Representation of pleasant and aversive taste in the human brain.

In this study, the representation of taste in the orbitofrontal cortex was investigated to determine whether or not a pleasant and an aversive taste have distinct or overlapping representations in this region. The pleasant stimulus used was sweet taste (1 M glucose), and the unpleasant stimulus was salt taste (0.1 M NaCl). We used an ON/OFF block design in a 3T fMRI scanner with a tasteless solution delivered in the OFF period to control for somatosensory or swallowing-related effects. It was found that parts of the orbitofrontal cortex were activated (P < 0.005 corrected) by glucose (in 6/7 subjects) and by salt (in 6/7 subjects). In the group analysis, separate areas of the orbitofrontal cortex were found to be activated by pleasant and aversive tastes. The involvement of the amygdala in the representation of pleasant as well as aversive tastes was also investigated. The amygdala was activated (region of interest analysis, P < 0.025 corrected) by the pleasant taste of glucose (5/7 subjects) as well as by the aversive taste of salt (4/7 subjects). Activation by both stimuli was also found in the frontal opercular/insular (primary) taste cortex. We conclude that the orbitofrontal cortex is involved in processing tastes that have both positive and negative affective valence and that different areas of the orbitofrontal cortex may be activated by pleasant and unpleasant tastes. We also conclude that the amygdala is activated not only by an affectively unpleasant taste, but also by a taste that is affectively pleasant, thus providing evidence that the amygdala is involved in effects produced by positively affective as well as by negatively affective stimuli.

[1]  E. T. Rolls,et al.  Effects of satiety on self-stimulation of the orbitofrontal cortex in the rhesus monkey , 1979, Neuroscience Letters.

[2]  E. Rolls,et al.  Visual responses of neurons in the dorsolateral amygdala of the alert monkey , 1979, Experimental Neurology.

[3]  Edmund T. Rolls,et al.  Sensory specific satiety in man , 1981, Physiology & Behavior.

[4]  E. Rolls,et al.  Sensory-specific and motivation-specific satiety for the sight and taste of food and water in man , 1983, Physiology & Behavior.

[5]  T. R. Scott,et al.  Gustatory responses in the frontal opercular cortex of the alert cynomolgus monkey. , 1986, Journal of neurophysiology.

[6]  E. Rolls,et al.  Hunger Modulates the Responses to Gustatory Stimuli of Single Neurons in the Caudolateral Orbitofrontal Cortex of the Macaque Monkey , 1989, The European journal of neuroscience.

[7]  E T Rolls,et al.  Gustatory responses of single neurons in the insula of the macaque monkey. , 1990, Journal of neurophysiology.

[8]  E. Rolls,et al.  Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. , 1990, Journal of neurophysiology.

[9]  Joseph E. LeDoux,et al.  Emotion and the amygdala. , 1992 .

[10]  J. Mazziotta,et al.  Rapid Automated Algorithm for Aligning and Reslicing PET Images , 1992, Journal of computer assisted tomography.

[11]  Edmund T. Rolls,et al.  Neurophysiology and functions of the primate amygdala. , 1992 .

[12]  T. R. Scott,et al.  Gustatory neural coding in the amygdala of the alert macaque monkey. , 1993, Journal of neurophysiology.

[13]  E. Rolls,et al.  Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[14]  R. Adolphs,et al.  Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala , 1994, Nature.

[15]  A. Damasio,et al.  Insensitivity to future consequences following damage to human prefrontal cortex , 1994, Cognition.

[16]  G. C. Baylis,et al.  Afferent connections of the caudolateral orbitofrontal cortex taste area of the primate , 1995, Neuroscience.

[17]  Joseph E LeDoux,et al.  Impaired fear conditioning following unilateral temporal lobectomy in humans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[19]  E T Rolls,et al.  Taste and olfactory processing in the brain and its relation to the control of eating. , 1997, Critical reviews in neurobiology.

[20]  Wolfgang Grodd,et al.  Functional MRI reveals left amygdala activation during emotion , 1997, Psychiatry Research: Neuroimaging.

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

[22]  E. Rolls.  The Brain and Emotion , 2000 .

[23]  J. Pardo,et al.  Aversive gustatory stimulation activates limbic circuits in humans. , 1998, Brain : a journal of neurology.

[24]  R. Davidson,et al.  The functional neuroanatomy of emotion and affective style , 1999, Trends in Cognitive Sciences.

[25]  R J Zatorre,et al.  Human cortical gustatory areas: a review of functional neuroimaging data. , 1999, Neuroreport.

[26]  E. Rolls,et al.  The representation of pleasant touch in the brain and its relationship with taste and olfactory areas. , 1999, Neuroreport.

[27]  Scott T. Grafton,et al.  Amygdala activity related to enhanced memory for pleasant and aversive stimuli , 1999, Nature Neuroscience.

[28]  E T Rolls,et al.  Sensory‐specific satiety‐related olfactory activation of the human orbitofrontal cortex , 2000, Neuroreport.

[29]  R. Elliott,et al.  Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. , 2000, Cerebral cortex.

[30]  E. Rolls.  Précis of The brain and emotion. , 2000, The Behavioral and brain sciences.