Prefrontal activity during taste encoding: An fNIRS study

To elucidate the function of the lateral prefrontal cortex (LPFC) in taste encoding, it is worth applying to taste, the psychological paradigms of intentional memorization that have been used with other extensively studied senses, and thus updating current models for LPFC functions to include a taste modality. Using multichannel functional near-infrared spectroscopy (fNIRS), we examined the LPFC's of healthy volunteers (N = 18) during the intentional memorization of a basic taste. In order to minimize the confounding effects of verbal processes that are known to employ the left LPFC, we used quaternary taste mixtures that were difficult to verbalize, and confined analysis to those who did not use a verbal strategy during memorization (N = 10). In order to examine the results in association with data in the literature, the location of activity was probabilistically estimated and anatomically labeled in the Montreal Neurological Institute (MNI) standard brain space. By contrasting the cortical activation under encoding conditions with that under control conditions without memory requirement, we found activation in the bilateral ventro-LPFC and the right posterior portion of the LPFC. The activation pattern was consistent with previous studies on the encoding of nonverbal materials using other senses. This suggests that models for LPFC functions that derive from previous studies can be generalized to intentional encoding processes of taste information, at least at a macro-structural level. The current study also demonstrates that, by using fNIRS, LPFC functions on taste can be examined with experimental paradigms relevant to those used for other senses.

[1]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[2]  B. Gulyás,et al.  Visual memory, visual imagery, and visual recognition of large field patterns by the human brain: functional anatomy by positron emission tomography. , 1995, Cerebral cortex.

[3]  J. Desmond,et al.  Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. , 2001, Brain : a journal of neurology.

[4]  D. Delpy,et al.  Methods of quantitating cerebral near infrared spectroscopy data. , 1988, Advances in experimental medicine and biology.

[5]  Morten Meilgaard,et al.  Sensory Evaluation Techniques , 2020 .

[6]  Bruce L. McNaughton,et al.  Differential Encoding of Behavior and Spatial Context in Deep and Superficial Layers of the Neocortex , 2005, Neuron.

[7]  J. Calabrese,et al.  Hemodynamic differences in the activation of the prefrontal cortex: attention vs. higher cognitive processing , 2004, Neuropsychologia.

[8]  I. Johnsrude,et al.  The problem of functional localization in the human brain , 2002, Nature Reviews Neuroscience.

[9]  Alan C. Evans,et al.  A Role for the Right Anterior Temporal Lobe in Taste Quality Recognition , 1997, The Journal of Neuroscience.

[10]  David A. Boas,et al.  A Quantitative Comparison of Simultaneous BOLD fMRI and NIRS Recordings during Functional Brain Activation , 2002, NeuroImage.

[11]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[12]  D. Pandya,et al.  Architecture and Connections of the Frontal Lobe , 2019, The Frontal Lobes Revisited.

[13]  Karl Magnus Petersson,et al.  Instruction-specific brain activations during episodic encoding a generalized level of processing effect , 2003, NeuroImage.

[14]  Archana K. Singh,et al.  Spatial registration of multichannel multi-subject fNIRS data to MNI space without MRI , 2005, NeuroImage.

[15]  R. Henson,et al.  Frontal lobes and human memory: insights from functional neuroimaging. , 2001, Brain : a journal of neurology.

[16]  Michael Petrides,et al.  6 – Mapping Prefrontal Cortical Systems for the Control of Cognition , 2000 .

[17]  Robert J. Zatorre,et al.  Functional Imaging of the Chemical Senses , 2000 .

[18]  E. Watanabe,et al.  Spatial and temporal analysis of human motor activity using noninvasive NIR topography. , 1995, Medical physics.

[19]  V Menon,et al.  Modality effects in verbal working memory: differential prefrontal and parietal responses to auditory and visual stimuli , 2004, NeuroImage.

[20]  Leslie G. Ungerleider,et al.  Face encoding and recognition in the human brain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Morten L Kringelbach,et al.  Taste-related activity in the human dorsolateral prefrontal cortex , 2004, NeuroImage.

[22]  Satoru Miyauchi,et al.  Circulatory basis of fMRI signals: relationship between changes in the hemodynamic parameters and BOLD signal intensity , 2004, NeuroImage.

[23]  L. Engelen,et al.  The role of intra-oral manipulation in the perception of sensory attributes , 2003, Appetite.

[24]  E. Ahissar,et al.  Neural signature of taste familiarity in the gustatory cortex of the freely behaving rat. , 2004, Journal of neurophysiology.

[25]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[26]  Edward E. Smith,et al.  PET Evidence for an Amodal Verbal Working Memory System , 1996, NeuroImage.

[27]  Yasushi Miyashita,et al.  Cognitive Memory: Cellular and Network Machineries and Their Top-Down Control , 2004, Science.

[28]  P. Grasby,et al.  PET activation of the medial temporal lobe in learning. , 1998, Brain : a journal of neurology.

[29]  Rüdiger J. Seitz,et al.  A fronto-parietal circuit for tactile object discrimination: an event-related fMRI study , 2003, NeuroImage.

[30]  Michael Petrides,et al.  Orbitofrontal contribution to auditory encoding , 2004, NeuroImage.

[31]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[32]  Masako Okamoto,et al.  Multimodal assessment of cortical activation during apple peeling by NIRS and fMRI , 2004, NeuroImage.

[33]  J C Gore,et al.  Hemispheric dominance of cortical activity evoked by focal electrogustatory stimuli. , 2001, Chemical senses.

[34]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[35]  R. Henson,et al.  The neural basis of episodic memory: evidence from functional neuroimaging. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[36]  Ellen Perecman,et al.  The frontal lobes revisited. , 1987 .

