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The reinforcement sensitivity theory RST proposed the behavioral activation system BAS as a neurobehavioral system that is dependent on dopamine-irrigated structures and that mediates the individual differences in sensitivity and reactivity to appetitive stimuli associated with BAS-related personality traits.
Theoretical developments propose that high BAS sensitivity is associated with both enhanced appetitive stimuli processing and the diminished processing of aversive stimuli. The objective of this study was to analyze how individual differences in BAS functioning were associated with brain activation during erotic and aversive picture processing while subjects were involved in a simple goal-directed task. Forty-five male participants took part in this study. The task activation results confirm the activation of the reward and punishment brain-related structures while viewing erotic and aversive pictures, respectively.
The SR scores show a positive correlation with activation of the left lateral prefrontal cortex, the mesial prefrontal cortex and the right occipital cortex while viewing erotic pictures, and a negative correlation with the right lateral prefrontal cortex and the left occipital cortex while viewing aversive pictures.
The Reinforcement Sensitivity Theory RST; Gray, , ; Gray and McNaughton, predicts that reinforcing stimulus detection and reactivity may vary among individuals depending on the sensitivity of their proposed neurobehavioral systems. In this context, sensitivity may be defined as the global reactivity of the neurobiology associated with this motivational system in the presence of rewarding stimuli Depue and Collins, The neurobiology of the BAS is related to the commonly identified dopaminergic reward circuitry.
It involves the projections from the substantia nigra and the ventral tegmental area VTA to the dorsal and ventral striatum, and also their corresponding cortical projections to the prefrontal cortex Depue and Collins, ; Pickering and Gray, ; Knutson and Cooper, Within the prefrontal cortex, the mesial prefrontal cortex MPFC and the orbitofrontal cortex OFC are proposed to be relevant areas during reward processing McClure et al.
On the other hand, the OFC has been proposed to be an area for storing the reward value of sensory stimuli McClure et al. RST predictions on BAS functioning are straightforward: appetitive motivational stimuli are expected to activate the BAS, and this activation should be greater in those individuals with higher scores in BAS-related trait measures.
The first prediction received clear support from neuroimaging studies that have served to clarify the role of the ventral striatum, the dorsal striatum, the OFC and the MPFC in reward processing see McClure et al. However, there is less evidence to support the second prediction.
An fMRI study has shown that individual differences in the BAS-related trait correlated with the brain activation of the mesocorticolimbic structures during the passive viewing of appetizing foods Beaver et al. Although this result is consistent with the RST, it would be interesting to replicate it in a larger sample and to use other kinds of appetitive stimuli.
The RST also states that sensitivity to aversive stimuli is mediated by two biobehavioral systems. Secondly, the Behavioral Inhibition System BIS; Gray and McNaugton, does not mediate direct reactions to aversive stimuli, but to those stimuli giving way to a conflict of goals. These two systems are proposed to work as a double system that activates aversive stimuli Corr, However, several experimental studies have shown that, under specific circumstances involving goal-directed responses frequently followed by reward, highly sensitive BAS subjects show a diminished processing of aversive secondary cues when compared with individuals with low BAS sensitivity Newman et al.
In order to test both hypotheses, we used a paradigm that our group had previously applied Meseguer et al. Therefore, in the current study, we investigated individual differences in BAS-sensitivity for brain functional activation during the processing of appetitive and aversive stimuli while subjects were involved in a simple goal-directed task. The task consisted of a continuous letter discrimination task while subjects viewed background pictures of the IAPS in a block-design fashion.
Consistent with previous research see Wager et al. On the other hand, background aversive pictures produced the activation of the bilateral middle, dorsolateral and inferior frontal cortices, the bilateral amygdala and the occipital cortex, among other areas see Meseguer et al. This measure has been suggested to be more closely related to the tendency to approach appetitive situations Smillie and Jackson, However, the SR scale shows a similar range of positive correlations with other subscales that measure different hedonic or motivational aspects within the BAS Caseras et al.
