Associative learning changes cross-modal representations in the gustatory cortex

A growing body of literature has demonstrated that primary sensory cortices are not exclusively unimodal, but can respond to stimuli of different sensory modalities. However, several questions concerning the neural representation of cross-modal stimuli remain open. Indeed, it is poorly understood if cross-modal stimuli evoke unique or overlapping representations in a primary sensory cortex and whether learning can modulate these representations. Here we recorded single unit responses to auditory, visual, somatosensory, and olfactory stimuli in the gustatory cortex (GC) of alert rats before and after associative learning. We found that, in untrained rats, the majority of GC neurons were modulated by a single modality. Upon learning, both prevalence of cross-modal responsive neurons and their breadth of tuning increased, leading to a greater overlap of representations. Altogether, our results show that the gustatory cortex represents cross-modal stimuli according to their sensory identity, and that learning changes the overlap of cross-modal representations. DOI: http://dx.doi.org/10.7554/eLife.16420.001

[1]  Matthew P. H. Gardner,et al.  Thalamic Contribution to Cortical Processing of Taste and Expectation , 2013, The Journal of Neuroscience.

[2]  G. H. Jacobs Evolution of colour vision in mammals , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[3]  C. Schroeder,et al.  Neuronal Oscillations and Multisensory Interaction in Primary Auditory Cortex , 2007, Neuron.

[4]  M. Nicolelis,et al.  Dynamic and Multimodal Responses of Gustatory Cortical Neurons in Awake Rats , 2001, The Journal of Neuroscience.

[5]  Lourens J P Nonkes,et al.  Serotonin transporter knockout rats show improved strategy set-shifting and reduced latent inhibition. , 2012, Learning & memory.

[6]  Donald B Katz,et al.  Control of Prestimulus Activity Related to Improved Sensory Coding within a Discrimination Task , 2011, The Journal of Neuroscience.

[7]  Drew B Headley,et al.  Relational associative learning induces cross-modal plasticity in early visual cortex. , 2015, Cerebral cortex.

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

[9]  Miguel A. L. Nicolelis,et al.  The neural mechanisms of gustation: a distributed processing code , 2006, Nature Reviews Neuroscience.

[10]  M. Nicolelis,et al.  Gustatory processing is dynamic and distributed , 2002, Current Opinion in Neurobiology.

[11]  Herman Martins Gomes,et al.  Cross-modal responses in the primary visual cortex encode complex objects and correlate with tactile discrimination , 2011, Proceedings of the National Academy of Sciences.

[12]  Masataka Watanabe Frontal units of the monkey coding the associative significance of visual and auditory stimuli , 2004, Experimental Brain Research.

[13]  N. Yuyama,et al.  Cortical neurons responding to tactile, thermal and taste stimulations of the rat's tongue , 1981, Brain Research.

[14]  Giuliano Iurilli,et al.  Cellular and Synaptic Architecture of Multisensory Integration in the Mouse Neocortex , 2013, Neuron.

[15]  El-Mehdi Meftah,et al.  Effects of a cross-modal manipulation of attention on somatosensory cortical neuronal responses to tactile stimuli in the monkey. , 2002, Journal of neurophysiology.

[16]  J. White,et al.  Sniffing controls an adaptive filter of sensory input to the olfactory bulb , 2007, Nature Neuroscience.

[17]  Edmund T Rolls,et al.  Representation in the Human Brain of Food Texture and Oral Fat , 2004, The Journal of Neuroscience.

[18]  B. Stein,et al.  Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. , 1986, Journal of neurophysiology.

[19]  Joost X. Maier,et al.  Multisensory Integration of Dynamic Faces and Voices in Rhesus Monkey Auditory Cortex , 2005 .

[20]  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.

[21]  Paul Miller,et al.  Natural stimuli evoke dynamic sequences of states in sensory cortical ensembles , 2007, Proceedings of the National Academy of Sciences.

[22]  D. Katz,et al.  Distinct Subtypes of Basolateral Amygdala Taste Neurons Reflect Palatability and Reward , 2009, The Journal of Neuroscience.

[23]  Ulf Toelch,et al.  Cross-modal effects of value on perceptual acuity and stimulus encoding , 2014, Proceedings of the National Academy of Sciences.

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

[25]  Ankoor S. Shah,et al.  Auditory Cortical Neurons Respond to Somatosensory Stimulation , 2003, The Journal of Neuroscience.

