Elsevier

Brain Research Bulletin

Volume 54, Issue 3, February 2001, Pages 287-298
Brain Research Bulletin

Cortical networks for working memory and executive functions sustain the conscious resting state in man

https://doi.org/10.1016/S0361-9230(00)00437-8Get rights and content

Abstract

The cortical anatomy of the conscious resting state (REST) was investigated using a meta-analysis of nine positron emission tomography (PET) activation protocols that dealt with different cognitive tasks but shared REST as a common control state. During REST, subjects were in darkness and silence, and were instructed to relax, refrain from moving, and avoid systematic thoughts. Each protocol contrasted REST to a different cognitive task consisting either of language, mental imagery, mental calculation, reasoning, finger movement, or spatial working memory, using either auditory, visual or no stimulus delivery, and requiring either vocal, motor or no output. A total of 63 subjects and 370 spatially normalized PET scans were entered in the meta-analysis. Conjunction analysis revealed a network of brain areas jointly activated during conscious REST as compared to the nine cognitive tasks, including the bilateral angular gyrus, the left anterior precuneus and posterior cingulate cortex, the left medial frontal and anterior cingulate cortex, the left superior and medial frontal sulcus, and the left inferior frontal cortex. These results suggest that brain activity during conscious REST is sustained by a large scale network of heteromodal associative parietal and frontal cortical areas, that can be further hierarchically organized in an episodic working memory parieto-frontal network, driven in part by emotions, working under the supervision of an executive left prefrontal network.

Introduction

A large part of our daily mental activities are internalized, id est performed without external input or motor output, and not goal directed. During this particular state of consciousness, that is not to be confounded with arousal or perceptual consciousness, one is monitoring both somesthesic and vegetative information, such as sensations and body position, and experiencing association of free thoughts that deal with the recollection of past experiences, inner speech, mental images, emotions, planning of future activities, etc. This mental state has been referred to as a Random Episodic Silent Thinking (REST) state by previous authors [3], thereby emphasizing the unconstrained nature of this kind of thoughts, as opposed to a more focused and constrained sort of episodic memory activity when one is driven to search into his past history.

Despite the fact that assessing the exact mental content of a subject during REST is by essence difficult and must rely on introspection, which clearly constitutes a scientific limitation, there is a considerable interest in the study of the neural bases of the conscious resting state.

First, from a strict cognitive neuroscience point of view, it is important to try to establish whether or not a network of brain areas is specifically engaged during this mental state brain. If so, this would provide a strong argument favoring the “computational” nature of brain activity during REST [7] and, depending on the locations of these areas, insights regarding the major cognitive processes involved.

The answer to this question is also of primary importance for cognitive neuroimaging experiments, because conscious rest has been (and is still) widely used in the cognitive neuroimaging community as a reference state to which better controlled cognitive processes are contrasted. This is explicitly the case for positron emission tomography (PET) or functional magnetic resonance imaging (FMRI) experiments, in which local neural activity during conscious rest serves as a baseline for assessing hemodynamic variations during cognitive process execution. To some extent, it is also implicitly the case for event-related electroencephalography or magnetoencephalography experiments, because electrical/magnetic activity is generally compared to a baseline activity measured over the several tens/hundreds of milliseconds that precede stimulus presentation when the subject is in a state that resembles to conscious rest.

Although it is an ill-defined mental state, there are some good reasons for using conscious rest as a reference state in cognitive neuroimaging. First, it is applicable in all imaging experiments, as opposed to high level cognitive control tasks that have been used to test the involvement of a specific cognitive module, with the potential drawback of masking joint activations in both the reference and the task of interest [24]. As a matter of fact, differences in the reference conditions have been put forward in order to try to solve controversies regarding the putative brain network involved in identical tasks [38]. As such, the conscious resting state can serve as a common reference both within and between laboratory experiments. Second, the conscious resting state does not rely on a given sensory modality for stimulus delivery or on a specific kind of behavioral output. Third, its variability both within and across subjects has been shown to be of the same magnitude than any other cognitive task [14].

