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Human fear conditioning and extinction in neuroimaging: a systematic review.

Sehlmeyer C, Schöning S, Zwitserlood P, Pfleiderer B, Kircher T, Arolt V, Konrad C - PLoS ONE (2009)

Bottom Line: On closer inspection, there is considerable variation in methodology and results between studies.However, some neuroimaging studies do not report these findings in the presence of methodological heterogeneities.Differences concerning experimental factors may partly explain the variance between neuroimaging investigations on human fear conditioning and extinction and should, therefore, be taken into serious consideration in the planning and the interpretation of research projects.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychiatry, University of Muenster, Muenster, Germany.

ABSTRACT
Fear conditioning and extinction are basic forms of associative learning that have gained considerable clinical relevance in enhancing our understanding of anxiety disorders and facilitating their treatment. Modern neuroimaging techniques have significantly aided the identification of anatomical structures and networks involved in fear conditioning. On closer inspection, there is considerable variation in methodology and results between studies. This systematic review provides an overview of the current neuroimaging literature on fear conditioning and extinction on healthy subjects, taking into account methodological issues such as the conditioning paradigm. A Pubmed search, as of December 2008, was performed and supplemented by manual searches of bibliographies of key articles. Two independent reviewers made the final study selection and data extraction. A total of 46 studies on cued fear conditioning and/or extinction on healthy volunteers using positron emission tomography or functional magnetic resonance imaging were reviewed. The influence of specific experimental factors, such as contingency and timing parameters, assessment of conditioned responses, and characteristics of conditioned and unconditioned stimuli, on cerebral activation patterns was examined. Results were summarized descriptively. A network consisting of fear-related brain areas, such as amygdala, insula, and anterior cingulate cortex, is activated independently of design parameters. However, some neuroimaging studies do not report these findings in the presence of methodological heterogeneities. Furthermore, other brain areas are differentially activated, depending on specific design parameters. These include stronger hippocampal activation in trace conditioning and tactile stimulation. Furthermore, tactile unconditioned stimuli enhance activation of pain related, motor, and somatosensory areas. Differences concerning experimental factors may partly explain the variance between neuroimaging investigations on human fear conditioning and extinction and should, therefore, be taken into serious consideration in the planning and the interpretation of research projects.

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Brain areas involved in aversive conditioning according to the modality of the US.Different brain areas (with at least unilateral activation during aversive conditioning) are plotted against the x-axis. The number of studies out of 46 studies per brain region is plotted against the y-axis, taking into account US modality, which is tactile in 33 studies (such as electrical shocks), auditory in nine studies (such as noise), olfactory in one study (such as odors), or visual in three studies (such as aversive pictures).
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pone-0005865-g003: Brain areas involved in aversive conditioning according to the modality of the US.Different brain areas (with at least unilateral activation during aversive conditioning) are plotted against the x-axis. The number of studies out of 46 studies per brain region is plotted against the y-axis, taking into account US modality, which is tactile in 33 studies (such as electrical shocks), auditory in nine studies (such as noise), olfactory in one study (such as odors), or visual in three studies (such as aversive pictures).

Mentions: Again, activation of the fear network was observed to be independent of US-modality. In spite of different USs, activations of the amygdala, ACC and insula were reported for every stimulus type. Of the 33 studies with tactile stimulation, fifteen found activation of the amygdala (e.g. [29]), ten of the ACC (e.g. [35]), and ten of the insular cortex (e.g. [39]). Other main activation foci for tactile stimuli concern the thalamus in seven (e.g. [46]), and the striatum in ten studies (e.g. [52]). Other regions such as the occipital cortex, motor or somatosensory cortices are also activated during tactile conditioning in 16 studies (e.g. [27], [35]). By contrast, the nine studies on auditory fear conditioning mainly report activation of the fear network, with emphasis on amygdala in seven (e.g. [31]), on ACC in five (e.g. [48]), and on insula in five studies (e.g. [41]). Moreover, activations of the motor or sensory cortices (e.g. auditory, occipital) are also apparent in five studies (e.g. [26]). The one study on olfactory conditioning mainly reports activations in amygdala, insula and orbitofrontal cortex (OFC) [37], areas that are also associated with the perception of disgust [70], [71]. All three studies on visual aversive conditioning reported activation of key fear areas such as the amygdala and ACC or the PCC [30], [40], [67]. Activation of the insula was found in two of the studies (e.g. [67]). Furthermore, activations of the DLPFC, OFC, thalamus, nucleus accumbens and the occipital cortex are apparent in these visual conditioning studies (e.g. [40]) (for details, see Figure 3).


