Gustatory responses of single neurons in the insula of the macaque monkey

Abstract

1. In recordings made from 2,925 single neurons, a region of primary taste cortex was localized to the rostral and dorsal part of the insula of the cynomolgus macaque monkey, Macaca fascicularis. The area is part of the dysgranular field of the insula and is bordered laterally by the frontal opercular taste cortex. 2. The responses of 65 single neurons with gustatory responses were analyzed in awake macaques with the use of the taste stimuli glucose, NaCl, HCl, quinine HCl (QHCl), water, and black currant juice. 3. Intensity-response functions showed that the lowest concentration in the dynamic part of the range conformed well to human thresholds for the basic taste stimuli. 4. A breadth-of-tuning coefficient was calculated for each neuron. This is a metric that can range from 0.0 for a neuron that responds specifically to only one of the four basic taste stimuli to 1.0 for one that responds equally to all four stimuli. The mean coefficient for 65 cells in the taste insula was 0.56. This tuning is sharper than that of neurons in the nucleus of the solitary tract of the monkey, and similar to that of neurons in the primary frontal opercular taste cortex. 5. A cluster analysis showed that at least six different groups of neurons were present. For each of the taste stimuli, glucose, NaCl, HCl, QHCl, water, and black currant juice, there was one group of neurons that responded much more to that tastant than to the other tastants. Other subgroups of these neurons responded to two or more of these tastants, such as glucose and black currant juice, or NaCl and QHCl. 6. On the basis of this and other evidence, it is concluded that the primary insular taste cortex, in common with the primary frontal opercular taste cortex, represents a stage of information processing in the taste system of the primate at which the tuning of neurons has become sharper than that of neurons in the nucleus of the solitary tract, and is moving toward the fineness achieved in the secondary taste cortex in the caudolateral orbitofrontal taste cortex, where motivation-dependence first becomes manifest in the taste system.

Neurobiology of anorexia and bulimia nervosa

“…That is, a primary taste cortex resides in the rostral insula and adjoining frontal operculum (189)(190)(191)(192). Some studies argue that these regions provide a representation of food in the mouth that is independent of hunger, and thus is of reward value (193).…”

A Psychological and Neuroanatomical Model of Obsessive-Compulsive Disorder

“…Rolls and colleagues28 have demonstrated that neurons in the OFC of the macaque represent the reward value of tastes. Taste neurons in the OFC, in contrast to neurons in the primary taste cortex,29,30 stop responding to the taste of a food if the monkey is fed to satiety with that food 31. Also, monkeys will work to receive electrical stimulation of the OFC if they are hungry, but not if they are satiated 32,33.…”

Altered Insula Response to Taste Stimuli in Individuals Recovered from Restricting-Type Anorexia Nervosa

“…Brain imaging studies performed in the past decade in human and nonhuman primates show that a primary taste cortex resides in the rostral insula and adjoining frontal operculum (Scott et al, 1986;Yaxley et al, 1990;Faurion et al, 1999;Schoenfeld et al, 2004). Some studies argue that these regions provide a representation of food in the mouth that is independent of hunger, and thus of reward value (Rolls, 2005).…”

“…This concentration is present in soft drinks and is a level of sweetness preferred by the general public (Drewnowski et al, 1987;Sunday and Halmi, 1990). In primates and healthy humans, both sugar (Rolls, 2005) and water (Scott et al, 1986;Yaxley et al, 1990;Zald and Pardo, 2000;De Araujo et al, 2003a) ingestion activates neurons in the primary and secondary cortical taste areas. We hypothesize that AN women might have a disturbance of these higher order pathways modulating the sensory and hedonic aspects of feeding.…”