The Neural Basis of Taste-visual Modal Conflict Control in Appetitive and Aversive Gustatory Context

Accepted Manuscript The neural basis of taste-visualmodal conflict control in appetitive and aversivegustatorycontext Xiao Xiao, Nicolas Dupuis-Roy, Jun Jiang, Xue Du, Mingmin Zhang, Qinglin Zhang PII: DOI: Reference:

S0306-4522(17)30932-6 https://doi.org/10.1016/j.neuroscience.2017.12.042 NSC 18212

To appear in:

Neuroscience

Received Date: Accepted Date:

5 March 2017 23 December 2017

Please cite this article as: X. Xiao, N. Dupuis-Roy, J. Jiang, X. Du, M. Zhang, Q. Zhang, The neural basis of tastevisualmodal conflict control in appetitive and aversivegustatorycontext, Neuroscience (2017), doi: https://doi.org/ 10.1016/j.neuroscience.2017.12.042

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The neural basis of taste-visualmodal conflict control in appetitive and aversivegustatorycontext Xiao Xiaoa,b,c, Nicolas Dupuis-Royd, Jun Jiange, Xue Duf, Mingmin Zhanga, Qinglin Zhangg a

School of Public Health and Management, Chongqing Medical University, Chongqing400016, China; b

Research Center for Medicine and Social Development, Chongqing Medical University, Chongqing400016, China;

c

Innovation Center for Social Risk Governance in Health , Chongqing Medical University, Chongqing 400016, China; d

Départment de Psychologie, Université de Montréal, Montréal, Québec, Canada

e

Department of Basic Psychology, School of Psychology, Third Military Medical University, Chongqing, China;

f

School of Education(The Key Laboratory of Psychological Diagnosis and Education Technology for Children with Special Needs）, Chongqing Normal University, Chongqing, China; g

Faculty of Psychological Science, Southwest University, Chongqing400715, China.

Number of figures: 2

Number of tables:2

Address Correspondence to:Xiao Xiao

School of Public Health and Management, Chongqing Medical University, No. 1 Yixueyuan Road, Yuzhong District, Chongqing 400016, China. E-mail address:[email protected]

Tel:

+86 13527386363 1

Abstract The functional magnetic resonance imaging (fMRI) technique was used to investigate brain activations related to conflict control in a taste-visual cross-modal pairing task. On each trial, participants had to decide if the taste of a gustatory stimulus matched or did not match the expected taste of the food item depicted in an image. There were four conditions: Negative match (NM; sour gustatory stimulus & image of sour food), negative mismatch (NMM; sour gustatory stimulus & image of sweet food), positive match (PM; sweet gustatory stimulus &image of sweet food), positive mismatch (PMM; sweet gustatory stimulus &image of sour food). Blood oxygenation level-dependent (BOLD) contrasts between the NMM and the NM conditions revealed an increased activity in the middle frontal gyrus (BA 6), the lingual gyrus (BA 18), and the postcentral gyrus. Furthermore, the NMM minus NM BOLD differences observed in the middle frontal gyrus were correlated with the NMM minus NM differences in response time. These activations were specifically associated with conflict control during the aversive gustatory stimulation. BOLD contrasts between the PMM and the PM condition revealed no significant positive activation, which supported the hypothesis that the human brain is especially sensitive to aversive stimuli. Altogether, these results suggest that the middle frontal gyrus is associated with the taste-visual cross-modal conflict control. A possible role of the lingual gyrus as an information conflict detector at an early perceptual stage is further discussed, along with a possible involvement of the postcentral gyrus in the processing of the taste-visual cross-modal sensory contrast. 2

Keywords: taste-visual cross-modality, conflict control, functional magnetic resonance imaging, emotional state