The SR scores were previously shown to be positively related to psychopathy Newman et al. They negatively relate to depression Pinto-Meza et al. In contrast, BAS overactivity is associated with a stronger processing of appetitive pictures as found in previous research Beaver et al.
Our specific hypotheses for the present study are i appetitive conditions would activate BAS-related structures i. The participants were thoroughly questioned about sexual orientation, and psychiatric, neurological or medical diseases, as well as their use of psychoactive substances. No subject included in the study had a history of Axis I or Axis II disorders, or of neurological or severe medical illnesses. All the participants signed a written informed consent prior to participation.
Three categories of 50 stimuli each were used for the experimental trials and were classified into block conditions in terms of their valence for the male population: neutral, appetitive and aversive. The contents of the neutral condition included those images with a valence rate of 5 or scores from the norming data closest to 5.
Aversive stimuli were selected from those with a lower valence rate and that were related to mutilations, murdered people, human threat, guns, etc. Finally, all the appetitive stimuli were related to erotic pictures with couples sexually erotic or romantic scenes. The mean valence ratings from the selected pictures were 2. The mean arousal scores were 6. The task was programmed using the Presentation software Neurobehavioral systems, Inc. Pictures were displayed inside the scanner using Visuastim goggles Resonance Technologies, Inc.
The participants were told that they were about to do a letter discrimination task, and that the pictures were used as a background and were not relevant for the task. Each picture was presented for 2. To ensure picture processing, white letters inside a small black square were presented in the middle of the screen that were also superimposed on the picture that had already appeared ms before.
The experiment was run as a single session. Prior to the scanning session, the participants viewed a reduced version 2 min of the task with neutral pictures, while they were carefully instructed to perform the letter-discrimination task.
The images during the valence and arousal ratings were randomly presented. Three or more continuous pictures of the same emotional condition to be scored were also avoided. Scanning was performed on a 1. We acquired 29 interleaved axial slices parallel to the anterior-posterior commissure AC-PC plane covering the entire brain.
Anatomical and functional volumes were coregistered and realigned, respectively, to the first functional volume. In addition, the time series of hemodynamic responses were high-pass filtered s to eliminate low-frequency components.
Image analyses were performed using a general linear model approach. Time series were modeled at each condition using the hemodynamic response function and its temporal derivative since slice timing was not preprocessed and, besides, it reduces error variance due to a temporal delay variation in different spatial locations.
Moreover, movement parameters from the motion correction were included for each subject as regressors of non-interest at this first-level analysis. The local maxima for each analysis were reported in the MNI coordinates. When differences among the conditions based on valence and arousal were tested, differences regarding image selection were found. As expected, erotic picture viewing produced brain activations in the neurobiological substrates of the BAS see Table 1 , Figure 1 , which involved structures in the striatum and the limbic cortex, such as the dorsal caudate and ventral nucleus accumbens striatum, the amygdala and the anterior cingulate.
Additional activations were located in the medial, bilateral lateral and medial prefrontal cortices, the precentral gyrus and the supplementary motor area see Table 1. R: right; L: left; B-cluster extended bilaterally within the same structure, but local maxima located at the reported coordinate.
Functional activity during erotic picture processing. The colorbar represents the T -values applicable to the image. Bottom image numbers correspond to z MNI coordinates. Aversive picture viewing produced activation in the brain areas of the limbic system and the frontal lobe, among others see Table 2 , Figure 2.
Thus, there was an activation of limbic and paralimbic structures like the posterior cingulate, the hippocampus and the bilateral amygdala.
Prefrontal activations were located bilaterally in the lateral and inferior parts, and in the superior medial prefrontal cortex. R: right; L: left; B-cluster extended bilaterally within the same structure, but local maxima located at reported coordinate.
Inf: undefined Z-value tends to infinite, but t -score reported. Functional activity during aversive picture processing. However, they did not show a positive correlation with the activation of either the striatum or the OFC, contrary to our hypotheses. The left lateral inferior frontal gyrus and the precuneus also positively correlated with SR during the same condition. Although not already hypothesized a priori, a negative correlation between the SR scores and activation in the sub-gyral portion of the left superior frontal gyrus was observed during erotic stimulus processing.
