Elsevier

NeuroImage

Volume 50, Issue 2, 1 April 2010, Pages 717-726
NeuroImage

Loss of control during instrumental learning: A source localization study

https://doi.org/10.1016/j.neuroimage.2009.12.094Get rights and content

Abstract

This study used multi-channel electroencephalography (EEG) to investigate cortical correlates of response-outcome contingency appraisal as indexed by the postimperative negative variation (PINV) during instrumental learning. PINV data were subjected to standardized low resolution brain electromagnetic tomography (sLORETA) for source localization. Forty-six healthy adult persons underwent a forewarned S1–S2 paradigm where response-outcome contingencies varied in three consecutive conditions. Initially subjects could control aversive stimulation by a correct behavioral response followed by loss of control and subsequent restitution of control. Throughout the experiment, reaction times, errors, ratings of controllability, arousal, emotional valence and helplessness were assessed. Topographical EEG analyses showed that in particular frontal PINV magnitudes covaried with the experimental manipulation. Loss of control induced extensive response-outcome uncertainty accompanied by a fronto-central PINV maximum. sLORETA functional analyses of the PINV revealed that dependent on the experimental conditions frontal, temporal and parietal areas seem to be related to PINV formation. In particular during loss of control, between-conditions sLORETA comparisons found Brodmann Area 24 in the anterior cingulate cortex (ACC) to be associated with PINV generation, which was confirmed by correlational analyses. These results provide further evidence for the role of the ACC in detecting response conflict and its involvement in the generation of the PINV.

Introduction

Instrumental learning, i.e., learning about response-outcome contingencies is of fundamental significance in order to obtain rewarding outcomes and to prevent the organism from punishment by a specific response (Shanks, 1993). Mainly based on animal studies, there is broad evidence that lack of control over aversive events can cause functional and structural alterations at the neurocortical, neuroendocrinological, and neurochemical level (Maier and Watkins, 2005) and may contribute to psychopathological conditions such as major depression (Overmier, 2002). However, in humans only a few studies have examined cortical correlates of uncontrollability in the context of instrumental learning.

Most findings about brain regions involved in the processing of uncontrollability in humans come from electroencephalographic (EEG) measurements where lack of control was operationalized by exposing subjects either to inescapable aversive (noise or electrical) stimuli or unsolvable cognitive tasks. Fretska et al. (1999) and in a replication study Bauer et al. (2003) measured slow cortical potential (SCP) changes during blocks of solvable (control) followed by blocks of unsolvable (loss of control) items of a reasoning task. Both studies found a generalized positive SCP shift, which was pronounced over temporal recording sites and enhanced negativity at frontopolar sites during loss of control. Pooled data analysis for low resolution electromagnetic tomography (LORETA; Pascual-Marqui et al., 1994) showed activation in the anterior cingulate cortex (ACC) associated with the processing of uncontrollability. Especially Brodmann Area (BA) 24 was characterized by differential activity in persons who responded emotionally high versus low during loss of control. SCP studies further suggest that in particular the postimperative negative variation (PINV) represents cortical processes related to changing response-outcome contingencies. The standard paradigm consists of a warning stimulus (S1), which is followed by an imperative stimulus (S2) signaling the subject to give a behavioral response in order to escape from or avoid aversive stimulation (Rockstroh et al., 1989). S1–S2 presentation is typically accompanied by a sustained negative SCP shift, which is termed contingent negative variation (CNV; for a review see Rohrbaugh et al., 1986). In its early (post-S1) component the CNV has been linked to the alerting properties of the warning stimulus (Loveless and Sanford, 1974), whereas its late (pre-S2) component was found to indicate motor preparation and response planning (Brunia and van Boxtel, 2001). In healthy subjects the SCP typically returns to baseline after response execution. However, under conditions of response ineffectiveness or ambiguity, the SCP shows enhanced negativity in terms of the PINV subsequent to the motor response. Elbert et al. (1982) proposed that the PINV indicates a reappraisal mechanism for stored contingencies whenever learned response-outcome contingencies contradict current observations (see also Birbaumer et al., 1986). In forewarned S1–S2 paradigms enhanced PINV magnitudes have consistently been found over frontal and fronto-central recording sites during an unexpected change from control to uncontrollability (Delaunoy et al., 1978, Diener et al., 2009b, Elbert et al., 1982, Rockstroh et al., 1979) and during ambiguous response-outcome relations in general (Kathmann et al., 1990). Although these results preferentially point to frontal areas implicated in the processing of response-outcome contingencies, only preliminary evidence exists for the cortical generation of the PINV. Berg et al. (1996) reported initial dipole models by means of brain electric source analysis (BESA; Scherg, 1990) that implicate neuronal processes originating in fronto-temporal areas for PINV generation. In addition to the EEG studies reported above, only one further neuroimaging study investigated contingency change to uncontrollability in healthy persons. Using positron emission tomography (PET), Schneider et al. (1996) found an increase in regional cerebral blood flow (rCBF) in the hippocampus and a decrease in the mammillary bodies during solvable items in a reasoning task. For subsequent unsolvable items a decrease in rCBF was observed in hippocampal regions in contrast to increases in the mammillary bodies and the amygdalae.

