The affective and cognitive processing of touch, oral texture, and temperature in the brain

Some of the principles of the representation of affective touch in the brain are described. Positively affective touch and temperature are represented in parts of the orbitofrontal and pregenual cingulate cortex. The orbitofrontal cortex is implicated in some of the affective aspects of touch that may be mediated through C fibre touch afferents, in that it is activated more by light touch to the forearm (a source of C-tactile (CT) afferents) than by light touch to the glabrous skin of the hand. Oral somatosensory afferents implicated in sensing the texture of food including fat in the mouth also activate the orbitofrontal and pregenual cingulate cortex, as well as the insular taste cortex. Top-down cognitive modulation of the representation of affective touch produced by word labels is found in parietal cortex area 7, the insula and ventral striatum. The cognitive labels also influence activations to the sight of touch and also the correlations with pleasantness in the pregenual cingulate/orbitofrontal cortex and ventral striatum.     

Enhanced affective brain representations of chocolate in cravers vs. non-cravers

To examine the neural circuitry involved in food craving, in making food particularly appetitive and thus in driving wanting and eating, we used fMRI to measure the response to the flavour of chocolate, the sight of chocolate and their combination in cravers vs. non-cravers. Statistical parametric mapping (SPM) analyses showed that the sight of chocolate produced more activation in chocolate cravers than non-cravers in the medial orbitofrontal cortex and ventral striatum. For cravers vs. non-cravers, a combination of a picture of chocolate with chocolate in the mouth produced a greater effect than the sum of the components (i.e. supralinearity) in the medial orbitofrontal cortex and pregenual cingulate cortex. Furthermore, the pleasantness ratings of the chocolate and chocolate-related stimuli had higher positive correlations with the fMRI blood oxygenation level-dependent signals in the pregenual cingulate cortex and medial orbitofrontal cortex in the cravers than in the non-cravers. To our knowledge, this is the first study to show that there are differences between cravers and non-cravers in their responses to the sensory components of a craved food in the orbitofrontal cortex, ventral striatum and pregenual cingulate cortex, and that in some of these regions the differences are related to the subjective pleasantness of the craved foods. Understanding individual differences in brain responses to very pleasant foods helps in the understanding of the mechanisms that drive the liking for specific foods and thus intake of those foods.     

Effects of acute tryptophan depletion on central processing of CT‐targeted and discriminatory touch in humans

C‐tactile afferents (CTs) are slowly conducting nerve fibres, present only in hairy skin. They are optimally activated by slow, gentle stroking touch, such as those experienced during a caress. CT stimulation activates affective processing brain regions, alluding to their role in affective touch perception. We tested a theory that CT‐activating touch engages the pro‐social functions of serotonin, by determining whether reducing serotonin, through acute tryptophan depletion, diminishes subjective pleasantness and affective brain responses to gentle touch. A tryptophan depleting amino acid drink was administered to 16 healthy females, with a further 14 receiving a control drink. After 4 h, participants underwent an fMRI scan, during which time CT‐innervated forearm skin and CT non‐innervated finger skin was stroked with three brushes of differing texture, at CT‐optimal force and velocity. Pleasantness ratings were obtained post scanning. The control group showed a greater response in ipsilateral orbitofrontal cortex to CT‐activating forearm touch compared to touch to the finger where CTs are absent. This differential response was not present in the tryptophan depleted group. This interaction effect was significant. In addition, control participants showed a differential primary somatosensory cortex response to brush texture applied to the finger, a purely discriminatory touch response, which was not observed in the tryptophan depleted group. This interaction effect was also significant. Pleasantness ratings were similar across treatment groups. These results implicate serotonin in the differentiation between CT‐activating and purely discriminatory touch responses. Such effects could contribute to some of the social abnormalities seen in psychiatric disorders associated with abnormal serotonin function.     

Selective attention to affective value alters how the brain processes taste stimuli

How does selective attention to affect influence sensory processing? In an fMRI investigation, when subjects were instructed to remember and rate the pleasantness of a taste stimulus, 0.1 m monosodium glutamate, activations were greater in the medial orbitofrontal and pregenual cingulate cortex than when subjects were instructed to remember and rate the intensity of the taste. When the subjects were instructed to remember and rate the intensity, activations were greater in the insular taste cortex. An interaction analysis showed that this dissociation of taste processing, depending on whether attention to pleasantness or intensity was relevant, was highly significant (P < 0.0002). Thus, depending on the context in which tastes are presented and whether affect is relevant, the brain responds to a taste differently. These findings show that, when attention is paid to affective value, the brain systems engaged to represent the sensory stimulus of taste are different from those engaged when attention is directed to the physical properties of a stimulus such as its intensity. This differential biasing of brain regions engaged in processing a sensory stimulus, depending on whether the cognitive demand is for affect‐related vs. more sensory‐related processing, may be an important aspect of cognition and attention. This has many implications for understanding the effects not only of taste but also of other sensory stimuli.     

