Satiety-responsive neurons in the medial orbitofrontal cortex of the macaque.

Feeding-related gustatory, olfactory, and visual activation of the orbitofrontal cortex (OFC) decreases following satiety. Previous neurophysiological studies have concentrated on the caudolateral OFC (clOFC). We describe satiety-induced modulation of 23 gustatory, 5 water, and 15 control neurons in the medial OFC (mOFC), where gustatory neurons represent a much larger percentage of the population. For 15 of the 23 gustatory neurons (65%), every significant taste response evoked during pre-satiety testing decreased following satiety (X=70%). Responses evoked by the ineffective taste stimuli during pre-satiety testing were unchanged following satiety. The graded response decrements of the mOFC gustatory neurons stand in marked contrast to the clOFC responses, which are almost completely suppressed by satiety. Two other novel findings are reported here. First, all significant pre-satiety taste responses of four gustatory neurons increased following satiety (X=51%). Second, post-satiety emergent taste responses were observed in 7 of 15 neurons (47%) classified as non-responsive during pre-satiety testing. The presence of increased responsiveness and emergent gustatory neurons in the mOFC suggests that meal termination may require active processes as well as the passive loss of hedonic value.

Taste in the medial orbitofrontal cortex of the macaque.

Taste activates about 6% of the neurons in the anterior insula (primary taste cortex) of the macaque. The anterior insula has many direct and indirect projections to the orbitofrontal cortex (OFC), including the caudolateral OFC (clOFC), where only 2% of the neurons respond to taste. We have identified a 12-mm(2) region in the medial OFC (mOFC) where taste represents 7-28% of the population. This rich trove of taste cells has functional characteristics typical of both the insular cortex that projects to it and the clOFC to which it projects. Mean spontaneous rate was 3.1 spikes/s, nearly identical to that in the insula, but double that of the clOFC. In the mOFC, 19% of the taste cells also responded to other modalities, most commonly olfaction and touch, slightly less than the 27% in the clOFC. The distribution of best stimulus neurons was almost even across the four prototypical stimuli in the mOFC, as in insula, but discrepant from the clOFC, where sugar responsiveness dominated. The broadly tuned taste neurons in the mOFC were similar to those in the insula and strikingly different from the more specialized cells of the clOFC. Whereas the responsiveness to the taste of a satiating stimulus declines among the narrowly tuned clOFC cells, satiety has much less impact on the responsiveness of mOFC neurons. The mOFC is a robust area worthy of exploration for its involvement in gustatory coding, the amalgamation of sensory inputs to create flavor, and the hedonics that guide feeding.

Gustatory neural responses in the medial orbitofrontal cortex of the old world monkey.

The primary taste cortex has widespread and occasionally dense projections to the orbitofrontal cortex (OFC) in the macaque. Nonetheless, electrophysiological studies have revealed that only 2-8% of the cells in the OFC are activated by taste stimuli on the tongue. We describe an area centered in Brodmann's area 13m of the medial OFC (mOFC) where taste neurons are more concentrated. It consists of a 12 mm2 core, where gustatory neurons constituted 20% of the population, and a 1 mm perimeter in which 8% of the cells responded to taste. Data were collected from three awake cynomolgus monkeys (Macaca fascicularis) prepared for chronic recording. Single neurons were isolated with epoxylite-coated tungsten microelectrodes and tested for responsiveness to 1.0 m glucose, 0.3 m NaCl, 0.03 m HCl, and 0.001 m QHCl. These stimuli elicited responses that were 96% excitatory and ranged from 5.2 to 5.9 spikes/s. Cells were broadly tuned (H = 0.79), similar to those in the anterior insula (H = 0.70), and decidedly unlike the narrowly tuned taste neurons in the caudolateral OFC (clOFC; H = 0.39). Whereas 82% of the taste cells in the clOFC respond to glucose, in the mOFC, HCl-responsive (56%), glucose-responsive (50%), NaCl-responsive (43%), and QHCl-responsive (40%) cells were almost evenly represented. The mOFC taste area appears to comprise a major gustatory relay that lies anatomically and functionally between the anterior insula and the clOFC.