Responses of neurons in the primate taste cortex to the glutamate ion and to inosine 5'-monophosphate.
To investigate the neural encoding of glutamate taste in the primate, recordings were made from taste responsive neurons in the cortical taste areas in macaques. Most of the neurons were in the orbitofrontal cortex taste area, with a small number in adjacent taste areas. First, it was shown that single neurons that had their best responses to sodium glutamate also had good responses to glutamic acid. The correlation between the responses to these two tastants was higher than between any other pair of tastants, which included glucose (sweet), sodium chloride (salty), HCl (sour), and quinine HCl (bitter). Accordingly, the responsiveness to glutamic acid clustered with the response to monosodium glutamate in a cluster analysis with this set of stimuli, and glutamic acid was close to sodium glutamate in a space created by multidimensional scaling. Second, it was shown that the responses of these neurons to the nucleotide umami tastant inosine 5'-monophosphate were more correlated with their responses to monosodium glutamate than to any prototypical tastant. Third, concentration response curves showed that concentrations of monosodium glutamate as low as 0.001 M were just above threshold for some of these neurons. Fourth, neurons have not yet been found in this cortical region that showed synergism of monosodium glutamate and the nucleotide inosine 5'-monophosphate: it was shown that mixtures of 0.0001 M inosine 5'-monophosphate with different concentrations (0.001, 0.01, and 0.1 M) of monosodium glutamate did not have a greater effect than the monosodium glutamate alone. Fifth, some neurons in the orbitofrontal region, which responded to monosodium glutamate and other food tastes, decreased their responses after feeding with monosodium glutamate to behavioural satiety. In some cases this reduction was sensory-specific. These findings show that the taste neurons activated by monosodium glutamate can also be activated by other umami tastants, including glutamic acid and the nucleotide inosine 5'-monophosphate. The responses to these umami tastants were more similar to each other than to any of the other prototypical tastants, providing evidence that in this system umami is encoded differently from the other tastants. Moreover, the findings with these tastants provide additional evidence that the responses to monosodium glutamate are not due just to activation of a sodium taste channel.
Rolls
E T
ET
Department of Experimental Psychology, University of Oxford, England.
Critchley
H D
HD
Wakeman
E A
EA
Mason
R
R
D000818:Animals; D005947:Glucose / Q000494:pharmacology; D018698:Glutamic Acid / Q000494:pharmacology*; D006851:Hydrochloric Acid / Q000494:pharmacology; D007291:Inosine Monophosphate / Q000494:pharmacology*; D008252:Macaca fascicularis; D008253:Macaca mulatta; D008839:Microelectrodes; D017072:Neostriatum / Q000166:cytology / Q000187:drug effects; D009474:Neurons / Q000187:drug effects*; D009830:Olfactory Bulb / Q000166:cytology / Q000187:drug effects; D011803:Quinine / Q000494:pharmacology; D012528:Satiety Response / Q000187:drug effects; D012965:Sodium Chloride / Q000494:pharmacology; D013003:Somatosensory Cortex / Q000166:cytology / Q000187:drug effects*; D013649:Taste / Q000187:drug effects*
D007291:Inosine Monophosphate; D018698:Glutamic Acid; D012965:Sodium Chloride; D011803:Quinine; D005947:Glucose; D006851:Hydrochloric Acid