Neuroanatomical and neurochemical bases of theory of mind

This paper presents a novel neurobiological model of theory of mind (ToM) that incorporates both neuroanatomical and neurochemical levels of specificity. Within this model, cortical and subcortical regions are functionally organized into networks that subserve the ability to represent cognitive and affective mental states to both self and other. The model maintains that (1) cognitive and affective aspects of ToM are subserved by dissociable, yet interacting, prefrontal networks. The cognitive ToM network primarily engages the dorsomedial prefrontal cortex, the dorsal anterior cingulate cortex and the dorsal striatum; and the affective ToM network primarily engages the ventromedial and orbitofrontal cortices, the ventral anterior cingulate cortex, the amygdala and the ventral striatum; (2) self and other mental-state representation is processed by distinct brain regions within the mentalizing network, and that the ability to distinguish between self and other mental states is modulated by a functionally interactive dorsal and ventral attention/selection systems at the temporoparietal junction and the anterior cingulate cortex; and (3) ToM functioning is dependent on the integrity of the dopaminergic and serotonergic systems which are primarily engaged in the maintenance and application processes of represented mental states. In addition to discussing the mechanisms involved in mentalizing in terms of its component processes, we discuss the model's implications to pathologies that variably impact one's ability to represent, attribute and apply mental states.     

The representation of pleasant touch in the brain and its relationship with taste and olfactory areas

Although there has been much investigation of brain pathways involved in pain, little is known about the brain mechanisms involved in processing somatosensory stimuli which feel pleasant. Employing fMRI it was shown that pleasant touch to the hand with velvet produced stronger activation of the orbitofrontal cortex than affectively neutral touch of the hand with wood. In contrast, the affectively neutral but more intense touch produced more activation of the primary somatosensory cortex than the pleasant stimulus. This indicates that part of the orbitofrontal cortex is concerned with representing the positively affective aspects of somatosensory stimuli, and in further experiments it was shown that this orbitofrontal area is different from that activated by taste and smell. The finding that three different primary or unlearned types of reinforcer (touch, taste, and smell) are represented in the orbitofrontal cortex helps to provide a firm foundation for understanding the neural basis of emotions, which can be understood in terms of states elicited by stimuli which are rewarding or punishing.     

Brain areas activated by uncertain reward-based decision-making in healthy volunteers

Reward-based decision-making has been found to activate several brain areas, including the ven- trolateral prefronta~ lobe, orbitofrontal cortex, anterior cingulate cortex, ventral striatum, and mesolimbic dopaminergic system. In this study, we observed brain areas activated under three de- grees of uncertainty in a reward-based decision-making task （certain, risky, and ambiguous）. The tasks were presented using a brain function audiovisual stimulation system. We conducted brain scans of 15 healthy volunteers using a 3.0T magnetic resonance scanner. We used SPM8 to ana- lyze the location and intensity of activation during the reward-based decision-making task, with re- spect to the three conditions. We found that the orbitofrontal cortex was activated in the certain reward condition, while the prefrontal cortex, precentral gyrus, occipital visual cortex, inferior parietal lobe, cerebellar posterior lobe, middle temporal gyrus, inferior temporal gyrus, limbic lobe, and midbrain were activated during the ＇risk＇ condition. The prefrontal cortex, temporal pole, inferior temporal gyrus, occipital visual cortex, and cerebellar posterior lobe were activated during am- biguous decision-making. The ventrolateral prefrontal lobe, frontal pole of the prefrontal lobe, orbi- tofrontal cortex, precentral gyrus, inferior temporal gyrus, fusiform gyrus, supramarginal gyrus, infe- rior parietal Iobule, and cerebellar posterior lobe exhibited greater activation in the ＇risk＇ than in the ＇certain＇ condition （P 〈 0.05）. The frontal pole and dorsolateral region of the prefrontal lobe, as well as the cerebellar posterior lobe, showed significantly greater activation in the ＇ambiguous＇ condition compared to the ＇risk＇ condition （P 〈 0.05）. The prefrontal lobe, occipital lobe, parietal lobe, temporal lobe, limbic lobe, midbrain, and posterior lobe of the cerebellum were activated during deci- sion-making about uncertain rewards. Thus, we observed different levels and regions of activation for different types of reward processing during decision-making. Specifically, when the degree of reward uncertainty increased, the number of activated brain areas increased, including greater ac- tivation of brain areas associated with loss.     