SR-correlated activations during appetitive and aversive stimulus processing. Positively correlated activations with SR during the appetitive stimulus condition. On the other hand, our second hypothesis was not fully confirmed as no negative correlation was found between the SR scores and the BIS- and FFFS-related structures during aversive picture viewing.
However, negative correlations were obtained between the SR scores and activation in the areas that modulate the action of BIS-FFFS structures, like the left occipital cortex and the right lateral prefrontal cortex see Table 3 , Figure 4. SR-correlated activation during aversive stimulus viewing was not hypothesized and a whole-brain voxel-wise correlation only reported a significant related activation in the right claustrum.
Our overall results are shown in Table 3. Negatively correlated activations with SR during the aversive stimulus condition. Specifically, BAS sensitivity has been associated with stronger sexual arousability and excitability Aluja and Torrubia, ; Carpenter et al. This study has been designed to investigate the neural basis of these processes using a simple cognitive task in which emotional stimuli were presented as a background. We studied the processing of appetitive erotic and aversive stimuli presented as being secondary to a simple goal-directed task, which could affect the reported activations Lane et al.
At the same time, however, our paradigm was designed to ensure emotional stimulus perception. That is, the objective of the experiment was to present emotional pictures as a background to a main cognitive task, and to also ensure that the emotional processing was really done. As expected, brain activations during the erotic picture condition in all the participants activated several structures related to the BAS, such as the substantia nigra, the caudate, the putamen, the nucleus accumbens, the MPFC and the OFC.
Meanwhile, the aversive picture condition led to the activation of areas within the limbic system, such as the amygdala, the hippocampus and the posterior and anterior cingulates. Furthermore, other areas in the frontal lobes were activated during the erotic and aversive picture conditions, and are summarized in Tables 1 and 2.
These results agree with previous studies using erotic and aversive pictures see Phan et al. Recent research has specifically related the pleasantness rating, while the passive viewing of erotic pictures of the IAPS with the activation in the nucleus accumbens and the MPFC Sabatinelli et al. Knutson and Cooper related the MPFC to the reward evaluation processes which, in the case of erotic pictures, may relate to image post-processing and could impel action toward reward.
Even though the erotic pictures activated the striatum for the overall study sample, this activation did not correlate with the SR scores. These data contrasted with a recently published study involving 12 participants that analyzed brain activation while passively viewing pictures of appetizing and bland foods Beaver et al.
Appetizing foods, unlike bland ones, activated the ventral striatum, the orbitofrontal cortex, the amygdala and the ventral tegmental areas, and these activations correlated positively with the BAS scores. However, there was a clear difference between both studies as all the subjects rated the erotic pictures presented in our study as highly pleasant mean pleasantness was 7.
Otherwise, the relationship between the BAS scores and activation in the striatum may reflect different sensitivity to appetitive stimuli, whereas the correlation between the BAS scores and MPFC activation could relate more to the post-processing of these stimuli. In fact, Hahn et al. The analysis based on regions-of-interest ROIs of this study Hahn et al.
Radiologia Básica -2ª Ed (LANGE)
The reinforcement sensitivity theory RST proposed the behavioral activation system BAS as a neurobehavioral system that is dependent on dopamine-irrigated structures and that mediates the individual differences in sensitivity and reactivity to appetitive stimuli associated with BAS-related personality traits. Theoretical developments propose that high BAS sensitivity is associated with both enhanced appetitive stimuli processing and the diminished processing of aversive stimuli. The objective of this study was to analyze how individual differences in BAS functioning were associated with brain activation during erotic and aversive picture processing while subjects were involved in a simple goal-directed task. Forty-five male participants took part in this study. The task activation results confirm the activation of the reward and punishment brain-related structures while viewing erotic and aversive pictures, respectively.