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Introduction Many of our daily adapted behaviours require the capacity for cognitive control. For example, during a final exam, high school students are well able to focus on their task and ignore distracting sounds. This ability involves the integration of goal-irrelevant information and the execution of goal-directed tasks in accordance with intentions and rules (Heinemann et al., 2009).In everyday life, the perception of surrounding information rarely takes place through a single sensory modality. Rather, perception is the result of the processing of information converging from different sensory channels. People are able to integrate information conveyed through distinct sensory modalities and to use this information to control their active behaviors (Lalanne and Lorenceau, 2004).Such cross-modal control ability is quite useful in daily life. For instance, when searching for the alarm clock in the dark, people strongly rely on both tactile and auditory cues. Additionally, empirical studies have revealed the effects of cognitive control on cross-modal information processing: congruent odors can facilitate taste identification (White and Prescott, 2007), olfaction can improve visual processing (Zhou et al., 2010), and odors can act as primes for visual information identification (Pauli et al., 1999). In fact, most studies on cross-modal information processing have focused on the facilitation. However, the processing of cross-modal stimuli sometimes hinders human performance rather than facilitating it. The last few years have seen a rapid growth of interest in cross-modal interference. Such interference has been observed in many perceptual settings. For instance, when multiple beeps are presented together with a single visual flash, people 4

report seeing more than one flash (Shams et al.,2000); when a tactile stimulus is presented together with more than one tone, people report perceiving more than a single touch (Hötting and Röder, 2004); when a flash is presented together with two taps, people report seeing two flashes (Violentyev et al.,2005). In summary, cross-modal processing of information can sometimes lead to either facilitating or interfering effect. The pairing task is a well-known paradigm that can be used to explore the neural mechanisms underlying cognitive control of cross-modal interference (Joassin et al., 2004,Puce et al., 2007, Yin et al., 2008). In this paradigm, participants are presented with cross-modal stimuli and they have to decide whether these stimuli match (e.g. human face – human sound) or not (e.g. house image – monkey sound) along some dimensions. Although several event-related potential (ERP) studies have been conducted on the subject —revealing the time-course and resolution of the cross-modal interference information processing in humans — very few have specifically examined the taste-visual cross-modal conflict control. A recent study by Xiao et al. (2011) filled this gap. In this study, participants had to decide if each pair of gustatory-visual stimuli matched (e.g. vitamin C/image of sour food) or did not match (e.g. crystal sugar/image of sour food). The sweet and sour gustatory stimuli were intermingled in the same condition. For instance, the mismatched trials included either a sour gustatory stimulation with an image of sweet food, or sweet gustatory stimulation with an image of sour food. The underlying assumption was that both type of trials elicited a common electrophysiological signal. 5

However, according to previous studies (Chapman et.al 2009, Macht and Mueller, 2007), palatable (or unpalatable) food can induce a positive (or negative) emotional mood. Moreover, evidence showed that cognitive control is influenced substantially by the emotional state. For instance, emotions can produce interference effects during ongoing cognitive tasks. In a functional MRI study, Hart and colleagues (2010) found a shorter reaction time lag for color-word incongruent trials in positive emotional state, which supports the hypothesis that positive mood can enhance the cognitive control ability. In addition, these results illustrate the important role played by the frontal cortex in cognitive control. Ashby et al. (1999) showed that a happy mood, through its effect on the dopaminergic system, could promote cognitive flexibility. Similarly, Dreisbach and Goschke (2004) suggested that positive mood could enhance the cognitive control ability to switch from an old cognitive setting to a novel set. More specifically, they found that positive mood increased the level of attention towards novel stimuli, thus reducing the costs of switching to a novel stimulus. They concluded that positive mood biased attention towards novel stimuli, but away from familiar information in the environment. Together, these findings support the facilitatory hypothesis which states that positive mood increases cognitive flexibility and improves executive functions. These results led us to speculate that the neural response to gustatory-visual cross-modal interference could be influenced by the emotional state induced by a gustatory stimulation. To the best of our knowledge, no evidence of such effect has been shown yet. Here we used the fMRI technique to test this hypothesis. 6