Priming for self-esteem influences the monitoring of one��s own performance

Social cues have subtle effects on a person, often without them being aware. One explanation for this influence involves implicit priming of trait associations. To study this effect, we activated implicit associations in participants of ‘being Clever’ or ‘being Stupid’ that were task relevant, and studied its behavioural impact on an independent cognitive task (the n-back task). Activating a representation of ‘Clever’ caused participants to slow their reaction times after errors on the working memory task, while the reverse pattern was seen for associations to ‘Stupid’. Critically, these behavioural effects were absent in control conditions. Using functional magnetic resonance imaging, we show that the neural basis of this effect involves the anterior paracingulate cortex (area 32) where activity tracked the observed behavioural pattern, increasing its activity during error monitoring in the ‘Clever’ condition and decreasing in the ‘Stupid’ condition. The data provide a quantitative demonstration of how implicit cues, which specifically target a person’s self-concept, influences the way we react to our own behaviour and point to the anterior paracingulate cortex as a critical cortical locus for mediating these self-concept related behavioural regulations.     

Brain mechanisms for processing affective touch

Despite the crucial role of touch in social development, there is very little functional magnetic resonance imaging (fMRI) research on brain mechanisms underlying social touch processing. The “skin as a social organ” hypothesis is supported by the discovery of C‐tactile (CT) nerves that are present in hairy skin and project to the insular cortex. CT‐fibers respond specifically well to slow, gentle touch such as that which occurs during close social interactions. Given the social significance of such touch researchers have proposed that the CT‐system represents an evolutionarily conserved mechanism important for normative social development. However, it is currently unknown whether brain regions other than the insula are involved in processing CT‐targeted touch. In the current fMRI study, we sought to characterize the brain regions involved in the perception of CT‐supported affective touch. Twenty‐two healthy adults received manual brush strokes to either the arm or palm. A direct contrast of the blood‐oxygenation‐level‐dependent (BOLD) response to gentle brushing of the arm and palm revealed the involvement of a network of brain regions, in addition to the posterior insula, during CT‐targeted affective touch to the arm. This network included areas known to be involved in social perception and social cognition, including the right posterior superior temporal sulcus and the medial prefrontal cortex (mPFC)/dorso anterior cingulate cortex (dACC). Connectivity analyses with an mPFC/dACC seed revealed coactivation with the left insula and amygdala during arm touch. These findings characterize a network of brain regions beyond the insula involved in coding CT‐targeted affective touch. Hum Brain Mapp, 2013. © 2011 Wiley Periodicals, Inc.     

Exposure shapes the perception of affective touch

Touch is a common occurrence in our lives, where affective and inter-personal aspects of touch are important for our well-being. We investigated whether touch exposure affects hedonic and discriminative aspects of tactile perception. The perceived pleasantness and intensity of gentle forearm stroking, over different velocities, was assessed in individuals reporting to seldom receive inter-personal touch, and in controls who received touch often. The groups did not differ in their stroking intensity judgements, nor in tactile discrimination sensitivity; however, individuals with low touch exposure evaluated the pleasantness of touch differently. These individuals did not differentiate pleasantness over the stroking velocities in the same way as the control group. The pleasantness curve for the low touch exposure group was significantly flatter and they rated 3 cm/s stroking as significantly less pleasant. Other physiological and questionnaire measures were obtained and the appreciation of touch from familiar persons was positively related to the pleasantness of touch in controls, but this was not found in low touch exposure individuals. This suggests that the association of human caresses from well-known individuals, with the pleasure derived, may depend on continued exposure to it.     

