Sweet and bitter taste in the brain of awake behaving animals
Activation of the sweet and bitter cortical fields in awake mice evokes predetermined behavioural programs, independent of learning and experience, illustrating the hardwired and innate nature of the sense of taste. Dissecting the sense of taste In mammals, information from taste receptor cells in t...
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Published in | Nature (London) Vol. 527; no. 7579; pp. 512 - 515 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
26.11.2015
Nature Publishing Group |
Subjects | |
Online Access | Get full text |
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Abstract | Activation of the sweet and bitter cortical fields in awake mice evokes predetermined behavioural programs, independent of learning and experience, illustrating the hardwired and innate nature of the sense of taste.
Dissecting the sense of taste
In mammals, information from taste receptor cells in the tongue is transmitted through multiple neural stations to the primary gustatory cortex in the brain. Previous studies indicated that bitter taste and sweet taste are represented in separate fields within the rodent gustatory cortex. Charles Zuker and colleagues directly manipulate the activity of these distinct cortical taste fields in awake mice to control the animals' internal representation, sensory perception, and behavioral actions, demonstrating that taste fields can control appetitive and aversive responses independent of learning and experience. This finding illustrates the hardwired and innate nature of the sense of taste.
Taste is responsible for evaluating the nutritious content of food, guiding essential appetitive behaviours, preventing the ingestion of toxic substances, and helping to ensure the maintenance of a healthy diet. Sweet and bitter are two of the most salient sensory percepts for humans and other animals; sweet taste allows the identification of energy-rich nutrients whereas bitter warns against the intake of potentially noxious chemicals
1
. In mammals, information from taste receptor cells in the tongue is transmitted through multiple neural stations to the primary gustatory cortex in the brain
2
. Recent imaging studies have shown that sweet and bitter are represented in the primary gustatory cortex by neurons organized in a spatial map
3
,
4
, with each taste quality encoded by distinct cortical fields
4
. Here we demonstrate that by manipulating the brain fields representing sweet and bitter taste we directly control an animal’s internal representation, sensory perception, and behavioural actions. These results substantiate the segregation of taste qualities in the cortex, expose the innate nature of appetitive and aversive taste responses, and illustrate the ability of gustatory cortex to recapitulate complex behaviours in the absence of sensory input. |
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AbstractList | Taste is responsible for evaluating the nutritious content of food, guiding essential appetitive behaviours, preventing the ingestion of toxic substances, and helping to ensure the maintenance of a healthy diet. Sweet and bitter are two of the most salient sensory percepts for humans and other animals; sweet taste allows the identification of energy-rich nutrients whereas bitter warns against the intake of potentially noxious chemicals. In mammals, information from taste receptor cells in the tongue is transmitted through multiple neural stations to the primary gustatory cortex in the brain. Recent imaging studies have shown that sweet and bitter are represented in the primary gustatory cortex by neurons organized in a spatial map, with each taste quality encoded by distinct cortical fields. Here we demonstrate that by manipulating the brain fields representing sweet and bitter taste we directly control an animal's internal representation, sensory perception, and behavioural actions. These results substantiate the segregation of taste qualities in the cortex, expose the innate nature of appetitive and aversive taste responses, and illustrate the ability of gustatory cortex to recapitulate complex behaviours in the absence of sensory input. Taste is responsible for evaluating the nutritious content of food, guiding essential appetitive behaviors, preventing the ingestion of toxic substances, and helping ensure the maintenance of a healthy diet. Sweet and bitter are two of the most salient sensory percepts for humans and other animals; sweet taste permits the identification of energy-rich nutrients while bitter warns against the intake of potentially noxious chemicals 1 . In mammals, information from taste receptor cells in the tongue is transmitted through multiple neural stations to the primary gustatory cortex in the brain 2 . Recent imaging studies have shown that sweet and bitter are represented in the primary gustatory cortex by neurons organized in a spatial map 3 , 4 , with each taste quality encoded by distinct cortical fields 4 . Here we demonstrate that by manipulating the brain fields representing sweet and bitter taste we directly control an animal’s internal representation, sensory perception, and behavioral actions. These results substantiate the segregation