CR expression is typically taken as evidence of associative learning in behavioral and fMRI studies of Pavlovian conditioning. However, the present findings indicate that UCR diminution can also serve as evidence that the CS-UCS association has been formed. In the present study, CS perception was monitored on a trial-by-trial basis, and behavioral and fMRI data were subsequently grouped into perceived and unperceived trial types. UCS expectancy ratings were higher to perceived than unperceived CS+ presentations, indicating that participants expected the UCS on perceived trials, but were uncertain of UCS presentation on unperceived trials. Further, unconditioned SCRs were larger to UCS presentations that followed the unperceived versus perceived CS+. These findings demonstrate unconditioned SCR diminution during Pavlovian conditioning, and generally support the view that UCS expectancies influence UCR production (Dunsmoor et al., 2008
; Rust, 1976
). The influence of conscious UCS expectancies on UCR magnitude was further investigated by comparing the change in unconditioned SCRs in relation to the UCS expectancy ratings that were reported on each conditioning trial. These data demonstrated that unconditioned SCR magnitude decreased as UCS expectancy increased (see ), providing further evidence that conscious UCS expectancies modulate the behavioral UCRs produced during Pavlovian conditioning.
UCR diminution was also demonstrated within the fMRI signal from several brain regions. Learning-related changes in UCR activity were observed within the ventromedial PFC, dorsomedial PFC, dorsolateral PFC, inferior parietal lobe, posterior cingulate, and insula. The UCRs within the ventromedial PFC and posterior cingulate cortex were modulated by CS perception. Functional MRI signal responses within these brain regions were larger when the UCS followed the unperceived compared to the perceived CS+ (). UCR magnitude within the dorsomedial PFC, dorsolateral PFC, inferior parietal lobe, and insula varied with UCS expectancy. As UCS expectancy increased, activity within these brain regions decreased (see ). These findings suggest that conscious UCS expectancies modulate UCR magnitude within these brain areas. Further, these imaging findings mirrored the behavioral data (see ) that showed UCS expectancies modulate unconditioned SCR expression. These findings are consistent with prior work demonstrating UCR diminution in human brain activity (Dunsmoor et al., 2008
The similarity of learning-related behavioral and fMRI signal responses suggests that brain regions such as the dorsomedial and dorsolateral PFC may mediate the diminution of unconditioned behavioral responses. Therefore, unconditioned fMRI data were sorted in relation to participants’ SCR magnitude to determine the role of these brain regions in the diminution of unconditioned SCRs. Activity within the dorsomedial PFC, dorsolateral PFC, and insula showed a linear relationship with unconditioned SCR amplitude (see ), suggesting that these brain regions influence the expression of unconditioned SCRs. These findings are consistent with prior work demonstrating a relationship between SCR production and neural activity within each of these brain regions (Critchley et al., 2000
; Knight et al., 2005
; Patterson et al., 2002
). The findings from the present study suggest that UCS expectancies modulate unconditioned fMRI responses within prefrontal brain regions, and in turn, these brain regions provide top-down modulation of behavioral responses (e.g. SCR) to aversive stimuli.
A number of previous studies have suggested that regions of the prefrontal cortex play a role in error detection (Carter et al., 1998
). The pattern of activation observed within this region in the present study is generally consistent with suggestions that prefrontal activity increases when errors are likely to be made (Carter et al., 1998
; Wittfoth et al., 2009
). Specifically, dorsomedial and dorsolateral PFC activity was larger on trials that participants reported the lowest UCS expectancy ratings, and thus made the largest UCS prediction errors. To determine whether the observed PFC activity was driven by UCR diminution or error detection we also analyzed the data from CS− trials. If a linear relationship between UCS expectancy and the fMRI signal following CS− presentation were demonstrated, the findings would be consistent with the view that error detection produced the PFC activity observed in this study. However, the analysis of these data determined that the fMRI signal on CS− trials did not vary with UCS expectancy (see supplemental Figure 2
). These findings indicate the reduction in UCR magnitude observed within the PFC in the present study is better explained by UCR diminution than an error detection-related process.
The acoustic noise associated with fMRI served as an auditory mask that limited CS perception in the present study. Although, the perception of auditory stimuli may be mediated by somewhat different mechanisms in silent compared to noise-filled environments, the pattern of activation we observed within the dorsomedial PFC, dorsolateral PFC, inferior parietal lobe, and insula generally replicates prior UCR diminution work that has not modulated auditory CS perception (Dunsmoor et al., 2008
). However, this prior UCR diminution research has also reported learning-related changes within the amygdala during Pavlovian conditioning (Dunsmoor et al., 2008
). We did not observe similar changes within this region in the present study, even when more lenient threshold criteria were applied. Prior work suggests the amygdala is an important component of the neural circuit that mediates fear learning and memory processes (Büchel et al., 1998
; Cheng et al., 2003
; Knight et al., 2005
; LaBar et al., 1998
; Tabbert et al., 2005
). Further, amygdala activity typically shows both a CR and UCR during fMRI studies of Pavlovian conditioning. However, the amygdala is more active during CR, than UCR expression (Knight et al., 2005
). Further, amygdala damage disrupts CR, but not UCR production (Bechara et al., 1995
). These findings suggest the amygdala may be more important for the production of the CR than the UCR. If so, the amygdala may not be a critical component of the neural circuit that mediates UCR diminution. However, an alternative explanation is that learning-related reductions in UCR amplitude may have developed within the amygdala on both perceived and unperceived conditioning trials. Prior work has shown that both perceived and unperceived CS+ presentations can produce learning-related CRs within the amygdala (Knight et al., 2009
; Morris et al., 1998
). Therefore, it is possible that amygdala UCRs were equally diminished to UCS presentations following the perceived and unperceived CS+. To investigate this possibility we compared CR and UCR magnitude within the amygdala. No relationship was demonstrated between these responses, suggesting that amygdala CRs do not directly modulate amygdala UCRs. However, these findings do not rule out the possibility that other brain regions modulate UCRs within the amygdala. These issues should be investigated further in future studies by including presentations of the UCS alone. Presentations of the UCS alone were not included in the present study. Therefore we cannot determine if UCR diminution occurred on both perceived and unperceived CS+ trials, or whether instead UCR diminution simply did not occur within this region of the brain. However, the inclusion of a UCS alone condition would help to determine whether amygdala UCRs are equally diminished on both trial types in future studies.
The present study investigated learning-related decreases in UCR magnitude (i.e. UCR diminution) that develop during Pavlovian conditioning. UCS expectancy, fMRI signal, and SCR expression were monitored as supra and sub-threshold auditory CS presentations were paired with a UCS. UCR diminution was observed within several brain regions associated with fear learning and memory including the ventromedial PFC, dorsomedial PFC, dorsolateral PFC, insula, posterior cingulate, and inferior parietal lobe. Activity within a subset of these brain regions showed an inverse relationship with UCS expectancy ratings, such that as UCS expectancy increased UCR magnitude within the dorsomedial and dorsolateral PFC decreased. Further, activity within the dorsomedial and dorsolateral PFC showed a linear relationship with unconditioned SCR expression. These findings suggest that UCS expectancies modulate prefrontal cortex responses to aversive stimuli. In turn, prefrontal activity appears to modulate the expression of unconditioned SCRs.