Choice selection and reward anticipation: an fMRI study

We examined neural activations during decision-making using fMRI paired with the wheel of fortune task, a newly developed two-choice decision-making task with probabilistic monetary gains. In particular, we assessed the impact of high-reward/risk events relative to low-reward/risk events on neural activations during choice selection and during reward anticipation. Seventeen healthy adults completed the study. We found, in line with predictions, that (i) the selection phase predominantly recruited regions involved in visuo-spatial attention (occipito-parietal pathway), conflict (anterior cingulate), manipulation of quantities (parietal cortex), and preparation for action (premotor area), whereas the anticipation phase prominently recruited regions engaged in reward processes (ventral striatum); and (ii) high-reward/risk conditions relative to low-reward/risk conditions were associated with a greater neural response in ventral striatum during selection, though not during anticipation. Following an a priori ROI analysis focused on orbitofrontal cortex, we observed orbitofrontal cortex activation (BA 11 and 47) during selection (particularly to high-risk/reward options), and to a more limited degree, during anticipation. These findings support the notion that (1) distinct, although overlapping, pathways subserve the processes of selection and anticipation in a two-choice task of probabilistic monetary reward; (2) taking a risk and awaiting the consequence of a risky decision seem to affect neural activity differently in selection and anticipation; and thus (3) common structures, including the ventral striatum, are modulated differently by risk/reward during selection and anticipation.     

Neuroimaging of valence decisions in children and adults

To date, the neural underpinnings of affective components in language processing in children remain largely unknown. To fill this gap, the present study examined behavioural and neural correlates of children and adults performing the same auditory valence decision task with an event-related fMRI paradigm. Based on previous findings in adults, activations in anterior and posterior cingulate cortex, orbitofrontal cortex and left inferior frontal gyrus were expected for both positive and negative valence categories. Recent behavioural findings on valence decisions showed similar ratings and reaction time patterns in children and adults. This finding was successfully replicated in the present study. On a neural level, our analysis of affective language processing showed activations in regions associated with both semantic (superior and middle temporal and frontal) and affective (anterior and posterior cingulate, orbitofrontal and inferior frontal, insula and amygdala) processing. Neural activations in children and adults were systematically different in explicit affective word processing. In particular, adults showed a more distributed semantic network activation while children recruited additional subcortical structures.     

ALE meta‐analysis reveals dissociable networks for affective and discriminative aspects of touch

Emotionally‐laden tactile stimulation—such as a caress on the skin or the feel of velvet—may represent a functionally distinct domain of touch, underpinned by specific cortical pathways. In order to determine whether, and to what extent, cortical functional neuroanatomy supports a distinction between affective and discriminative touch, an activation likelihood estimate (ALE) meta‐analysis was performed. This meta‐analysis statistically mapped reported functional magnetic resonance imaging (fMRI) activations from 17 published affective touch studies in which tactile stimulation was associated with positive subjective evaluation (n = 291, 34 experimental contrasts). A separate ALE meta‐analysis mapped regions most likely to be activated by tactile stimulation during detection and discrimination tasks (n = 1,075, 91 experimental contrasts). These meta‐analyses revealed dissociable regions for affective and discriminative touch, with posterior insula (PI) more likely to be activated for affective touch, and primary somatosensory cortices (SI) more likely to be activated for discriminative touch. Secondary somatosensory cortex had a high likelihood of engagement by both affective and discriminative touch. Further, meta‐analytic connectivity (MCAM) analyses investigated network‐level co‐activation likelihoods independent of task or stimulus, across a range of domains and paradigms. Affective‐related PI and discriminative‐related SI regions co‐activated with different networks, implicated in dissociable functions, but sharing somatosensory co‐activations. Taken together, these meta‐analytic findings suggest that affective and discriminative touch are dissociable both on the regional and network levels. However, their degree of shared activation likelihood in somatosensory cortices indicates that this dissociation reflects functional biases within tactile processing networks, rather than functionally and anatomically distinct pathways. Hum Brain Mapp 37:1308‐1320, 2016. © 2016 Wiley Periodicals, Inc.     

Differential pattern of functional brain plasticity after compassion and empathy training

Although empathy is crucial for successful social interactions, excessive sharing of others’ negative emotions may be maladaptive and constitute a source of burnout. To investigate functional neural plasticity underlying the augmentation of empathy and to test the counteracting potential of compassion, one group of participants was first trained in empathic resonance and subsequently in compassion. In response to videos depicting human suffering, empathy training, but not memory training (control group), increased negative affect and brain activations in anterior insula and anterior midcingulate cortex—brain regions previously associated with empathy for pain. In contrast, subsequent compassion training could reverse the increase in negative effect and, in contrast, augment self-reports of positive affect. In addition, compassion training increased activations in a non-overlapping brain network spanning ventral striatum, pregenual anterior cingulate cortex and medial orbitofrontal cortex. We conclude that training compassion may reflect a new coping strategy to overcome empathic distress and strengthen resilience.     