Given previous studies showing that(1) a positive mood can improve cognitive control abilities and that (2) cross-modal cognitive control functions are associated with activity in the frontal cortex, we expected a higher activation of the frontal cortex associated with cross-modal cognitive control during the aversive gustatory context than during the appetitive gustatory context. And since neural mechanisms involved in multisensory information processing are different from neural mechanisms elicited by inputs from a single sensory modality(Thesen et al., 2004, Macaluso and Driver, 2005, Macaluso, 2006), we also anticipated new findings concerning the brain areas specifically involved in taste-visual cross-modal cognitive control.

Materials and methods Participants Eighteen students (nine males and nine females) aged between 20 and 25 years (M= 23.1±1.3 years) participated in the experiment. All participants were healthy, right-handed, and had a normal or corrected to normal vision. Moreover, none of them ever had an allergic reaction to sour or sweet food. The experiment was approved by the Academic Committee, and an informed consent was obtained before the beginning of the study. Finally, participants were asked not to eat, smoke or drink anything but water an hour before the experiment. Stimuli The visual stimuli included ten digital images of ordinary food items. Five of these images depicted typical sour food: lemon, vinegar, and vitamin C. The remainder represented typical sweet food: ice cream, chocolate, butter cake, and sweet 7

dumplings. Prior to the experiment, the 70 students (33 males and 37 females) were presented with these images and were asked to categorize them as “sour food” or “sweet food”. No mistakes were made in this categorization task. The sour gustatory sensation was evoked by putting a 500mg vitamin C tablet on the tongue of the participant, whereas the sweet gustatory sensation was evoked by putting 2000mg of crystal sugar on their tongue. Before the experiment, all participants had to rate these two gustatory stimuli on a scale of 1 (very disgusting) to 5 (very tasteful). All of them rated crystal sugar as being very tasteful and the vitamin C tablet as being very disgusting. Procedure Each trial started with a white fixation cross displayed on a black background for a duration of 2000 ms, 4000 ms or 6000 ms. This duration was randomized across trials. The image of a food item was then shown for 2000 ms. Participants were asked to indicate as quickly as possible if the taste of the food depicted in the image matched or did not match the taste of the gustatory stimulus put on their tongue by pressing the appropriate keyboard key. Participants had to complete two blocks of 60 trials each, that is 30 trials in each of the four experimental conditions: Negative match (NM; sour gustatory stimulus & image of sour food), negative mismatch (NMM; sour gustatory stimulus & image of sweet food), positive match (PM; sweet gustatory stimulus &image of sweet food), positive mismatch (PMM; sweet gustatory stimulus &image of sour food). Just before the beginning of a block, the participant was instructed to put either sugar or a vitamin C tablet on his/her tongue and to keep it in 8

his/her mouth for the whole duration of the block. To avoid gustatory desensitization and contamination, successive blocks did not have the same gustatory stimulus. Imaging data acquisition Functional magnetic resonance imaging data were gathered while participants viewed and tested the stimuli. Scanning was performed at the Brain Imaging Center of Southwest University with a Siemens 3T Trio scanner (Siemens Medical Systems, Erlangen,

Germany)

equipped

with

an

eight-channel

phased

array

coil.

High-resolution T1-weighted structural images were collected using a Magnetization Prepared Rapid Acquisition Gradient-echo (MPRAGE) sequence (TR =1900 ms, TE = 2.52 ms, FA = 9 degrees, FOV= 256 × 256; matrix size = 256×256; slices = 176; thickness = 1.0 mm; voxel size = 1 mm3). Whole-brain functional images were acquired using a T2*-weighted gradient-EPI scan (TR =2000 ms, TE = 30 ms, FA = 90 degrees, matrix size = 64×64, FOV= 192×192, and thickness = 3 mm, gap = 33%, acquisition voxel size = 3×3×4 mm3). Imaging data analyses Data analysis was performed with SPM8 (http://www.fil.ion.ucl.ac.uk/spm/; Wellcome Department of Imaging Neuroscience, London, United Kingdom). Images were corrected for slice acquisition time within each volume and they were motion corrected with realignment to the first volume. They were also spatially normalized to the standard Montreal Neurological Institute EPI template, and spatially smoothed using a Gaussian kernel with a full width at half maximum of 8 mm. An intensity normalization and a high-pass temporal filter (width of 128 s) were also applied to the 9