Studies on the cortical anatomy of the resting state have been first relying on the observation of the regional pattern of the glucose metabolic rate (rCMRGlu) or regional cerebral blood flow (rCBF) 14, 42, 55. These studies revealed brain areas of higher or lower metabolic/hemodynamic activity, provided figures of their local variability, but did not allow to uncover a specific network of brain areas involved during the resting state. A recent PET experiment compared rCMRGlu maps in healthy volunteers at REST to that of patients in a vegetative state [40], showing a widely distributed network of brain areas having higher neural activity during REST. A recent FMRI experiment has focused on the issue of the neural bases of the resting state, contrasting REST to auditory perceptual or semantic tasks [7]. A left hemisphere parieto-frontal network was found of equal activity during REST and the semantic task, but of reduced activity during the perceptual task, leading the authors to propose that mental activity during REST was of “conceptual processing” nature.

However, this claim remains to be formally demonstrated because it relied on simple contrast analysis (REST vs. tone, REST vs. semantic, etc.), concerned task involving the sole auditory modality, with possible unwanted interference of attentional process due to scanner noise, and was based on a somewhat limited sample size, which raises a sensitivity issue. One way of alleviating these limits could be through a meta-analysis of activation protocols in which a REST condition was used. The idea of using a meta-analysis to uncover process common to different tasks has been proposed and previously exploited by others 63, 64, 65, 66. In their approach, Shulman et al. reanalyzed a set of 9 PET experiments contrasting passive vs. active visual tasks, using activation map averaging in order to uncover processes that generalize across tasks. This approach has the potential drawback that it could reveal activation that would not necessarily be common to all protocols but rather driven by the strongest ones, with possibly reduced activity in some others. Actually, conjunction analysis appears as the optimal statistical approach of choice when trying to identify joint activations across protocols [57].

The present study was designed to alleviate some of the concerns raised by previous studies dealing with the neural bases of the conscious resting state. It combines the intrinsic power of meta-analysis, the specificity of conjunction analysis, and a variety of cognitive tasks to be contrasted to REST. Accordingly, a set of nine PET activation protocols performed in our laboratory over the past 3 years, all including REST as a control task, have been reanalyzed using conjunction analysis, searching for joint activation during REST as compared to a variety of cognitive tasks, including different stimulus presentation modalities, cognitive processes, and behavioral outputs.

Section snippets

Subjects

Sixty-three young healthy male volunteers participated to the study (22.0 ± 2.0 years, mean ± SD). All were right-handed as assessed by the Edinburgh questionnaire (88.1 ± 13.7; range, 50–100) and were free of brain abnormalities as assessed on their T1-weighted 3D MRI scan. All subjects gave their informed consent. The study was approved by the Basse-Normandie Ethic Committee.

Cognitive tasks

Each of the 63 subjects participated in one and only one of nine different activation protocols (see Table 1). Each

Behavioral observations

Among the 63 subjects that were included in the study, 41 properly answered the questionnaire dealing with their REST condition mental activity. Overall, a majority of subjects (56%) reported that mental events were partly dealing with autobiographic reminiscences, either recent or ancient, consisting of familiar faces, scenes, dialogs, stories, melodies, etc.

Inner speech and mental images were the most frequently reported types of mental events during REST. Ranking the occurrence of such

Discussion

The present meta-analysis uncovered a parieto-frontal network of brain areas that was more active during the resting condition than during a variety of cognitive tasks, independent of the modality in which the stimuli were delivered, of the type of cognitive activity, and of behavioral output. In the following we will, (1) argue that this network sustains processes active during REST rather than reflects deactivation processes common to all tasks, (2) discuss the similarities between this

Conclusion

The conscious resting state in humans is sustained by a large scale network of heteromodal associative parietal and frontal cortical areas, that can be further hierarchically organized in an episodic working memory parieto-frontal network, driven in part by emotions, working under the supervision of an executive prefrontal network. The bilateral angular gyrus and the anterior precuneus, parts of the parieto-frontal sub-network, appears to be specifically involved during REST and may reflect the

Acknowledgements

The authors are indebted to the Cyceron Cyclotron (P. Lochon, O. Tirel) and PET camera staff (V. Beaudoin, G. Perchey) for their invaluable help in acquiring the PET activation studies. The authors would also like to thank A. Mazard for her help in some of data acquisition. Parts of this work have been supported by grants from the GIS Sciences de la Cognition.