Intentional social distance regulation alters affective responses towards victims of violence: an FMRI study

We used functional magnetic resonance imaging (fMRI) to investigate brain processes underlying control of emotional responses towards a person in distress by cognitive social distance modulation. fMRI and peripheral physiological responses (startle response and electrodermal activity) were recorded from 24 women while they watched victim-offender scenes and modulated their social distance to the victim by cognitive reappraisal. We found that emotional responses, including startle eyeblink and amygdala responses, can effectively be modulated by social distance modulation. Furthermore, our data provide evidence that activity in the dorsomedial prefrontal cortex (dmPFC) and the anterior paracingulate cortex (aPCC), two brain regions that have previously been associated with brain processes related to distant and close others, is differentially modulated by intentional social distance modulation: activity in the dmPFC increased with increasing disengagement from the victim and activity in the aPCC increased with increasing engagement with the victim. We suggest that these two regions play opposing roles in cognitive modulation of social distance and affective responses towards persons in distress that enable the adaptive and flexible social behavior observed in humans.     

From affective value to decision-making in the prefrontal cortex

Representing the affective value of a reward on a continuous scale may occur separately from making a binary, for example yes vs no, decision about whether to choose the reward. To investigate whether these are separable processes, we used functional magnetic resonance imaging to measure activations produced by pleasant warm, unpleasant cold, and affectively complex combinations of these stimuli applied to the hand. On some trials the affective value was rated on a continuous scale, and on different trials a yes-no decision was made about whether the stimulus should be repeated in future. Decision-making contrasted with just rating the affective stimuli revealed activations in the medial prefrontal cortex area 10, implicating this area in binary decision-making. Activations related to the pleasantness ratings and which were not influenced when a binary decision was made were found in the pregenual cingulate and parts of the orbitofrontal cortex, implicating these regions in the continuous representation of affective value. When a decision was yes vs. no, effects were found in the dorsal cingulate cortex, agranular (anterior) insula and ventral tegmental area, implicating these areas in initiating actions to obtain goals.     

Pleasant or Unpleasant: Attentional Modulation of Odor Perception

Using positron emission tomography, we investigated whether regional brain activations differ as a function of attending to pleasant versus unpleasant components of odors. There were two experimental (attention to pleasantness and attention to unpleasantness) and one control (baseline) condition. The stimuli presented during the two experimental conditions were exactly the same (three binary mixtures, each consisting of one pleasant and one unpleasant compound), but the affective property to which participants?? attention was directed was different: They indicated with a mouse click whether each stimulus contained a pleasant (during attention to pleasantness) or unpleasant (during attention to unpleasantness) odor. During baseline, odorless stimuli were presented, and participants pressed the mouse button randomly after each one. Several brain regions were involved in both types of attention, and these included ventral striatum, right orbitofrontal cortex, and anterior cingulate cortex. Subtle differences were also revealed: Attending to pleasantness was associated preferentially with a sensory/perceptual network (piriform cortex and amygdala), whereas attending to unpleasantness engaged a component of the attentional (right parietal) network. Thus, we delineate neural substrates of attending to olfactory pleasantness and unpleasantness, some of which are common to both and others that are specific to pleasantness or to unpleasantness. Our results suggest that the view of the mesolimbic dopaminergic system as the reward network that responds selectively to positive reinforcers is somewhat limited: Our findings are more in keeping with a view of this set of structures as the salience system of the brain.     

Maternal sensitivity and infant neural response to touch: an fNIRS study

The mother’s attunement to her infant’s emotional needs influences her use of touching behaviors during mother–infant interactions. Moreover, maternal touch appears to modulate infants’ physiological responses to affective touch. However, little is known about the impact of maternal sensitivity on infants’ touch processing at a brain level. This study explored the association between maternal sensitivity when infants (N = 24) were 7 months old and their patterns of cortical activation to touch at 12 months. Brain activation was measured using functional near-infrared spectroscopy. Changes in oxy-hemoglobin (HbO₂) and deoxy-hemoglobin (HHb) concentrations were measured in the left somatosensory cortex and right temporal cortex while infants received two types of tactile stimulation—affective and discriminative touch. Results showed that a lower maternal sensitivity was associated with a higher HbO₂ response for discriminative touch over the temporal region. Additionally, infants of less sensitive mothers tended to present a higher response in HbO₂ for affective touch over the somatosensory region. These findings suggest that less sensitive interactions might result in a lower exposure to maternal touch, which can be further related to infants’ neural processing of touch.