data. After pre-processing functional images, two statistical contrasts were computed on individual data: NMM condition vs NM condition, and PMM condition vs PM condition. A second-level random effect analysis was then performed on the resulting individual volumes for each contrast type. The statistical significance for these two analyses was determined by a false discovery rate procedure (p<0.05, 50 contiguous voxels cutoff at the voxel level).

Results Behavioral results Mean RTs and accuracy rates for all conditions are summarized in Table 1. RTs and accuracy rates were calculated for each condition. A two-way repeated measures ANOVA was conducted on each of these two measures in order to compare the effect of the cross-modal stimuli type (match versus mismatch) and the type of gustatory stimulation (sweet versus sour). No significant main effect or interaction was found in the ANOVA on accuracy, whereas a significant main effect of cross-modal stimuli type was found in the ANOVA on RTs[F(1,17)=13.89,p=0.002], indicating that participants needed a longer time to process stimuli in the mismatch condition than in the match condition. Functional imaging results The contrast between negative mismatch (NMM) and negative match (NM) conditions indicated that the negative mismatch (NMM) condition produced significantly more neural activation in the middle frontal gyrus, lingual gyrus and 10

postcentral gyrus (see Table 2 and Figure1).Additionally, in order to explore the general relationship between the behavioral performance and the neural response, we performed correlation analyses between the difference beta-values (NMM minus NM) found in the middle frontal gyrus, lingual gyrusand postcentral gyrus, and the difference in RTs between the NMM and NM conditions (NMM minus NM).The result indicated a positive correlation between the difference beta-values of middle frontal gyrus and the difference reaction time (r = 0.498, p = 0.036)(see Figure 2). A statistical contrast between the positive mismatch (PMM) and the positive match (PM) condition was also computed but no region showed any significant positive activation. As a control, a statistical contrast between the positive and the negative gustatory conditions was performed and no significant positive activation was found.

Discussion The main goal of the present study was to investigate the neural basis of taste-visual cross-modal conflict control in an appetitive and aversive gustatory context using fMRI. We hypothesized that there would be a more activation of the frontal cortex associated to cross-modal cognitive control during the aversive gustatory condition than during the appetitive gustatory condition. The fMRI results support this hypothesis. The negative mismatch condition was associated with significantly more activation in the right middle frontal gyrus, the right lingual gyrus and the left postcentral gyrus than the negative match condition. However, no brain region showed more activation in the positive mismatch condition than in positive 11

match condition. Sweetness is an appetitive taste leading to a pleasurable experience, whereas extreme sourness is usually aversive, warning people of unpleasant acidic substances. The differences we observed in the brain regions associated with the appetitive versus the aversive gustatory conditions might be resulting from the facilitatory effect of positive mood on conflict control ability. Positive affect has been shown to facilitate cognitive control abilities in task-switching and creative problem solving. In contrast, negative affect has been shown to have a limited effect on cognitive control processes involved in planning and switching to novel stimulus (Isen, 1999). This suggests that cognitive control ability could have improved in the positive gustatory condition, thus facilitating brain processes were required by the mismatch condition. Relatedly, the current study using a pairing paradigm showed no significant positive activation in brain regions associated with conflict control during the positive gustatory condition. Middle Frontal Gyrus(MFG) It is well known that the control of the conflicting information can be localized to the MFG. Adlemanet al. (2002) used fMRI to investigate developmental changes in brain activation during a Stroop color-word interference task. Their results showed that conflict control processes involved in Stroop interference task are localized in the MFG. Similarly, Schroeteret al. (2012) discovered that the decrease of behavioral performance in a Stroop task was correlated with hypometabolism in the MFG. Schneider et al. (2011) also found that for semantically incongruent inputs, the total gamma-band activity (GBA) increased in the MFG, possibly indicating the processing 12

