Academic journal article Cognitive, Affective and Behavioral Neuroscience

Neural Substrates of Individual Differences in Human Fear Learning: Evidence from Concurrent fMRI, Fear-Potentiated Startle, and US-Expectancy Data

Academic journal article Cognitive, Affective and Behavioral Neuroscience

Neural Substrates of Individual Differences in Human Fear Learning: Evidence from Concurrent fMRI, Fear-Potentiated Startle, and US-Expectancy Data

Article excerpt

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 behavioral0 neural (fMRI) research on fear learning0in which the emotional expression of fear was generally indexed by skin conductance0we used fear0potentiated startle, a more reliable and specific index of fear. While we obtained concurrent fear0potentiated startle, neuroimaging (fMRI), and USexpectancy data, healthy participants underwent a fearconditioning paradigm in which one of two conditioned stimuli (CS+ but not CS0) was paired with a shock (unconditioned stimulus [US]). Fear learning was evident from the differential expressions of fear (CS+ > CS0) 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 (CS0US contingency or hippocampal activation). Our study provides the first evidence for the potential of examining startle potentiation in concurrent fMRI research on fear learning.

Keywords Discriminative fear learning . Fear0potentiated startle . fMRI . Amygdala . Hippocampus . Deconvolution . Individual differences . Anxiety

(ProQuest: ... denotes formulae omitted.)

According to general consensus, emotional memory involves multiple systems that can be distinguished in terms of the information that they process, the ways that they operate, and the brain systems that they depend on (LaBar & Cabeza, 2006; Squire, 2004). Although these independent memory systems generally converge to guide behavior, they may occasionally diverge (see, e.g., LaBar & Cabeza, 2006). Spiderphobic patients, for example, usually know that most spiders are harmless (declarative memory), but the encounter of a spider may nevertheless elicit an autonomic fear response (nondeclarative memory). Human fear conditioning has proven to be an excellent paradigm for the study of the independent but interrelated cognitive (e.g., contingency awareness and US-expectancy ratings) and emotional (e.g., fear0potentiation startle responding) expressions of fear learning (e.g., Hamm& Weike, 2005; Soeter & Kindt, 2010; Weike, Hamm, Schupp, Runge, Schroeder & Kessler, 2005). Indeed, brain lesion and functional magnetic resonance imaging (fMRI) studies have suggested a double dissociation between the cognitive and emotional expressions of fear learning relative to hippocampal and amygdala activation (Bechara, Tranel, Damasio, Adolphs, Rockland & Damasio, 1995; LaBar & Cabeza, 2006; LaBar, LeDoux, Spencer, & Phelps, 1995; Phelps, 2004).

In previous fMRI studies on human fear learning, skin conductance responding (SCR) has been considered to reflect the emotional expression of fear. Most of these studies showed a relationship between conditioned SCR and amygdala activity (e.g., Cheng, Knight, Helmstetter, & Smith, 2006; Cheng, Richards, & Helmstetter, 2007; Knight, Nguyen, & Bandettini, 2005; LaBar, Gatenby, Gore, LeDoux, & Phelps, 1998). There are, however, indications that SCR is a less specific and less reliable index of autonomic fear responding than is startle eyeblink potentiation (measured by electromyography [EMG]). In fact, behavioral studies have suggested that startle potentiation dissociates more strongly from the cognitive expression of fear learning than does SCR (e.g., Hamm & Weike, 2005; Soeter & Kindt, 2010; Weike et al. …

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