Elsevier

Neuropsychologia

Volume 43, Issue 9, 2005, Pages 1318-1328
Neuropsychologia

Effortless control: executive attention and conscious feeling of mental effort are dissociable

https://doi.org/10.1016/j.neuropsychologia.2004.11.024Get rights and content

Abstract

Recruitment of executive attention is normally associated to a subjective feeling of mental effort. Here we investigate the nature of this coupling in a patient with a left mesio-frontal cortex lesion including the anterior cingulate cortex (ACC), and in a group of comparison subjects using a Stroop paradigm. We show that in normal subjects, subjective increases in effort associated with executive control correlate with higher skin-conductance responses (SCRs). However, our patient experienced no conscious feeling of mental effort and showed no SCR, in spite of exhibiting normal executive control, and residual right anterior cingulate activity measured with event-related potentials (ERPs). Finally, this patient demonstrated a pattern of impaired behavior and SCRs in the Iowa gambling task—elaborated by Damasio, Bechara and colleagues—replicating the findings reported by these authors for other patients with mesio-frontal lesions. Taken together, these results call for a theoretical refinement by revealing a decoupling between conscious cognitive control and consciously reportable feelings. Moreover, they reveal a fundamental distinction, observed here within the same patient, between the cognitive operations which are depending on normal somatic marker processing, and those which are withstanding to impairments of this system.

Introduction

The involvement of the prefrontal cortex in the ability to engage executive control constitutes one of the fundamental results of cognitive neuroscience. Current research focuses on the respective roles of frontal lobe structures such as anterior cingulate cortex (ACC), dorso-lateral prefrontal cortex (DLPFC), or orbito-frontal cortex (OFC) in this general process of control. Most investigated aspects of control include conflict detection and estimation, executive control modulation and response selection processes. In particular, diverging theories stimulate experimental research on the precise role of ACC in control. One influential theory postulates that ACC is involved in conflict monitoring and serves as a regulator signaling to other executive regions such as DLPFC whether executive attention has to be reinforced or alleviated (Botvinick, Braver et al., 2001). Another theory attributes to ACC a more active function related to response selection, as illustrated by patients exhibiting dissociations between control abilities depending on the motor response modality (Turken & Swick, 1999).

Within this scientific context, we planned to explore control abilities in patient RMB, a 50-year-old woman presenting with a vast left mesio-frontal ischaemic lesion including the left ACC (Fig. 1). We were initially motivated by the perspective of describing control impairments likely to be found in such a patient, and then to test which theory would best account for them.

We designed a set of behavioral experiments using a simplified Stroop task in which, on each trial the subject had to respond according to the ink color of a color word (e.g. the word “red” written in green ink) (Stroop, 1935, Carter et al., 2000). Stroop trials can be sorted into two categories: congruent trials in which both the ink color and the word itself refer to the same response, and incongruent trials in which the subject has to focus his executive attention to select the relevant information (the ink color) and to inhibit the prepotent response associated with the irrelevant information (the printed color word). Incongruent trials are usually responded slower and with a greater subjective feeling of mental effort.

Our results section begins with a detailed description of patient RMB's performance in this Stroop task (Experiments 1–3). Unexpectedly, control abilities of patient RMB evaluated in various versions of this Stroop tasks were amazingly preserved, and no dissociation was observed between manual and vocal response modalities. Moreover, we could show the presence of an efficient dynamic regulation of control abilities as indexed by Gratton and proportion effects.

However, we accidentally discovered that she had lost entirely the ability to experience and report a feeling of mental effort normally present during this task. In order to better assess and describe this unexpected deficit, we designed a further set of experiments exploring subjective verbal and non-verbal report of mental effort during the Stroop task in patient RMB and in normals (Experiments 4–7).

Once we could establish the existence of a dissociation between preserved cognitive aspects of control on the one hand, and impaired consciously reportable feeling of mental effort on the other hand, we hypothesized that the spared right ACC might subtend preserved control. We tested this hypothesis by replicating one of the Stroop experiments while recording scalp event-related potentials (ERPs), and confirmed the implication of this unlesioned neural structure, by revealing a correlation between its activity and patient RMB's executive attention performance (Experiment 8).

Finally, given that mental effort is normally associated to a cortege of bodily or somatic markers, we checked if patient RMB's lack of mental effort was associated to an impairment of skin conductance response (SCR)—a well-known somatic marker—during the Stroop task, and during the perception of external emotional stimuli (Experiments 9–11).

Section snippets

Patient RMB

Miss RMB was a right-handed 50-year-old lady who suffered in 1993 from a subarachnoid haemorrhage complicated by a vasospasm in the left anterior cerebral artery territory. She was referred to one of us (L.N.) for mild memory complaint. In July 2002, physical neurological examination revealed only discrete motor frontal lobe symptoms such as bilateral Babinski sign and hyperactive tendon reflexes. Educational level was 4 years of universitary studies.

The ischaemic lesion encompassed the left

Stroop effects

We first tested patient RMB in a manual version of this basic Stroop task (Experiment 1). Analysis of correct trials showed the classical Stroop effect (F(1, 299) = 37.13; p < 10E−4; effect size = 120 ms: 707 ms on congruent trials versus 827 ms on incongruent trials). The Stroop effect was also present on error rates: patient RMB committed nine errors on a total number of 320 trials, only on incongruent trials.

Given that executive attention may show dissociable patterns according to the response

Discussion

Our behavioral and neurophysiological investigation of patient RMB revealed a novel dissociation between preserved conscious executive control, reflected in normal behavioral performance—including verbal and non-verbal reports of task monitoring—and residual ACC activity, and absence of any associated subjective feeling of mental effort. This lack of consciousness of mental effort coincided with a lack of bodily-mediated physiological responses indexing mental effort in healthy subjects. We

Acknowledgments

We thank patient RMB for her constant collaboration during testing, M. Chastanet for his technical assistance with the SCR device, K. Naccache and B. Laurent for helpful discussions, and Prof. David Milner and two anonymous referees. Supported by INSERM, The French Ministry for Research (Action Cognitique), and a centennial fellowship from the McDonnell foundation to S.D.

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