An fMRI Study of the Interactions Between the Attention and the Gustatory Networks

Abstract

In a prior study, we showed that trying to detect a taste in a tasteless solution results in enhanced activity in the gustatory and attention networks. The aim of the current study was to use connectivity analyses to test if and how these networks interact during directed attention to taste. We predicted that the attention network modulates taste cortex, reflecting top-down enhancement of incoming sensory signals that are relevant to goal-directed behavior. fMRI was used to measure brain responses in 14 subjects as they performed two different tasks: (1) trying to detect a taste in a solution or (2) passively perceiving the same solution. We used psychophysiological interaction analysis to identify regions demonstrating increased connectivity during a taste attention task compared to passive tasting. We observed greater connectivity between the anterior cingulate cortex and the frontal eye fields, posterior parietal cortex, and parietal operculum and between the anterior cingulate cortex and the right anterior insula and frontal operculum. These results suggested that selective attention to taste is mediated by a hierarchical circuit in which signals are first sent from the frontal eye fields, posterior parietal cortex, and parietal operculum to the anterior cingulate cortex, which in turn modulates responses in the anterior insula and frontal operculum. We then tested this prediction using dynamic causal modeling. This analysis confirmed a model of indirect modulation of the gustatory cortex, with the strongest influence coming from the frontal eye fields via the anterior cingulate cortex. In summary, the results indicate that the attention network modulates the gustatory cortex during attention to taste and that the anterior cingulate cortex acts as an intermediary processing hub between the attention network and the gustatory cortex.

Keywords: Attention; Connectivity; Humans; Insula; Taste; fMRI.

Fig. 1

a, b Experimental design. Timeline of events within a trial. Events lasted 26 s and began with a 1-s auditory cue. In condition DETECT, the auditory cue was “liquid”, after which a solution was presented, which could be sweet, sour, salty, or tasteless. Once delivery was complete, the subject indicated whether or not he or she had tasted something by pressing a button. After the 10-s response time, the sounding of a 3-s tone indicated the window during which subjects should swallow. This was followed by a 4-s rinse of the tasteless solution and then a second swallow tone during which subjects should swallow the rinse solution. In condition PASSIVE, the cue was “sweet”, “salty”, “sour”, or “tasteless”, and thus, the subject was accurately informed about the identity of the stimulus. In this condition, the subject was required to make a random button press

Fig. 2

a Results from random effects analysis of DETECTtasteless–PASSIVEtasteless in insula and overlying operculum. Activations in the left anterior insula (AI), mid insula (MI), and parietal operculum (PO) are shown in the left axial section. Activations in the right anterior insula and frontal operculum are shown in the right axial section. The color bar represents the t values. b Results from random effects analysis of DETECTtasteless–PASSIVEtasteless in attention network. The color bar represents the t values. Axial and sagittal sections show activity in the anterior cingulate cortex (ACC), posterior cingulate cortex (PCC), left posterior parietal cortex (PPC), and right frontal eye fields (FEF)

Fig. 3

Psychophysiological interaction results. The top panels show scatterplots of regression of activity in the anterior cingulate cortex on the activity in the seed regions parietal operculum, frontal eye fields, and posterior parietal cortex, and the bottom panels of activity in anterior insula and frontal operculum on the activity in the seed region anterior cingulate cortex during condition DETECT (dark red line and triangles) vs. PASSIVE (green line and squares). Each observation corresponds to the time-series interaction with that condition (averaged over subjects). For each condition, the correlation coefficient (Pearson’s) between the activity in seed and target region is indicated. The section above each scatterplot shows the location of the seed region (circle size is not representative of sphere size of 15 mm), and the location of the region that shows neural response that was significantly associated with a stronger connectivity under DETECT vs. PASSIVE with the seed region. Color bar depicts t values

Fig. 4

DCM models and model evidence. a Invariable configuration of all network models. Taste and tasteless events (collapsed across condition) were used as driving inputs into the anterior insula (anterior insula), and all models were specified to have full “steady-state” connectivity between the nodes in the network. b The three models that were tested in DCM differed in the connections between nodes that are modulated by DETECT vs. PASSIVE. Model A specified indirect modulation of the anterior insula by the attention network; the frontal eye fields, posterior parietal cortex, and parietal operculum modulate the anterior cingulate cortex; and the anterior cingulate cortex modulates the anterior insula. Model B specified direct modulation of the anterior insula by the attention network; the frontal eye fields, posterior parietal cortex, parietal operculum, and anterior cingulate cortex all modulate the anterior insula directly. Model C specified direct and indirect modulation of the anterior insula; the frontal eye fields, posterior parietal cortex, and parietal operculum modulate the anterior cingulate cortex and anterior insula; and the anterior cingulate cortex modulates the anterior insula (model C). c Exceedance probabilities of the three models. The exceedance probability is the probability that a model is more likely than any of the other models given the observed fMRI data. Exceedance probabilities showed strong evidence in favor of model A. d Estimates of parameters in model A. Next to each of the connections, the estimated modulation parameters are specified per condition (arbitrary units, averaged over subjects +/−; standard deviation). Significant differences between conditions DETECT and PASSIVE in modulatory strength are indicated with an asterisk. Next to the anterior insula, the parameter estimate for the input strength is given for taste and tasteless events. Inputs significantly different from 0 are indicated with an asterisk