[26]  G. La Camera,et al.  Dynamics of Multistable States during Ongoing and Evoked Cortical Activity , 2015, The Journal of Neuroscience.

[27]  A. Grinvald,et al.  Imaging Spatiotemporal Dynamics of Surround Inhibition in the Barrels Somatosensory Cortex , 2003, The Journal of Neuroscience.

[28]  A. Carleton,et al.  Coding in the mammalian gustatory system , 2010, Trends in Neurosciences.

[29]  N. Weinberger Associative representational plasticity in the auditory cortex: a synthesis of two disciplines. , 2007, Learning & memory.

[30]  C. Gallistel,et al.  The learning curve: implications of a quantitative analysis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[31]  A. Fontanini,et al.  State Dependency of Chemosensory Coding in the Gustatory Thalamus (VPMpc) of Alert Rats , 2015, The Journal of Neuroscience.

[32]  Dora E Angelaki,et al.  Dissecting neural circuits for multisensory integration and crossmodal processing , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[33]  Shree Hari Gautam,et al.  Retronasal Odor Representations in the Dorsal Olfactory Bulb of Rats , 2012, The Journal of Neuroscience.

[34]  Joost X. Maier,et al.  A Multisensory Network for Olfactory Processing , 2015, Current Biology.

[35]  T. Yamamoto,et al.  Taste responses of cortical neurons in freely ingesting rats. , 1989, Journal of neurophysiology.

[36]  H. Markowitsch,et al.  Cortical and thalamic afferent connections of the insular and adjacent cortex of the rat , 1983, The Journal of comparative neurology.

[37]  Diego Contreras,et al.  Integration of evoked responses in supragranular cortex studied with optical recordings in vivo. , 2006, Journal of neurophysiology.

[38]  Matthew P. H. Gardner,et al.  Encoding and Tracking of Outcome-Specific Expectancy in the Gustatory Cortex of Alert Rats , 2014, The Journal of Neuroscience.

[39]  S. Simon,et al.  The gustatory cortex and multisensory integration , 2009, International Journal of Obesity.

[40]  H. Eichenbaum,et al.  Crossmodal Associative Memory Representations in Rodent Orbitofrontal Cortex , 1999, Neuron.

[41]  James K. Kroger,et al.  Cross-modal and cross-temporal association in neurons of frontal cortex , 2000, Nature.

[42]  C. Schroeder,et al.  Somatosensory input to auditory association cortex in the macaque monkey. , 2001, Journal of neurophysiology.

[43]  A. Ghazanfar,et al.  Is neocortex essentially multisensory? , 2006, Trends in Cognitive Sciences.

[44]  Mark F Bear,et al.  Reward timing in the primary visual cortex. , 2006, Science.

[45]  D. Katz,et al.  Learning-Related Plasticity of Temporal Coding in Simultaneously Recorded Amygdala–Cortical Ensembles , 2008, The Journal of Neuroscience.

[46]  M. Kilgard,et al.  Cortical speech-evoked response patterns in multiple auditory fields are correlated with behavioral discrimination ability. , 2013, Journal of neurophysiology.

[47]  T. Yamamoto,et al.  Sensory inputs from the oral region to the cerebral cortex in behaving rats: an analysis of unit responses in cortical somatosensory and taste areas during ingestive behavior. , 1988, Journal of neurophysiology.

[48]  D. Senkowski,et al.  The multifaceted interplay between attention and multisensory integration , 2010, Trends in Cognitive Sciences.

[49]  D. Gitelman,et al.  Human Neuroscience , 2022 .

[50]  Matthew P. H. Gardner,et al.  Effects of Cue-Triggered Expectation on Cortical Processing of Taste , 2012, Neuron.

[51]  W. Freeman The physiological basis of mental images. , 1983, Biological psychiatry.

[52]  Christoph Kayser,et al.  Functional Imaging Reveals Visual Modulation of Specific Fields in Auditory Cortex , 2007, The Journal of Neuroscience.

[53]  Earl K. Miller,et al.  Selective representation of relevant information by neurons in the primate prefrontal cortex , 1998, Nature.

[54]  Matt Wachowiak,et al.  Why sniff fast? The relationship between sniff frequency, odor discrimination, and receptor neuron activation in the rat. , 2009, Journal of neurophysiology.

[55]  A. Zador,et al.  Selective corticostriatal plasticity during acquisition of an auditory discrimination task , 2014, Nature.

