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

Abstract

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.

Figure 1.

Photomicrograph (left) and diagram (right) of a coronal section of the mOFC in monkey SAT2. The HRP injection in the right panel marks the location of the core taste area in BA 13m.

Figure 2.

The core and perimeter taste areas projected onto an unfolded map of the OFC of monkey SAT2. Distances between BA boundaries were measured through layer IV.

Figure 3.

Three-dimensional histogram showing the percentage of taste cells recorded within the mOFC search grid of monkey SAT2. The anterior/posterior and medial/lateral coordinates (in millimeters) are indexed to the anterior clinoid process of the sphenoid bone.

Figure 4.

Evoked responses from two neurons recorded in the mOFC. A, The neuron responded to HCl and benzaldehyde. B, A neuron that responded during the application of distilled water (dH₂O). The responses to the sapid stimuli were not significantly different from the water-evoked response. Fluid onset is marked by the arrowhead. Significant responses are indicated by asterisks.

Figure 5.

Average response rate for G-, N-, H-, and Q-best cells.

Figure 6.

Response similarity based on cluster analysis of 142 neurons is shown as a dendrogram. The cell number indicates the order in which cells were recorded during the experiment. Each best-stimulus of the neuron, plus other stimuli that met the 80% criterion, is shown along the ordinate. Q, H, N, and G indicate Q-, H-, N-, and G-group, respectively.

Figure 7.

Multidimensional map showing neuron similarity in two dimensions (A) and three dimensions (B). The dimensions are undefined but mathematically orthogonal to one another. Each neuron is represented as one data point. Interneuronal proximity is based on the similarity of their response profiles, as calculated by the Pearson product-moment correlation coefficient. Asterisks represent neurons that responded equally to two stimuli. Circles represent neurons with responses that were exclusively inhibitory.

Figure 8.

Percentage of taste neurons in the mOFC and the clOFC that respond to one, two, three, or all four of the basic taste stimuli.