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Neural substrates of individual differences in human fear learning: evidence from concurrent fMRI, fear-potentiated startle, and US-expectancy data.

van Well S, Visser RM, Scholte HS, Kindt M - Cogn Affect Behav Neurosci (2012)

Bottom Line: Fear learning was evident from the differential expressions of fear (CS(+) > CS(-)) at both the behavioral level (startle potentiation and US expectancy) and the neural level (in amygdala, anterior cingulate cortex, hippocampus, and insula).We examined individual differences in discriminative fear conditioning by classifying participants (as conditionable vs. unconditionable) according to whether they showed successful differential startle potentiation.This revealed that the individual differences in the emotional expression of discriminative fear learning (startle potentiation) were reflected in differential amygdala activation, regardless of the cognitive expression of fear learning (CS-US contingency or hippocampal activation).

View Article: PubMed Central - PubMed

Affiliation: University of Amsterdam, Amsterdam, The Netherlands.

ABSTRACT
To provide insight into individual differences in fear learning, we examined the emotional and cognitive expressions of discriminative fear conditioning in direct relation to its neural substrates. Contrary to previous behavioral-neural (fMRI) research on fear learning--in which the emotional expression of fear was generally indexed by skin conductance--we used fear-potentiated startle, a more reliable and specific index of fear. While we obtained concurrent fear-potentiated startle, neuroimaging (fMRI), and US-expectancy data, healthy participants underwent a fear-conditioning paradigm in which one of two conditioned stimuli (CS(+) but not CS(-)) was paired with a shock (unconditioned stimulus [US]). Fear learning was evident from the differential expressions of fear (CS(+) > CS(-)) at both the behavioral level (startle potentiation and US expectancy) and the neural level (in amygdala, anterior cingulate cortex, hippocampus, and insula). We examined individual differences in discriminative fear conditioning by classifying participants (as conditionable vs. unconditionable) according to whether they showed successful differential startle potentiation. This revealed that the individual differences in the emotional expression of discriminative fear learning (startle potentiation) were reflected in differential amygdala activation, regardless of the cognitive expression of fear learning (CS-US contingency or hippocampal activation). Our study provides the first evidence for the potential of examining startle potentiation in concurrent fMRI research on fear learning.

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US-expectancy ratings: Percentages of responses in each of the three response categories (i.e., certainly shock, maybe, and no shock) for the (a) fear-conditioned (CS+) and (b) control (CS–) stimuli
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Fig3: US-expectancy ratings: Percentages of responses in each of the three response categories (i.e., certainly shock, maybe, and no shock) for the (a) fear-conditioned (CS+) and (b) control (CS–) stimuli

Mentions: Figure 3 shows the US-expectancy data over the course of fear acquisition for both CSs separately. To analyze learning-related changes in CS–US contingency, the ordinal US-expectancy ratings were collapsed across the CS+ and CS– into three categories: (1) aware of CS–US association (i.e., CS+ = certainly shock and CS– = no shock), (2) uncertain CS–US association (i.e., CS+ = certainly shock and CS– = maybe shock, or CS+ = maybe shock and CS– = no shock), and (3) not aware of CS–US association (i.e., all remaining combinations of CS–US expectancies). Given that our ordinal data do not allow us to calculate the means over the first two and the last two acquisition trials (cf. startle data), we analyzed early versus late acquisition by comparing Trial 1 with Trial 8. As expected, the results of Friedman’s test revealed a significant change in participants’ CS–US expectancy between early and late acquisition [χ2(1, N = 40) = 34.0, p < .001, W = .85].Fig. 3


Neural substrates of individual differences in human fear learning: evidence from concurrent fMRI, fear-potentiated startle, and US-expectancy data.

van Well S, Visser RM, Scholte HS, Kindt M - Cogn Affect Behav Neurosci (2012)

US-expectancy ratings: Percentages of responses in each of the three response categories (i.e., certainly shock, maybe, and no shock) for the (a) fear-conditioned (CS+) and (b) control (CS–) stimuli
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3400034&req=5

Fig3: US-expectancy ratings: Percentages of responses in each of the three response categories (i.e., certainly shock, maybe, and no shock) for the (a) fear-conditioned (CS+) and (b) control (CS–) stimuli
Mentions: Figure 3 shows the US-expectancy data over the course of fear acquisition for both CSs separately. To analyze learning-related changes in CS–US contingency, the ordinal US-expectancy ratings were collapsed across the CS+ and CS– into three categories: (1) aware of CS–US association (i.e., CS+ = certainly shock and CS– = no shock), (2) uncertain CS–US association (i.e., CS+ = certainly shock and CS– = maybe shock, or CS+ = maybe shock and CS– = no shock), and (3) not aware of CS–US association (i.e., all remaining combinations of CS–US expectancies). Given that our ordinal data do not allow us to calculate the means over the first two and the last two acquisition trials (cf. startle data), we analyzed early versus late acquisition by comparing Trial 1 with Trial 8. As expected, the results of Friedman’s test revealed a significant change in participants’ CS–US expectancy between early and late acquisition [χ2(1, N = 40) = 34.0, p < .001, W = .85].Fig. 3

Bottom Line: Fear learning was evident from the differential expressions of fear (CS(+) > CS(-)) at both the behavioral level (startle potentiation and US expectancy) and the neural level (in amygdala, anterior cingulate cortex, hippocampus, and insula).We examined individual differences in discriminative fear conditioning by classifying participants (as conditionable vs. unconditionable) according to whether they showed successful differential startle potentiation.This revealed that the individual differences in the emotional expression of discriminative fear learning (startle potentiation) were reflected in differential amygdala activation, regardless of the cognitive expression of fear learning (CS-US contingency or hippocampal activation).

View Article: PubMed Central - PubMed

Affiliation: University of Amsterdam, Amsterdam, The Netherlands.

ABSTRACT
To provide insight into individual differences in fear learning, we examined the emotional and cognitive expressions of discriminative fear conditioning in direct relation to its neural substrates. Contrary to previous behavioral-neural (fMRI) research on fear learning--in which the emotional expression of fear was generally indexed by skin conductance--we used fear-potentiated startle, a more reliable and specific index of fear. While we obtained concurrent fear-potentiated startle, neuroimaging (fMRI), and US-expectancy data, healthy participants underwent a fear-conditioning paradigm in which one of two conditioned stimuli (CS(+) but not CS(-)) was paired with a shock (unconditioned stimulus [US]). Fear learning was evident from the differential expressions of fear (CS(+) > CS(-)) at both the behavioral level (startle potentiation and US expectancy) and the neural level (in amygdala, anterior cingulate cortex, hippocampus, and insula). We examined individual differences in discriminative fear conditioning by classifying participants (as conditionable vs. unconditionable) according to whether they showed successful differential startle potentiation. This revealed that the individual differences in the emotional expression of discriminative fear learning (startle potentiation) were reflected in differential amygdala activation, regardless of the cognitive expression of fear learning (CS-US contingency or hippocampal activation). Our study provides the first evidence for the potential of examining startle potentiation in concurrent fMRI research on fear learning.

Show MeSH
Related in: MedlinePlus