[56]  Heydar Davoudi,et al.  Selective Activation of a Putative Reinforcement Signal Conditions Cued Interval Timing in Primary Visual Cortex , 2015, Current Biology.

[57]  Henning Sprekeler,et al.  Inhibitory Plasticity Balances Excitation and Inhibition in Sensory Pathways and Memory Networks , 2011, Science.

[58]  T. Stanford,et al.  What does a neuron learn from multisensory experience? , 2015, Journal of neurophysiology.

[59]  G. La Camera,et al.  Processing of Hedonic and Chemosensory Features of Taste in Medial Prefrontal and Insular Networks , 2013, The Journal of Neuroscience.

[60]  Dylan C. Barnes,et al.  Generalized vs. stimulus-specific learned fear differentially modifies stimulus encoding in primary sensory cortex of awake rats. , 2011, Journal of neurophysiology.

[61]  Alexander M. Benison,et al.  Auditory, somatosensory, and multisensory insular cortex in the rat. , 2008, Cerebral cortex.

[62]  H Eichenbaum,et al.  Information coding in the rodent prefrontal cortex. I. Single-neuron activity in orbitofrontal cortex compared with that in pyriform cortex. , 1995, Journal of neurophysiology.

[63]  H. Nagata,et al.  The merging of the senses: integration of subthreshold taste and smell , 2000, Nature Neuroscience.

[64]  T. Stanford,et al.  Development of multisensory integration from the perspective of the individual neuron , 2014, Nature Reviews Neuroscience.

[65]  Donald A Wilson,et al.  Olfactory perceptual stability and discrimination , 2008, Nature Neuroscience.

[66]  A. Bonci,et al.  Central role for the insular cortex in mediating conditioned responses to anticipatory cues , 2015, Proceedings of the National Academy of Sciences.

[67]  J. Fuster,et al.  Visuo-tactile cross-modal associations in cortical somatosensory cells. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[68]  Brian Zingg,et al.  Cross-Modality Sharpening of Visual Cortical Processing through Layer-1-Mediated Inhibition and Disinhibition , 2016, Neuron.

[69]  J. O'Doherty,et al.  Appetitive and Aversive Olfactory Learning in Humans Studied Using Event-Related Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[70]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[71]  Benjamin A Rowland,et al.  Initiating the Development of Multisensory Integration by Manipulating Sensory Experience , 2010, The Journal of Neuroscience.

[72]  Daniel C Millard,et al.  Detection of tactile inputs in the rat vibrissa pathway. , 2012, Journal of neurophysiology.

[73]  Anne E Carpenter,et al.  Neuron-type specific signals for reward and punishment in the ventral tegmental area , 2011, Nature.

[74]  H. Markowitsch,et al.  Cortical and thalamic afferent connections of the insular and adjacent cortex of the cat , 1983, The Journal of comparative neurology.

[75]  B E Stein,et al.  Unimodal and multimodal response properties of neurons in the cat's superior colliculus. , 1972, Experimental neurology.

[76]  Christoph Kayser,et al.  Do early sensory cortices integrate cross-modal information? , 2007, Brain Structure and Function.

[77]  M. T. Shipley,et al.  Anatomical evidence for convergence of olfactory, gustatory, and visceral afferent pathways in mouse cerebral cortex , 1984, Brain Research Bulletin.

[78]  C. Spence Multisensory Flavor Perception , 2015, Cell.

[79]  J. Victor,et al.  Odor-Taste Convergence in the Nucleus of the Solitary Tract of the Awake Freely Licking Rat , 2015, The Journal of Neuroscience.

[80]  J. Driver,et al.  Multisensory Interplay Reveals Crossmodal Influences on ‘Sensory-Specific’ Brain Regions, Neural Responses, and Judgments , 2008, Neuron.

[81]  Joost X. Maier,et al.  Chemosensory Convergence on Primary Olfactory Cortex , 2012, The Journal of Neuroscience.

[82]  B. Sakmann,et al.  ‐Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex , 2002, The Journal of physiology.

[83]  E. Bullmore,et al.  Activation of auditory cortex during silent lipreading. , 1997, Science.

[84]  Donald A. Wilson,et al.  Smelling Sounds: Olfactory–Auditory Sensory Convergence in the Olfactory Tubercle , 2010, The Journal of Neuroscience.

[85]  S. Devore,et al.  Odor preferences shape discrimination learning in rats. , 2013, Behavioral neuroscience.