Activation of Human Prefrontal Cortex to Pleasant and Aversive Taste Using Functional Near-Infrared Spectroscopy

Abstract

The aim of the study was to investigate the representation of taste in human prefrontal cortex (PFC), in particular, to compare the representation of a pleasant and an aversive taste using functional near-infrared spectroscopy (fNIRS), so as to obtain further understanding of the taste preference mechanism. The pleasant stimulus used was sweet taste (10% sucrose), and the unpleasant stimulus was sour taste (1% critic acid). Based on event-related design, the experiments were performed with 16 healthy volunteers using the OEG-16 fNIRS sensor. A general linear model was used to analyze the collected data. For the concentration change of oxygenated hemoglobin (ΔoxyHb), we found that significant deactivation was induced by sweetness and sourness in parts of the frontopolar area, orbitofrontal area and dorsolateral prefrontal cortex in bilateral hemisphere of human brain. And the right PFC showed different levels of activation between sweetness and sourness. In addition, brain activities were more sensitive to sourness than sweetness. Finally, we confirmed that the PFC was involved in sweet and sour taste processing, and fNIRS provided an alternative way for studying taste-related brain function under more natural conditions.

Share and Cite:

C. Hu, Y. Kato and Z. Luo, "Activation of Human Prefrontal Cortex to Pleasant and Aversive Taste Using Functional Near-Infrared Spectroscopy," Food and Nutrition Sciences, Vol. 5 No. 2, 2014, pp. 236-244. doi: 10.4236/fns.2014.52029.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] H. C. Liu, “Study of Relationship between Oral Function and Brain Function,” Chinese Journal of Prosthodontics, Vol. 3, No. 4, 2002, pp. 137-139.
[2] Y. Kato, “Relationship among Stress, Drive for Thinness, and Eating Behavior of Female University Students: Attitude toward Sweetness an Inclination to Eating Disorders,” Japan Society of Home Economics, Vol. 55, No. 8, 2007, pp. 453-461.
[3] M. L. Kringelbach, I. E. de Araujo and E. T. Rolls, “Taste-Related Activity in the Human Dorsolateral Prefrontal Cortex,” Neuroimage, Vol. 21, No. 2, 2004, pp. 781-788.
http://dx.doi.org/10.1016/j.neuroimage.2003.09.063
[4] E. K. Miller and J. D. Cohen, “An Integrative Theory of Prefrontal Cortex Function,” Annual Review of Neuroscience, Vol. 24, 2001, pp. 167-202.
http://dx.doi.org/10.1146/annurev.neuro.24.1.167
[5] M. Okamoto, H. Dan, A. K. Singh, F. Hayakawa, V. Jurcak, T. Suzuki, K. Kohyama and I. Dan, “Prefrontal Activity during Flavor Difference Test: Application of Functional Near-Infrared Spectroscopy to Sensory Evaluation Studies,” Appetit, Vol. 74, No. 2, 2006, pp. 220-232.
http://dx.doi.org/10.1016/j.appet.2006.04.003
[6] M. Okamoto, M. Matsunami, H. Dan, T. Kohata, K. Kohyama and I. Dan, “Prefrontal Activity during Taste Encoding: An fNIRS Study,” Neuroimage, Vol. 31, No. 2, 2006b, pp. 796-806.
http://dx.doi.org/10.1016/j.neuroimage.2005.12.021
[7] C. Gagnon, L. Desjardins-Crepeau, I. Tournier, M. Desjardins, F. Lesage, C. E. Greenwood and L. Bherer, “Near-Infrared Imaging of the Effects of Glucose Ingestion and Regulation on Prefrontal Activation during DualTask Execution in Healthy Fasting Older Adults,” Behavioural Brain Research, Vol. 232, No. 1, 2012, pp. 137147. http://dx.doi.org/10.1016/j.bbr.2012.03.039
[8] S. Bembich, C. Lanzara, A. Clarici, S. Demarini, B. J. Tepper, P. Gasparini and D. L. Grasso, “Individual Difference in Prefrontal Cortex Activity during Perception of Bitter Taste Using fNIRS Methodology,” Chemical Senses, Vol. 35, No. 9, 2010, pp. 801-812.
http://dx.doi.org/10.1093/chemse/bjq080
[9] M. Ferrari and V. Quaresima, “A Brief Review of on the History of Human Functional Near-Infrared Spectroscopy (fNIRS) Development and Fields of Application,” Neuroimage, Vol. 63, No. 2, 2012, pp. 921-935.
http://dx.doi.org/10.1016/j.neuroimage.2012.03.049
[10] S. Coyle, T. Ward, C. Markham and G. McDarby, “On the Suitability of Near-Infrared (NIR) Systems for Next Generation Brain Computer Interfaces,” Physiological Measurement, Vol. 25, No. 4, 2004, pp. 815-822.
http://dx.doi.org/10.1088/0967-3334/25/4/003
[11] Y. Hoshi, N. Kobayashi and M. Tamura, “Interpretation of Near-Infrared Spectroscopy Signals: A Study with a Newly Developed Perfused Rat Brain Model,” Journal of Applied Physiology, Vol. 90, No. 5, 2001, pp. 16571662.
