The role of contingency awareness in single-cue human eyeblink conditioning

Abstract

Single-cue delay eyeblink conditioning is presented as a prototypical example of automatic, nonsymbolic learning that is carried out by subcortical circuits. However, it has been difficult to assess the role of cognition in single-cue conditioning because participants become aware of the simple stimulus contingency so quickly. In this experiment (n ¼ 166), we masked the contingency to reduce awareness. We observed a strong relationship between contingency awareness and conditioned responding, with both trace and delay procedures. This finding suggests that explicit associative knowledge and anticipatory behavior are regulated by a coordinated system rather than by functionally and neurally distinct systems.[Supplemental material is available for this article.]It is often claimed that Pavlovian conditioning is mediated by a functionally and neurally distinct system that developed early in evolution and has been preserved in humans. This system is considered to be independent of the cognitive system that underpins reasoning, language, and explicit "declarative" learning (e.g., Schacter and Tulving 1994; Squire 1994;Eichenbaum and Cohen 2001). Although several variations of this approach have been proposed in the learning and memory literature, they will collectively be referred to as the "dual-system" model. The principal alternative is a single system model in which one integrated learning system gives rise to both conscious declarative knowledge and conditioned behavior (e.g., Mitchell et al. 2009). The predictions of the dual-system model can be seen clearly in the case of eyeblink conditioning, often considered to be a prototypical Pavlovian procedure (Squire 1987).In human eyeblink conditioning, a conditioned stimulus (CS) such as a tone is paired with an unconditioned stimulus (US), usually an airpuff to the eye. After several pairings, the CS acquires the ability to elicit anticipatory eyeblink responses (conditioned responses, CRs). In differential conditioning, a second CS, such as white noise, is presented in the absence of the US in order to provide a within-participant control. In addition to recording eyeblink responses, it is also possible to assess the conscious, explicit knowledge acquired by participants. The dual-system model predicts that CRs will develop regardless of whether the participant has explicit awareness of the contingency between the CS and the US. It also predicts that cognitive load or misleading instructions will selectively impair the cognitive system but leave the conditioning system, and hence CRs, largely unaffected.The strongest evidence for the dual-system model comes from research carried out by Squire's group. Squire (1998, 1999) and Smith et al. (2005) found that participants classified as unaware of a differential contingency in a post-experimental questionnaire nonetheless showed differential eyeblink CRs. However, they only observed this pattern when they used a delay conditioning procedure, in which the CS and US overlap in time. Participants conditioned with a tra...

The role of working memory and declarative memory in trace conditioning

“…Thus, differential conditioning, which is more difficult than single-cue conditioning, may be more dependent on awareness (LaBar & Disterhoft, 1998). However, using a false pretense masking task, involving reporting letter cues at a similar volume as CS volume, awareness was found to be critical for acquisition of both delay and trace single-cue eyeblink conditioning (Weidemann, Best, Lee, & Lovibond, 2013). Therefore, while trace conditioning appears to critically depend on awareness, data regarding the role of awareness in delay conditioning appears more equivocal.…”

Contingency awareness as a prerequisite for differential contextual fear conditioning

“…Single-cue conditioning produces only very few unaware subjects, whereas more complex conditioning schemes such as differential conditioning (where one stimulus -CS+is associated with the US while the other -CS-is not) prevent more subjects from becoming aware (Carter et al, 2003). The question whether declarative knowledge of the relationship between CS und US is necessary for successful conditioning has sparked a considerable debate amongst scientists Lovibond, Liu, Weidemann, & Mitchell, 2011;Lovibond & Shanks, 2002;Manns et al, 2002;Mitchell, De Houwer, & Lovibond, 2009;Schultz & Helmstetter, 2010;Smith, Clark, Manns, & Squire, 2005;Weidemann, Best, Lee, & Lovibond, 2013).…”

Contingency Awareness Shapes Acquisition and Extinction of Emotional Responses in a Conditioning Model of Pain-Related Fear

“…Our data therefore extend evidence from fear conditioning studies actively manipulating contingency awareness, which question the assumption of explicit knowledge about cue-outcome contingencies as a prerequisite in human aversive learning (Knight et al, 2006 ; Schultz and Helmstetter, 2010 ; Raio et al, 2012 ). Unlike approaches actively manipulating contingency awareness to create groups with full vs. no contingency awareness through masking (Knight et al, 2006 , 2009 ; Weidemann et al, 2013 ), explicit instructions and/or distraction (Klucken et al, 2009 ; Schultz and Helmstetter, 2010 ; Tabbert et al, 2011 ) we herein addressed contingency accuracy developed “naturally” over the course of differential learning. While our findings may not generalize to results in individuals fully unaware of CS-US contingencies, varying manifestations of differentially acquired contingency accuracy appear closer to clinical reality in chronic pain patients.…”

“…Contingency awareness was accordingly conceptualized as a mediator between associative learning and the display of conditioned responses (Lovibond, 2003 , 2004 ). In support of this notion, several human studies reliably observed conditioned responses in perceived CS valence and in physiological changes of skin conductance responses in aware subjects only, suggesting that contingency awareness is necessary for successful fear conditioning (Lovibond and Shanks, 2002 ; Tabbert et al, 2006 , 2011 ; Klucken et al, 2009 ; Mitchell et al, 2009 ; Lovibond et al, 2011 ; Weidemann and Antees, 2012 ; Weidemann et al, 2013 ). However, others have questioned this assumption given evidence that autonomic fear responses also occur without explicit knowledge regarding contingencies (Wiens and Öhman, 2002 ; Smith et al, 2005 ; Knight et al, 2006 , 2009 ; Schultz and Helmstetter, 2010 ; Raio et al, 2012 ).…”