Incongruent Abstract Stimulus–Response Bindings Result in Response Interference: fMRI and EEG Evidence from Visual Object Classification Priming

Abstract

Stimulus repetition often leads to facilitated processing, resulting in neural decreases (repetition suppression) and faster RTs (repetition priming). Such repetition-related effects have been attributed to the facilitation of repeated cognitive processes and/or the retrieval of previously encoded stimulus-response (S-R) bindings. Although previous research has dissociated these two forms of learning, their interaction in the brain is not fully understood. Utilizing the spatial and temporal resolutions of fMRI and EEG, respectively, we examined a long-lag classification priming paradigm that required response repetitions or reversals at multiple levels of response representation. We found a repetition effect in occipital/temporal cortex (fMRI) that was timelocked to stimulus onset (EEG) and robust to switches in response, together with a repetition effect in inferior pFC (fMRI) that was time-locked to response onset (EEG) and sensitive to switches in response. The response-sensitive effect occurred even when changing from object names (words) to object pictures between repetitions, suggesting that S-R bindings can code abstract representations of stimuli. Most importantly, we found evidence for interference effects when incongruent S-R bindings were retrieved, with increased neural activity in inferior pFC, demonstrating that retrieval of S-R bindings can result in facilitation or interference, depending on the congruency of response between repetitions.

Object identification leads to a conceptual broadening of object representations in lateral prefrontal cortex

“…Dobbins et al (2004) found that changing the task being performed on a visual object picture from initial exposure (“bigger than a shoebox?”) to later exposure (“smaller than a shoebox?”) reduced repetition priming and repetition suppression in left lateral frontal cortex and eliminated repetition suppression in the left fusiform gyrus, with the largest covariation between repetition suppression and priming magnitudes across this manipulation occurring in the left lateral frontal cortex. This is the likely explanation as to why we failed to observe significant repetition suppression to the anchor stimuli in left lateral frontal cortex in the current experiment, changing the task from picture naming in the pre-fMRI session to man-made object detection during fMRI (see also Horner, 2012; Horner & Henson, 2008, 2012; Wig et al, 2009; Race et al, 2009, 2010, for further discussion). The alteration in repetition suppression and priming with a task change is what led Dobbins et al (2004) to propose that the left lateral frontal cortex in the territory of the inferior frontal junction is responsible for binding together particular stimuli with particular responses in a certain task, an idea recently reviewed and elaborated by Henson, Horner and colleagues (Henson et al, 2014).…”

“…Experience with visual objects commonly leads to improved behavioral identification in terms of speed and accuracy, referred to as “repetition priming”, while neural activity measured in BOLD fMRI in humans or in single-cell recording experiments in monkeys commonly decreases, referred to as “repetition suppression” (see Gotts et al, 2012a; Henson et al, 2014, for recent reviews). These joint behavioral and neural phenomena are relatively automatic, long-lasting, and occur generally across a wide range of task contexts and sensory and motor modalities, although the matching of study and test contexts leads to the largest and most robust effects (for discussion, see Dobbins et al, 2004; Horner & Henson, 2008, 2012; Wig et al, 2009; Race et al, 2009, 2010). The simultaneous observation of improved identification with decreased neural activity clearly indicates some form of improved neural information processing efficiency, yet the precise form of this efficiency remains unclear.…”

Baroreceptor activity impacts upon controlled but not automatic distractor processing

“…That is, studies on repetition suppression, a potential CNS-based correlate of behavioral priming (Grill-Spector, Henson, & Martin, 2006), point to ventrolateral regions of the PFC, namely the left posterior and left inferior PFC, to be involved in the retrieval of previously formed S-R bindings (Dobbins, Schnyer, Verfaellie, & Schacter, 2004;Horner & Henson, 2008). Moreover, the left dorsal premotor cortex (PMd) and right inferior frontal gyrus are assumed to reflect the retrieval of S-R bindings (Horner & Henson, 2012;Race, Shanker, & Wagner, 2008). Interestingly, the left presupplementary motor area, and the PMd, areas involved in the selection, preparation, and control of movement (Kennerley, Sakai, & Rushworth, 2004;van Gaal, Scholte, Lamme, Fahrenfort, & Ridderinkhof, 2011;Yamagata, Nakayama, Tanji, & Hoshi, 2012), are in fact related to S-R learning (Race et al, 2008) but neither to NP nor have they been found to be modulated by baroreceptor loading or unloading (Kimmerly et al, 2005).…”

The temporal dynamics of visual object priming

“…Although we have focused on contrasting a parallel processing hypothesis with a serial stage hypothesis, a third interaction hypothesis deserves mention in the context of investigating the late-stage activity related to priming (Horner & Henson, 2012; Henson et al, 2014). The neural mechanisms of sharpening and S-R retrieval may proceed in parallel but their outputs may converge at a common decision-making process.…”

“…We anticipated difficulty in capturing this late stage activity with the traditional method of time-locked the ERP to a stimulus onset, since such processing could be masked by the temporal misalignment of response-based activity related to primed (Studied and Exemplar) and unprimed (Unstudied) items. Therefore, we examined response-locked ERPs to examine late stage activity (Horner & Henson, 2012). …”