or detection of conflicting information during tactile-visual cross-modal conflict control. Moreover, the MFG has been found to be active when the subjects have to allot the cognitive resource to the cross-modal information (Cerf-ADucastel and Murphy, 2006; Cerf-Ducastel and Murphy, 2009; Gottfried et al. 2004; Schneider et al. 2011). In the current study, the authors observed that the middle frontal gyrus (MFG) was more activated in the NMM than in the NM condition, and a positive correlation was found between the difference beta-values (NMM minus NM) in the MFG and the difference RT values (NMM minus NM).First, this correlation indicates that the significant BOLD contrast found between the NMM and NM condition was task-related, and could not have come from a simple modulation of aversive gustatory processing by sweet images. Second, this result supports the involvement of the MFG in the control of taste-visual cross-modal informational conflict, which might reflect semantic incongruity. Lingual Gyrus(LG) The lingual gyrus has been reported to be involved in the processing of novel information. Bischof and Bassetti (2004) suggested that the LG might play a key role in the novel experience of dreams. Jauk et al., (2015) discovered that the ideational fluency was correlated with the gray matter volume in the lingual gyrus. Luo et al.[13] showed that the LG might be involved in forming novel associations during insightful problem-solving. Stoppel et al. (2009) found that the lingual gyrus (LG) was activated when novel stimuli were presented in a spatially unattended visual field. The 13

researchers’ interpretation of this finding was that LG might represent the “novelty detector at early perceptual level”. According to Menon et al. (2000), the LG might be involved in the novel information processing and encoding. In the current investigation, participants needed to taste the flavor on his or her tongue in order to judge if it matched or not the visual information. The gustatory inputs provided at the beginning of a block automatically triggered a certain taste, which primed the reaction for the upcoming trials. In the mismatch condition, the new taste of the food item depicted in the image (visual inputs) violated these gustatory expectations, consequently introducing a slight lag in responses. Consistent with the proposed “novel cognitive process” function of the LG, it is possible that the activation of the LG recorded in our study was associated with the novelty detection of an unexpected visual input during taste-visual cross-modal information processing. Postcentral Gyrus The postcentral gyrus was found to be part of taste cortical areas in humans (Faurion et al., 1998). Relatedly, a lesion in the postcentral gyrus of monkeys led to a decrease of taste contrast acuity (Bradley, 1963).Another study in humans found positive activations in the postcentral gyri when participants tasted flavourful versus tasteless food (Smeets et al., 2006). Moreover, the postcentral gyrus has been found to be part of the brain regions that represent objects in a similar fashion across different modalities (Man et al. 2013). Altogether, this suggests that the postcentral gyrus is involved in the processing of sensory contrast. Sensory contrasts regularly occur in everyday life. For instance, a person will feel 14

that an apple tastes more acidic than usual after having a candy. This is an example of a gustatory contrast. In the current study, a cross-modal sensory contrast was induced in the NMM condition when the image of a sweet food item was shown at the same time the participant received a sour vitamin C tablet on his/her tongue. Based on previous studies and the fact that the postcentral gyrus was the brain region with the highest activation in the NMM condition, it is possible that this brain region was involved in the processing of the taste-visual cross-modal sensory contrast. Considerable research indicates that the human brain is especially sensitive to emotionally negative stimuli relative to neutral and positive stimuli (Delplanque et al., 2005; Huang and Luo 2006). Behavioral study has shown that negative stimuli recruit attentional resources more rapidly, or automatically relative to positive events (Wentura et al., 2000). This could explain why we only found significant activation in the negative gustatory conditions but not in the positive gustatory conditions.