of taste qualities in the cortex, expose the innate nature of appetitive and aversive taste responses, and illustrate the ability of gustatory cortex to recapitulate complex behaviors in the absence of sensory input. Taste is responsible for evaluating the nutritious content of food, guiding essential appetitive behaviours, preventing the ingestion of toxic substances, and helping to ensure the maintenance of a healthy diet. Sweet and bitter are two of the most salient sensory percepts for humans and other animals; sweet taste allows the identification of energy-rich nutrients whereas bitter warns against the intake of potentially noxious chemicals1. In mammals, information from taste receptor cells in the tongue is transmitted through multiple neural stations to the primary gustatory cortex in the brain2. Recent imaging studies have shown that sweet and bitter are represented in the primary gustatory cortex by neurons organized in a spatial map3,4, with each taste quality encoded by distinct cortical fields4. Here we demonstrate that by manipulating the brain fields representing sweet and bitter taste we directly control an animal's internal representation, sensory perception, and behavioural actions. These results substantiate the segregation of taste qualities in the cortex, expose the innate nature of appetitive and aversive taste responses, and illustrate the ability of gustatory cortex to recapitulate complex behaviours in the absence of sensory input. Activation of the sweet and bitter cortical fields in awake mice evokes predetermined behavioural programs, independent of learning and experience, illustrating the hardwired and innate nature of the sense of taste. Dissecting the sense of taste In mammals, information from taste receptor cells in the tongue is transmitted through multiple neural stations to the primary gustatory cortex in the brain. Previous studies indicated that bitter taste and sweet taste are represented in separate fields within the rodent gustatory cortex. Charles Zuker and colleagues directly manipulate the activity of these distinct cortical taste fields in awake mice to control the animals' internal representation, sensory perception, and behavioral actions, demonstrating that taste fields can control appetitive and aversive responses independent of learning and experience. This finding illustrates the hardwired and innate nature of the sense of taste. Taste is responsible for evaluating the nutritious content of food, guiding essential appetitive behaviours, preventing the ingestion of toxic substances, and helping to ensure the maintenance of a healthy diet. Sweet and bitter are two of the most salient sensory percepts for humans and other animals; sweet taste allows the identification of energy-rich nutrients whereas bitter warns against the intake of potentially noxious chemicals 1 . In mammals, information from taste receptor cells in the tongue is transmitted through multiple neural stations to the primary gustatory cortex in the brain 2 . Recent imaging studies have shown that sweet and bitter are represented in the primary gustatory cortex by neurons organized in a spatial map 3 , 4 , with each taste quality encoded by distinct cortical fields 4 . Here we demonstrate that by manipulating the brain fields representing sweet and bitter taste we directly control an animal’s internal representation, sensory perception, and behavioural actions. These results substantiate the segregation of taste qualities in the cortex, expose the innate nature of appetitive and aversive taste responses, and illustrate the ability of gustatory cortex to recapitulate complex behaviours in the absence of sensory input. |
Audience | Academic |
Author | Peng, Yueqing Tränkner, Dimitri Ryba, Nicholas J. P. Jin, Hao Zuker, Charles S. Gillis-Smith, Sarah |
AuthorAffiliation | 2 HHMI/Janelia Farm Research Campus, 19700 Helix Drive, Ashburn, VA 20147, USA 1 Howard Hughes Medical Institute and Departments of Biochemistry and Molecular Biophysics and of Neuroscience, Columbia College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA 3 National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, MD 20892, USA |
AuthorAffiliation_xml | – name: 3 National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, MD 20892, USA – name: 1 Howard Hughes Medical Institute and Departments of Biochemistry and Molecular Biophysics and of Neuroscience, Columbia College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA – name: 2 HHMI/Janelia Farm Research Campus, 19700 Helix Drive, Ashburn, VA 20147, USA |
