timescales across primate cortex , 2014, Nature Neuroscience.

[50]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

[51]  Hongkui Zeng,et al.  Differential tuning and population dynamics of excitatory and inhibitory neurons reflect differences in local intracortical connectivity , 2011, Nature Neuroscience.

[52]  A. Hasenstaub,et al.  Visual Information Present in Infragranular Layers of Mouse Auditory Cortex , 2018, The Journal of Neuroscience.

[53]  J. Muthuswamy,et al.  Artificial dural sealant that allows multiple penetrations of implantable brain probes , 2008, Journal of Neuroscience Methods.

[54]  D. Simons,et al.  Somatotopic organization of the second somatosensory area (SII) in the cerebral cortex of the mouse. , 1986, Somatosensory research.

[55]  C. Frith,et al.  Modulation of human visual cortex by crossmodal spatial attention. , 2000, Science.

[56]  Hannes P. Saal,et al.  Natural scenes in tactile texture. , 2014, Journal of neurophysiology.

[57]  V. Jousmäki,et al.  Parchment-skin illusion: sound-biased touch , 1998, Current Biology.

[58]  Per Magne Knutsen,et al.  Haptic Object Localization in the Vibrissal System: Behavior and Performance , 2006, The Journal of Neuroscience.

[59]  Lexi E. Crommett,et al.  Auditory adaptation improves tactile frequency perception. , 2017, Journal of neurophysiology.

[60]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[61]  P. J. Sjöström,et al.  Functional specificity of local synaptic connections in neocortical networks , 2011, Nature.

[62]  M. Nicolelis,et al.  Behavioral Properties of the Trigeminal Somatosensory System in Rats Performing Whisker-Dependent Tactile Discriminations , 2001, The Journal of Neuroscience.

[63]  R. Reid,et al.  Local Diversity and Fine-Scale Organization of Receptive Fields in Mouse Visual Cortex , 2011, The Journal of Neuroscience.

[64]  M. Wallace,et al.  A revised view of sensory cortical parcellation , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[65]  G. DeAngelis,et al.  A Normalization Model of Multisensory Integration , 2011, Nature Neuroscience.

[66]  Erik Seedhouse,et al.  Behavior and performance , 2011 .

[67]  René Vidal,et al.  Structured Low-Rank Matrix Factorization: Optimality, Algorithm, and Applications to Image Processing , 2014, ICML.

[68]  D. Burr,et al.  The Ventriloquist Effect Results from Near-Optimal Bimodal Integration , 2004, Current Biology.

[69]  M. Giard,et al.  Auditory-Visual Integration during Multimodal Object Recognition in Humans: A Behavioral and Electrophysiological Study , 1999, Journal of Cognitive Neuroscience.

[70]  Martin Vinck,et al.  Arousal and Locomotion Make Distinct Contributions to Cortical Activity Patterns and Visual Encoding , 2014, Neuron.