The main purpose of this study was to investigate the neural correlates of taste-visual cross-modal conflict control in an appetitive and aversive gustatory context. It was hypothesized that the activation in brain regions associated with conflict control would depend on the gustatory context, whether appetitive or aversive. Consistent with previous research, we have suggested that: (1) the middle frontal gyrus was associated with the taste-visual cross-modal conflict control in the aversive gustatory conditions; (2) the lingual gyrus has served as an information conflict detector in the aversive gustatory conditions; and (3) the postcentral gyrus was 15

involved in the processing of the taste-visual cross-modal sensory contrast occurring in the aversive gustatory context. It should also be mentioned that the fMRI results showed conflict control improvements related to positive mood, but that the behavioral data did not show any significant behavioral effect of appetitive vs aversive gustatory condition. It is possible that the neural measurements were more sensitive to the process of conflict control than the behavioral ones. Similar contradictions were reported in previous studies where significant neural activations associated with cognitive control improvements were found, but no significant effect was recorded in the reaction times (see Jung-Beeman et al. 2004; Luo et al. 2011). In the current study, sour (acid) food was used as an aversive stimulus. However, sour (acid) stimuli also act on somatosensory neurons, leading to some additional changes in cortical representation. To avoid this effect, bitter taste food should be used as aversive stimuli in future studies. In the current study, we did not control the intensity of the cross-modal conflict. Whether or not such manipulation has an impact on the activation of the MFG remains an open question that should be addressed in future studies. To the best of our knowledge, this is the first fMRI study that investigated the neural correlates of taste-visual cross-modal conflict control. Given the strong relationship between the sense of smell and taste, future studies are needed to clarify whether the activation in brain regions associated with conflict control would depend on the olfactory context.

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Acknowledgements This study was supported by the National Natural Science Foundation of China (Grant No. 31500874 Xiao Xiao), Funds for outstanding young scholars in Chongqing Medical University (Grant No.CYYQ201406, Xiao Xiao) and the National Natural Science Foundation of China (Grant No. 31600874, Jun Jiang). We thank two anonymous reviewers for their helpful comments in the manuscript revision.

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Table 1

Descriptive statistics for behavioral data.

Table 2 Brain regions showing significant differences by comparisons of negative mismatch (NMM) versus negative match (NM) conditions. (FDR-corrected threshold of P < 0.05, 50 contiguous voxels cutoff at the voxel level)

Figure1.Voxels showing significant differences (t-value) between the negative mismatch (NMM) and the negative match (NM) conditions are depicted in color. A FDR-corrected threshold of p < 0.05 was used, with a 50 contiguous voxels cut-off at the voxel level. The color density represents the T score.

Figure2. Correlation between the difference beta-values of middle frontal gyrus and the difference reaction time

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Table 1

Descriptive statistics for behavioral data.

Condition

RT(ms)

Accuracy rates(%)

NMM

780±136

98.5%±3.5%

NM

733±157

99.1%±1.9%

PMM

832±161

98.5%±2.1%

PM

759±145

98.1%±4%

Table 2

Brain regions showing significant differences by comparisons of negative mismatch (NMM) versus negative match (NM) conditions. (FDR-corrected threshold of P < 0.05, 50 contiguous voxels cutoff at the voxel level) Brain regions

He mi

MNI coordinates (Peak voxel) x

y

z

21 30 -48

-18 -72 -15

60 -12 57

Cluster size (voxels)

t Value (cluster maxima)

136 341 192

7.73 6.17 3.97

NMM - NM Middle frontal gyrus Lingual gyrus Postcentral gyrus

R R L

NM - NMM There were no regions that showed positive activation Note: MNI: Montreal Neurological Institute; Hemi: hemisphere; L: left; R: right.

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>An appetitive gustatory stimulation increases cognitive flexibility. > MFG is associated with the taste-visual cross-modal conflict control.

25