Gustatory responses of cortical neurons in rats. II. Information processing of taste quality

Abstract

The present report was designed to investigate neural coding of taste information in the cerebral cortical taste area of rats. The magnitude and/or type (excitatory, inhibitory, or no-response) of responses of 111 cortical neurons evoked by single concentrations of the four basic taste stimuli (sucrose, NaCl, HCl, and quinine HCl) were subjected to four types of analyses in the context of the four proposed hypotheses of taste-quality coding: across-neuron response-pattern, labeled-line, matrix-pattern, and across-region response-pattern notions (88 histologically located neurons). An across-neuron response-pattern notion assumes that taste quality is coded by differential magnitudes of response across many neurons. This theory utilizes across-neuron correlation coefficients as a metric for the evaluation of taste quality coding. Across-neuron correlations between magnitudes of responses to any pairs of the four basic taste stimuli across 111 cortical neurons were very high and were similar. However, calculations made with net responses (spontaneous rate subtracted) resulted in less positive correlations but still similar values among the various pairs of taste stimuli. This finding suggests that across-neuron response patterns of cortical neurons become less discriminating among taste qualities compared with those of the lower-order neurons. A labeled-line notion assumes that there are identifiable groups of neurons and that taste quality is coded by activity in these particular sets of neurons. Some investigators have classified taste-responsive neurons into best-stimulus categories, depending on their best sensitivity to any one of the four basic stimuli, such as sucrose-best, NaCl-best, HCl-best, and quinine-best neurons; they have suggested that taste can be classified along four qualitative dimensions that correspond to these four neuron types (i.e., four labeled lines). The present study shows that responsiveness of each of the four best-stimulus neurons had similar profiles between peripheral and cortical levels. That is, when the stimuli were arranged along the abscissa in the order of sucrose, NaCl, HCl, and quinine, there is a peak response in one place, and the responses decreased gradually from the peak. However, such response characteristics do not favor the labeled-line theory, since they can be explained in the context of the across-neuron pattern theory. A matrix-pattern notion assumes that taste quality is coded by a spatially arranged matrix pattern of activated neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

Differential Spatial Representation of Taste Modalities in the Rat Gustatory Cortex

“…Although reflexes of acceptance and avoidance might not need the presence of the GC (Grill and Norgren, 1978), our results provided the evidence for functional taste differentiation even at the cortical level, although the territories are not strictly distinct. Our results are in agreement with previous electrophysiological studies (Yamamoto et al, 1985(Yamamoto et al, , 1989 and partially consistent with the genetic tracing study (Sugita and Shiba, 2005) because the labeled neurons might belong to the regions that we found activated by one but not by the other taste modality. However, the presence of overlapping regions does not allow us to state that the two modalities have a segregated cortical representation.…”

“…Focusing on the GC level, consistent with the labeled-line model, a recent genetic tracing approach showed partially segregated neuronal circuitries for bitter and sweet along the entire gustatory pathway (Sugita and Shiba, 2005). Using extracellular recordings from anesthetized rats, a chemotopic organization of the primary GC was proposed (Yamamoto et al, 1985).…”

“…1), anterior and dorsal to areas receiving visceral and nociceptive inputs (Cechetto and Saper, 1987;Barnett et al, 1995). The MCA and the RHVs provide anatomical landmarks helping to locate precisely the GC (Yamamoto et al, 1985;Kosar et al, 1986). The MCA passes vertically through the GC, whereas the RHV runs in the rhinal sulcus, perpendicular to the MCA and ventral to the GC (Fig.…”

“…However, these results do not allow ruling out of the possibility of a spatial organization. Indeed, Yamamoto et al (1985) proposed a possible chemotopic organization of the rat GC based on extracellular recordings and on an arbitrary grid partition of the cortical area.…”

Taste representation in the human insula

“…The data were estimated based on the finite impulse response model. The color bar represents the t values and the t-map image was thresholded at P \ 0.001 uncorrected Brain Struct Funct (2010) 214:551-561 553 somatosensory and taste stimulation (Yamamoto et al 1985;Smith-Swintosky et al 1991;Plata-Salaman et al 1992Kadohisa et al 2004). Thus, activation in response to a taste stimulus may well be caused by costimulation of oral somatosensation.…”