Taken together, several EEG and one imaging study suggest that prefrontal regions including the ACC, and temporal regions – presumably including limbic structures such as the hippocampus, the amygdala, and the mammillary bodies – are responsive to loss of control after successful response-outcome contingency learning. However, only Bauer et al., 2003, Berg et al., 1996 reported cortical source analysis of EEG/SCP data indicative of a functional relevance of frontal and temporal regions during uncontrollability. In particular, only preliminary results exist for PINV generation (Berg et al., 1996) although this slow cortical potential has been identified as a valid index of response-outcome contingency reappraisal (Diener et al., 2009b, Elbert et al., 1982, Kathmann et al., 1990).

PINV abnormalities indicative of cortical dysfunctions under psychopathological conditions have been reported for several mental disorders such as Alzheimer-type dementia (Zappoli et al., 1991), epilepsy (Drake et al., 1997), schizophrenia (Eikmeier et al., 1993, Klein et al., 1996, Löw et al., 2000, Verleger et al., 1999, Wagner et al., 1996), schizotypal personality disorder (Klein et al., 1998), and major depression (Diener et al., 2009a, Thier et al., 1986, Bolz and Giedke, 1981). Especially studies of the PINV in schizophrenia point to the involvement of the working memory system for PINV generation. Klein et al. (1996) found that high working memory load during an S1–S2 paradigm resulted in enhanced PINV magnitudes in schizophrenic patients, suggesting that limited working memory capacities interfere with the acquisition and maintenance of reliable response-outcome contingencies accompanied by enhanced ambiguity. Elevated PINV magnitudes were also found in healthy subjects during working memory challenge (Löw et al., 2000). In this context, Rockstroh et al. (1997) emphasized that all tasks that have been found to invoke a PINV (in schizophrenic patients) depend highly on working memory functions, which are supposed to constitute the ‘bridge from perception to action across time’ (Fuster, 1989).

In the present study we conducted source analysis of multi-channel EEG data to determine the cortical generators of the PINV in a forewarned S1–S2 paradigm. As an extension of previous PINV studies that employed an S1–S2 paradigm, controllability over aversive stimulation was varied across three consecutive conditions: (a) initial control, (b) subsequent loss of control and (c) restitution of control. This factorial design allowed us to assess cortical functioning associated with both uncontrollability (during loss of control) and the consequences of uncontrollability (during restitution of control). Guided by the preliminary findings of Berg et al. (1996), we expected that neuronal activity in fronto-temporal areas might account for the generation of the PINV. Limbic input during uncontrollability as found by Schneider et al. (1996) also points to a possible involvement of temporal lobe structures. Moreover, in line with the findings of Bauer et al. (2003) and the appraisal processing features of the PINV, we hypothesized the ACC to be relevant for PINV generation. Numerous studies have found the ACC to play a key role for conflict monitoring (see Botvinick et al., 1999, Botvinick et al., 2001, Botvinick et al., 2004), and Van Veen et al. (2001) showed that the ACC is particularly activated during response conflict. Against this background, we generally assumed that the interaction of multiple brain areas rather than a single region account for PINV generation. The hypothesis of multiple brain areas involved in PINV generation is supported by the finding that high-level cognitive functions such as contingency appraisal recruit the working memory system (Baddeley, 1992, Baddeley, 2000, Fuster, 2000), which is essential to maintain and manipulate internal information and needs the interaction of several cerebral networks (Collette and Van der Linden, 2002).

Section snippets

Participants

Forty-six healthy adult persons (27 female) in the age range of 19–60 years (mean age 34.4 ± 12.8) and a mean of 12 ± 1.4 years of education were pooled from two previously published studies (Diener et al., 2009a, Diener et al., 2009b). Participants were examined using the Structured Clinical Interview for the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV, American Psychiatric Association, 1994) Axis I disorders (First et al., 1997). Exclusion criteria were: current or lifetime

Subjective ratings

Figure 1 shows the ratings of controllability, helplessness, emotional valence, and arousal during the experimental conditions. For controllability, a significant main effect of condition (F(2,45) = 24.95, P <  .001) indicated that subjects perceived high controllability during both initial control (t(45) = 6.65, P <  .001) and restitution of control (t(45) = 4.57, P <  .001) in contrast to loss of control. Furthermore, controllability ratings during restitution of control were slightly lower than during

Discussion

The present study focused on the cortical generation of the PINV as an index of cognitive processing provoked by changing response-outcome contingencies during instrumental learning. Prior research pointed to frontal regions including the ACC and temporal regions involved in the experience of loss of control after successful response-outcome contingency learning.

Conclusions

This study investigated the cortical generation of the PINV as a psychophysiological index of response-outcome appraisal during instrumental learning. In line with previous results, fronto-central PINV magnitudes were found to be enhanced when successful responses became ineffective during loss of control over aversive stimulation. Source localization analysis by sLORETA identified BA 24 in the anterior cingulate cortex to be involved in PINV generation. We conclude that response conflict

Acknowledgments

This work was supported by the Deutsche Forschungsgemeinschaft (SFB 636/D4) and the Marsilius Kolleg (Center for Advanced Study), University of Heidelberg, Germany. We gratefully acknowledge the valuable assistance of Elena Maininguer, Nicole Balz and Wencke Brusniak in data collection.

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