[12] D. T. Delpy, M. Cope, P. van der Zee, S. Arridge, S. Wray and J. Wyatt, “Estimation of Optical Pathlength through Tissue from Direct Time of Flight Measurement,” Physics in Medicine and Biology, Vol. 33, No. 12, 1988, pp. 1433-1442.
http://dx.doi.org/10.1088/0031-9155/33/12/008
[13] H. Eda, “Problems of NIRS and the Future Prospects,” Systems, Control and Information, Vol. 53, No. 4, 2009, pp. 155-161.
[14] D. M. Small, M. Jones-Gotman, R. J. Zatorre, M. Petrides and A. C. Evans, “A Role for the Right Anterior Temporal Lobe in Taste Quality Recognition,” Journal of Neuroscience, Vol. 17, No. 13, 1997, pp. 5136-5142.
[15] D. M. Small, D. H. Zald, M. Jones-Gotman, R. J. Zatorre, J. V. Pardo, S. Frey and M. Petrides, “Human Cortical Gustatory Areas: A Review of Functional Neuroimaging Data,” NeuroReport, Vol. 10, No. 1, 1999, pp. 7-14.
http://dx.doi.org/10.1097/00001756-199901180-00002
[16] D. H. Zald, J. T. Lee, K. W. Fluegel and J. V. Pardo, “Aversive Gustatory Stimulation Activates Limbic Circuits in Humans,” Brain, Vol. 121, No. 6, 1998, pp. 11431154.
http://dx.doi.org/10.1093/brain/121.6.1143
[17] R. J. Zatorre and M. Jones-Gotman, “Functional Imaging of the Chemical Senses,” In: A. W. Toga and J. C. Mazzoiotta, Eds., Brain Mapping: The Systems, Academic Press, San Diego, 2000, pp. 403-424.
http://dx.doi.org/10.1016/B978-012692545-6/50015-5
[18] M. A. Barry, J. C. Gatenby, J. D. Zeiger and J. C. Gore, “Hemispheric Dominance of Cortical Activity Evoked by Focal Electrogustatory Stimuli,” Chemical Senses, Vol. 26, No. 5, 2001, pp. 471-482.
http://dx.doi.org/10.1093/chemse/26.5.471
[19] S. Kinomura, R. Kawashima, K. Yamada, et al., “Functional Anatomy of Taste Perception in the Human Brain Studied with Positron Emission Tomography,” Brain Research, Vol. 659, No. 1-2, 1994, pp. 263-266.
http://dx.doi.org/10.1016/0006-8993(94)90890-7
[20] T. C. Pritchard, D. A. Macaluso and P. J. Eslinger, “Taste Perception in Patients with Insular Cortex Lesions,” Behavioral Neuroscience, Vol. 113, No. 4, 1999, pp. 663671.
http://dx.doi.org/10.1037/0735-7044.113.4.663
[21] G. Matsuda and K. Hiraki, “Sustained Decrease in Oxygenated Hemoglobin during Video Games in the Dorsal Prefrontal Cortex: A fNIRS Study of Children,” NeuroImage, Vol. 29, 2006, pp. 706-711.
http://dx.doi.org/10.1016/j.neuroimage.2005.08.019
[22] E. T. Rolls, Z. J. Sienkiewicz and S. Yaxley, “Hunger Modulates the Responses to Gustatory Stimuli of Single Neurons in the Caudolateral Orbitofrontal Cortex of the Macaque Monkey,” European Journal of Neuroscience, Vol. 1, No. 1, 1989, pp. 53-60.
http://dx.doi.org/10.1111/j.1460-9568.1989.tb00774.x
[23] P. Mazoyer, B. Wicker and P. Fonlupt, “A Neural Network Elicited by Parametric Manipulation of the Attention Load,” NeuroReport, Vol. 13, No. 17, 2002, pp. 2331-2334.
http://dx.doi.org/10.1097/00001756-200212030-00032
[24] G. L. Shulman, J. A. Fiez, M. Corbetta, R. L. Buckner, F. M. Miezin, M. E. Raichle and S. E. Petersen, “Common Blood Flow Changes Across Visual Tasks: II. Decreases in Cerebral Cortex,” Journal of Cognitive Neuroscience, Vol. 9, No. 5, 1997, pp. 648-663.
http://dx.doi.org/10.1162/jocn.1997.9.5.648
[25] A. R. Wade, “The Negative BOLD Signal Unmasked,” Neuron, Vol. 36, No. 6, 2002, pp. 993-995.
http://dx.doi.org/10.1016/S0896-6273(02)01138-8
[26] F. Mora, D. B. Avrith, A. G. Phillios and E. T. Rolls, “Effects of Satiety on Self-Stimulation of the Orbitofrontal Cortex in the Monkey,” Neuroscience Letters, Vol. 13, No. 2, 1979, pp. 141-145.
http://dx.doi.org/10.1016/0304-3940(79)90031-4
[27] M. W. Chee, V. Venkatraman, C. Westphal and S. C. Siong, “Comparison of Block and Event-Related fMRI Designs in Evaluating the Word-Frequency Effect,” Human Brain Mapping, Vol. 18, No.3, 2003, pp. 186-193.
http://dx.doi.org/10.1002/hbm.10092
[28] K. J. Friston, E. Zarahn, O. Josephs, R. N. Henson and A. M. Dale, “Stochastic Designs in Event-Related fMRI,” Neuroimaging, Vol. 10, No. 5, 1999, pp. 607-619.
http://dx.doi.org/10.1006/nimg.1999.0498
[29] S. T. Carmichael and J. L. Price, “Limbic Connections of the Orbital and Medial Prefrontal Cortex in Macaque Monkeys,” Journal of Comparative Neurology, Vol. 363, No. 3, 1995, pp. 615-641.
http://dx.doi.org/10.1002/cne.903630408
[30] S. T. Carmichael and J. L. Price, “Connectional Networks within the Orbital and Medial Prefrontal Cortex of Macaque Monkeys,” Journal of Comparative Neurology, Vol. 371, No. 2, 1996, pp. 179-207.
http://dx.doi.org/10.1002/(SICI)1096-9861(19960722)371:2<179::AID-CNE1>3.0.CO;2-#

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.