Author_xml | – sequence: 1 givenname: Yueqing surname: Peng fullname: Peng, Yueqing organization: Howard Hughes Medical Institute, Columbia College of Physicians and Surgeons, Columbia University, Departments of Biochemistry and Molecular Biophysics, Columbia College of Physicians and Surgeons, Columbia University, Department of Neuroscience, Columbia College of Physicians and Surgeons, Columbia University – sequence: 2 givenname: Sarah surname: Gillis-Smith fullname: Gillis-Smith, Sarah organization: Howard Hughes Medical Institute, Columbia College of Physicians and Surgeons, Columbia University, Departments of Biochemistry and Molecular Biophysics, Columbia College of Physicians and Surgeons, Columbia University, Department of Neuroscience, Columbia College of Physicians and Surgeons, Columbia University – sequence: 3 givenname: Hao surname: Jin fullname: Jin, Hao organization: Howard Hughes Medical Institute, Columbia College of Physicians and Surgeons, Columbia University, Departments of Biochemistry and Molecular Biophysics, Columbia College of Physicians and Surgeons, Columbia University, Department of Neuroscience, Columbia College of Physicians and Surgeons, Columbia University – sequence: 4 givenname: Dimitri surname: Tränkner fullname: Tränkner, Dimitri organization: Howard Hughes Medical Institute, Columbia College of Physicians and Surgeons, Columbia University, Departments of Biochemistry and Molecular Biophysics, Columbia College of Physicians and Surgeons, Columbia University, Department of Neuroscience, Columbia College of Physicians and Surgeons, Columbia University, HHMI/Janelia Farm Research Campus – sequence: 5 givenname: Nicholas J. P. surname: Ryba fullname: Ryba, Nicholas J. P. email: nick.ryba@nih.gov organization: National Institute of Dental and Craniofacial Research, National Institutes of Health – sequence: 6 givenname: Charles S. surname: Zuker fullname: Zuker, Charles S. email: cz2195@cumc.columbia.edu organization: Howard Hughes Medical Institute, Columbia College of Physicians and Surgeons, Columbia University, Departments of Biochemistry and Molecular Biophysics, Columbia College of Physicians and Surgeons, Columbia University, Department of Neuroscience, Columbia College of Physicians and Surgeons, Columbia University, HHMI/Janelia Farm Research Campus |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26580015$$D View this record in MEDLINE/PubMed |
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References | Boyden, Zhang, Bamberg, Nagel, Deisseroth (CR5) 2005; 8 Mueller (CR18) 2005; 434 Lindemann (CR1) 2001; 413 Guo (CR8) 2014; 9 Grill, Norgren (CR9) 1978; 143 Simon, de Araujo, Gutierrez, Nicolelis (CR23) 2006; 7 Chen, Gabitto, Peng, Ryba, Zuker (CR4) 2011; 333 Atasoy, Betley, Su, Sternson (CR26) 2012; 488 Zhang (CR10) 2003; 112 Graham, Sun, Hill (CR14) 2014; 34 Nieh (CR27) 2015; 160 Calu, Roesch, Haney, Holland, Schoenbaum (CR19) 2010; 68 Reilly, Pritchard (CR12) 1996; 110 Lammel (CR6) 2012; 491 Tokita, Armstrong, John, Boughter (CR28) 2014; 8 Yamamoto (CR2) 1984; 23 Zhao (CR17) 2003; 115 Tye (CR20) 2011; 471 CR7 Li (CR15) 2002; 99 Small (CR21) 2003; 39 Nelson (CR16) 2001; 106 Gardner, Fontanini (CR13) 2014; 34 Witten (CR24) 2010; 330 Grill, Norgren (CR11) 1978; 143 Choi (CR25) 2011; 146 Accolla, Bathellier, Petersen, Carleton (CR3) 2007; 27 Spector, Travers (CR22) 2005; 4 26656255 - Nat Rev Neurosci. 2016 Jan;17(1):1 26859421 - Oral Dis. 2016 May;22(4):251-2 BFnature15763_CR7 HJ Grill (BFnature15763_CR9) 1978; 143 S Reilly (BFnature15763_CR12) 1996; 110 X Chen (BFnature15763_CR4) 2011; 333 K Tokita (BFnature15763_CR28) 2014; 8 HJ Grill (BFnature15763_CR11) 1978; 143 G Nelson (BFnature15763_CR16) 2001; 106 GQ Zhao (BFnature15763_CR17) 2003; 115 EH Nieh (BFnature15763_CR27) 2015; 160 ES Boyden (BFnature15763_CR5) 2005; 8 IB Witten (BFnature15763_CR24) 2010; 330 SA Simon (BFnature15763_CR23) 2006; 7 D Atasoy (BFnature15763_CR26) 2012; 488 Y Zhang (BFnature15763_CR10) 2003; 112 R Accolla (BFnature15763_CR3) 2007; 27 GB Choi (BFnature15763_CR25) 2011; 146 B Lindemann (BFnature15763_CR1) 2001; 413 KM Tye (BFnature15763_CR20) 2011; 471 S Lammel (BFnature15763_CR6) 2012; 491 T Yamamoto (BFnature15763_CR2) 1984; 23 AC Spector (BFnature15763_CR22) 2005; 4 MP Gardner (BFnature15763_CR13) 2014; 34 X Li (BFnature15763_CR15) 2002; 99 DM Small (BFnature15763_CR21) 2003; 39 DJ Calu (BFnature15763_CR19) 2010; 68 KL Mueller (BFnature15763_CR18) 2005; 434 ZV Guo (BFnature15763_CR8) 2014; 9 DM Graham (BFnature15763_CR14) 2014; 34 |
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Snippet | Activation of the sweet and bitter cortical fields in awake mice evokes predetermined behavioural programs, independent of learning and experience,... Taste is responsible for evaluating the nutritious content of food, guiding essential appetitive behaviours, preventing the ingestion of toxic substances, and... Taste is responsible for evaluating the nutritious content of food, guiding essential appetitive behaviors, preventing the ingestion of toxic substances, and... |
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SubjectTerms | 631/378/2626/2628 631/378/3917 Animal behavior Animal feeding behavior Animals Appetitive Behavior - physiology Appetitive Behavior - radiation effects Avoidance Learning - physiology Avoidance Learning - radiation effects Brain Mapping Cerebral Cortex - cytology Cerebral Cortex - physiology Cerebral Cortex - radiation effects Cortex (Botany) Discrimination, Psychological - physiology Humanities and Social Sciences Ingestion letter Male Mice Mice, Inbred C57BL multidisciplinary Optogenetics Science Sensory perception Stereotaxic Techniques Studies Taste Taste - physiology Taste Perception - physiology Taste Perception - radiation effects Toxic substances Wakefulness - physiology |
Title | Sweet and bitter taste in the brain of awake behaving animals |
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