Human fear conditioning and extinction in neuroimaging: a systematic review.

Sehlmeyer C, Schöning S, Zwitserlood P, Pfleiderer B, Kircher T, Arolt V, Konrad C - PLoS ONE (2009)

Brain areas involved in aversive conditioning according to the modality of the US.Different brain areas (with at least unilateral activation during aversive conditioning) are plotted against the x-axis. The number of studies out of 46 studies per brain region is plotted against the y-axis, taking into account US modality, which is tactile in 33 studies (such as electrical shocks), auditory in nine studies (such as noise), olfactory in one study (such as odors), or visual in three studies (such as aversive pictures).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2692002&req=5

pone-0005865-g003: Brain areas involved in aversive conditioning according to the modality of the US.Different brain areas (with at least unilateral activation during aversive conditioning) are plotted against the x-axis. The number of studies out of 46 studies per brain region is plotted against the y-axis, taking into account US modality, which is tactile in 33 studies (such as electrical shocks), auditory in nine studies (such as noise), olfactory in one study (such as odors), or visual in three studies (such as aversive pictures).
Mentions: Again, activation of the fear network was observed to be independent of US-modality. In spite of different USs, activations of the amygdala, ACC and insula were reported for every stimulus type. Of the 33 studies with tactile stimulation, fifteen found activation of the amygdala (e.g. [29]), ten of the ACC (e.g. [35]), and ten of the insular cortex (e.g. [39]). Other main activation foci for tactile stimuli concern the thalamus in seven (e.g. [46]), and the striatum in ten studies (e.g. [52]). Other regions such as the occipital cortex, motor or somatosensory cortices are also activated during tactile conditioning in 16 studies (e.g. [27], [35]). By contrast, the nine studies on auditory fear conditioning mainly report activation of the fear network, with emphasis on amygdala in seven (e.g. [31]), on ACC in five (e.g. [48]), and on insula in five studies (e.g. [41]). Moreover, activations of the motor or sensory cortices (e.g. auditory, occipital) are also apparent in five studies (e.g. [26]). The one study on olfactory conditioning mainly reports activations in amygdala, insula and orbitofrontal cortex (OFC) [37], areas that are also associated with the perception of disgust [70], [71]. All three studies on visual aversive conditioning reported activation of key fear areas such as the amygdala and ACC or the PCC [30], [40], [67]. Activation of the insula was found in two of the studies (e.g. [67]). Furthermore, activations of the DLPFC, OFC, thalamus, nucleus accumbens and the occipital cortex are apparent in these visual conditioning studies (e.g. [40]) (for details, see Figure 3).

Bottom Line: On closer inspection, there is considerable variation in methodology and results between studies.However, some neuroimaging studies do not report these findings in the presence of methodological heterogeneities.Differences concerning experimental factors may partly explain the variance between neuroimaging investigations on human fear conditioning and extinction and should, therefore, be taken into serious consideration in the planning and the interpretation of research projects.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychiatry, University of Muenster, Muenster, Germany.

ABSTRACT
Fear conditioning and extinction are basic forms of associative learning that have gained considerable clinical relevance in enhancing our understanding of anxiety disorders and facilitating their treatment. Modern neuroimaging techniques have significantly aided the identification of anatomical structures and networks involved in fear conditioning. On closer inspection, there is considerable variation in methodology and results between studies. This systematic review provides an overview of the current neuroimaging literature on fear conditioning and extinction on healthy subjects, taking into account methodological issues such as the conditioning paradigm. A Pubmed search, as of December 2008, was performed and supplemented by manual searches of bibliographies of key articles. Two independent reviewers made the final study selection and data extraction. A total of 46 studies on cued fear conditioning and/or extinction on healthy volunteers using positron emission tomography or functional magnetic resonance imaging were reviewed. The influence of specific experimental factors, such as contingency and timing parameters, assessment of conditioned responses, and characteristics of conditioned and unconditioned stimuli, on cerebral activation patterns was examined. Results were summarized descriptively. A network consisting of fear-related brain areas, such as amygdala, insula, and anterior cingulate cortex, is activated independently of design parameters. However, some neuroimaging studies do not report these findings in the presence of methodological heterogeneities. Furthermore, other brain areas are differentially activated, depending on specific design parameters. These include stronger hippocampal activation in trace conditioning and tactile stimulation. Furthermore, tactile unconditioned stimuli enhance activation of pain related, motor, and somatosensory areas. Differences concerning experimental factors may partly explain the variance between neuroimaging investigations on human fear conditioning and extinction and should, therefore, be taken into serious consideration in the planning and the interpretation of research projects.

Show MeSH
Related in: MedlinePlus