[37]  S. Kinomura,et al.  Functional anatomy of taste perception in the human brain studied with positron emission tomography , 1994, Brain Research.

[38]  Florin Dolcos,et al.  Dissociable effects of arousal and valence on prefrontal activity indexing emotional evaluation and subsequent memory: an event-related fMRI study , 2004, NeuroImage.

[39]  R S Berndt,et al.  Modality-specific processing streams in verbal working memory: evidence from spatio-temporal patterns of brain activity. , 1997, Brain research. Cognitive brain research.

[40]  John R. Piggott,et al.  Dynamic methods of sensory analysis , 2000 .

[41]  K. Berridge Food reward: Brain substrates of wanting and liking , 1996, Neuroscience & Biobehavioral Reviews.

[42]  Alan C. Evans,et al.  Working Memory in Another Dimension: Functional Imaging of Human Olfactory Working Memory , 2001, NeuroImage.

[43]  Noriaki Hattori,et al.  Functional Imaging of Gustatory Perception and Imagery: Btop-downq Processing of Gustatory Signals , 2004 .

[44]  Masako Okamoto,et al.  Automated cortical projection of head-surface locations for transcranial functional brain mapping , 2005, NeuroImage.

[45]  Masako Okamoto,et al.  Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping , 2004, NeuroImage.

[46]  Robert J Zatorre,et al.  Olfactory learning: convergent findings from lesion and brain imaging studies in humans. , 2002, Brain : a journal of neurology.

[47]  N. Sadato,et al.  Functional asymmetry of human prefrontal cortex in verbal and non-verbal episodic memory as revealed by fMRI. , 2000, Brain research. Cognitive brain research.

[48]  H. Müller-Gärtner,et al.  Encoding and retrieval in declarative learning: a positron emission tomography study , 1998, Behavioural Brain Research.

[49]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[50]  A. Villringer,et al.  Beyond the Visible—Imaging the Human Brain with Light , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[51]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[52]  M Petrides,et al.  Orbitofrontal cortex: A key prefrontal region for encoding information. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Archana K. Singh,et al.  Virtual 10–20 measurement on MR images for inter-modal linking of transcranial and tomographic neuroimaging methods , 2005, NeuroImage.

[54]  P. Eslinger,et al.  Taste perception in patients with insular cortex lesions. , 1999, Behavioral neuroscience.

[55]  E. Tulving Elements of episodic memory , 1983 .

[56]  Tsunehiro Takeda,et al.  The primary gustatory area in human cerebral cortex studied by magnetoencephalography , 1996, Neuroscience Letters.

[57]  L. Nyberg,et al.  Common fronto-parietal activity in attention, memory, and consciousness: Shared demands on integration? , 2005, Consciousness and Cognition.

[58]  J. Mazziotta,et al.  Brain mapping : the systems , 2000 .

[59]  U. Krings,et al.  In vitro study of the influence of physiological parameters on dynamic in-mouth flavour release from liquids. , 2004, Chemical Sensors.

[60]  P M Grasby,et al.  Brain systems for encoding and retrieval of auditory-verbal memory. An in vivo study in humans. , 1995, Brain : a journal of neurology.

[61]  Michael Petrides,et al.  Orbitofrontal Cortex and Memory Formation , 2002, Neuron.

[62]  Hellmuth Obrig,et al.  Towards a standard analysis for functional near-infrared imaging , 2004, NeuroImage.

[63]  D. Delpy,et al.  Performance comparison of several published tissue near-infrared spectroscopy algorithms. , 1995, Analytical biochemistry.

[64]  Y. Hoshi Functional near-infrared optical imaging: utility and limitations in human brain mapping. , 2003, Psychophysiology.

[65]  A. Toga,et al.  Functional assessment of Broca's area using near infrared spectroscopy in humans. , 2003 .

[66]  Anthony Randal McIntosh,et al.  Transperceptual Encoding and Retrieval Processes in Memory: A PET Study of Visual and Haptic Objects , 2001, NeuroImage.

[67]  Alan C. Evans,et al.  Functional localization and lateralization of human olfactory cortex , 1992, Nature.

[68]  M. Theunissen,et al.  Mouth movements diminish taste adaptation, but rate of mouth movement does not affect adaptation. , 1996, Chemical senses.

[69]  D. Boas,et al.  Non-invasive neuroimaging using near-infrared light , 2002, Biological Psychiatry.

[70]  S. Petersen,et al.  Hemispheric Specialization in Human Dorsal Frontal Cortex and Medial Temporal Lobe for Verbal and Nonverbal Memory Encoding , 1998, Neuron.

[71]  C. S. Lin,et al.  Taste memory induces brain activation as revealed by functional MRI. , 1999, Journal of computer assisted tomography.

[72]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[73]  Susan M. Courtney,et al.  Functional topography of working memory for face or voice identity , 2005, NeuroImage.

[74]  M. Petrides,et al.  Differential activation of the human orbital, mid-ventrolateral, and mid-dorsolateral prefrontal cortex during the processing of visual stimuli , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[75]  A R McIntosh,et al.  The neural correlates of intentional learning of verbal materials: a PET study in humans. , 1996, Brain research. Cognitive brain research.

[76]  M. Tamura,et al.  Interpretation of near-infrared spectroscopy signals: a study with a newly developed perfused rat brain model. , 2001, Journal of applied physiology.

[77]  J. Mehler,et al.  Sounds and silence: An optical topography study of language recognition at birth , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[78]  D. Katz The many flavors of temporal coding in gustatory cortex. , 2005, Chemical senses.

[79]  T. Shallice,et al.  Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. , 1999, Brain : a journal of neurology.

[80]  L. Parsons,et al.  Location-Probability Profiles for the Mouth Region of Human Primary Motor–Sensory Cortex: Model and Validation , 2001, NeuroImage.