This work has been presented in part at the 5th International Conference on Functional Mapping of the Human Brain (Dusseldorf, Germany,

References (72)

  • C.J Price et al.

    Cognitive conjunctionA new approach to brain activation experiments

    Neuroimage

    (1997)
  • M.D Rugg et al.

    Neural correlates of memory retrieval during recognition memory and cued recall

    Neuroimage

    (1998)
  • J.D Schmahmann et al.

    Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space

    Neuroimage

    (1999)
  • L Zago et al.

    Functional anatomy of simple and complex mental calculation using PET

    Neuroimage

    (2001)
  • N.C Andreasen et al.

    Short-term and long-term verbal memoryA positron emission tomography study

    Proc. Natl. Acad. Sci. USA

    (1995)
  • N.C Andreasen et al.

    Remembering the pastTwo facets of episodic memory explored with positron emission tomography

    Am. J. Psychiatry

    (1995)
  • Andreasen, N. C.; O’Leary, D. S.; Cizadlo, T.; Arndt, S.; Rezai; Watkins, G. L.; Boles Ponto, L. L.; Hichwa, R. D. II....
  • A Bechara et al.

    Emotion, decision making and the orbitofrontal cortex

    Cereb. Cortex

    (2000)
  • A Bechara et al.

    Dissociation of working memory from decision making within the human prefrontal cortex

    J. Neurosci.

    (1998)
  • J.R Binder et al.

    Conceptual processing during the conscious resting stateA functional MRI study

    J. Cogn. Neurosci.

    (1999)
  • S Bricogne et al.

    Mental navigation within an environment learned from reading

    Neuroimage

    (1999)
  • R.L Buckner et al.

    Functional anatomical studies of explicit and implicit memory retrieval tasks

    J. Neurosci.

    (1995)
  • R.L Buckner et al.

    Functional anatomic studies of memory retrieval for auditory words and visual pictures

    J. Neurol. Sci.

    (1996)
  • S.A Bunge et al.

    A resource model of the neural basis of executive working memory

    Proc. Natl. Acad. Sci. USA

    (2000)
  • Cabeza, R.; Anderson, N. D.; Kester, J.; Lennartsson, E. R.; McIntosh, A. R. Involvement of prefrontal regions on...
  • R Cabeza et al.

    Imaging cognition IIAn empirical review of 275 PET and fMRI studies

    J. Cogn. Neurosci.

    (2000)
  • O.G Cameron et al.

    Changes in sensory-cognitive inputEffects on cerebral blood flow

    J. Cereb. Blood Flow Metab.

    (1990)
  • C.R Clark et al.

    Updating working memory for wordsA PET activation study

    Hum. Brain Mapp.

    (2000)
  • M D’Esposito et al.

    The neural substrate and temporal dynamics of interference effects in working memory as revealed by event-related functional MRI

    Proc. Natl. Acad. Sci. USA

    (1999)
  • O Etard et al.

    Picture naming without Broca and Wernicke’s area

    Neuroreport

    (1999)
  • G.R Fink et al.

    Cerebral representation of one’s own pastNeural networks involved in autobiographical memory

    J. Neurosci.

    (1996)
  • P Fiset et al.

    Brain mechanisms of propofol-induced loss of consciousness in humansA positron emission tomographic study

    J. Neurosci.

    (1999)
  • P.C Fletcher et al.

    Brain activity during memory retrieval. The influence of imagery and semantic cueing

    Brain

    (1996)
  • K.J Friston et al.

    Spatial registration and normalization of images

    Hum. Brain Mapp.

    (1995)
  • O Ghaem et al.

    Mental navigation along memorized routes activates the hippocampus, precuneus, and insula

    Neuroreport

    (1997)
  • P.M Grasby et al.

    Functional mapping of brain areas implicated in auditory-verbal memory function

    Brain

    (1993)
  • Cited by (0)

    View full text