Posterior cingulate, precuneal and retrosplenial cortices: cytology and components of the neural network correlates of consciousness

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Abstract

Neuronal aggregates involved in conscious awareness are not evenly distributed throughout the CNS but comprise key components referred to as the neural network correlates of consciousness (NNCC). A critical node in this network is the posterior cingulate, precuneal, and retrosplenial cortices. The cytological and neurochemical composition of this region is reviewed in relation to the Brodmann map. This region has the highest level of cortical glucose metabolism and cytochrome c oxidase activity. Monkey studies suggest that the anterior thalamic projection likely drives retrosplenial and posterior cingulate cortex metabolism and that the midbrain projection to the anteroventral thalamic nucleus is a key coupling site between the brainstem system for arousal and cortical systems for cognitive processing and awareness. The pivotal role of the posterior cingulate, precuneal, and retrosplenial cortices in consciousness is demonstrated with posterior cingulate epilepsy cases, midcingulate lesions that de-afferent this region and are associated with unilateral sensory neglect, observations from stroke and vegetative state patients, alterations in blood flow during sleep, and the actions of general anesthetics. Since this region is critically involved in self reflection, it is not surprising that it is similarly a site for the NNCC. Interestingly, information processing during complex cognitive tasks and during aversive sensations such as pain induces efforts to terminate self reflection and result in decreased processing in posterior cingulate and precuneal cortices.

Introduction

Consciousness is a multifaceted concept that can be divided into two major components: the level of consciousness (i.e., arousal, wakefulness, or vigilance) and the content of consciousness (i.e., awareness of the environment and its relations to self) (see also Zeman, this volume). Although the entire forebrain is engaged to some extent in conscious information processing, there may be specific areas that are particularly crucial to consciousness. The midbrain reticular formation and its projections to the thalamic intralaminar nuclei establish and maintain wakefulness (Kinomura et al., 1996; Steriade, 1996), and postmortem assessments of the vegetative state show that damage to the dorsolateral midbrain and thalamus is a common feature in these cases (Kinney et al., 1994; Adams et al., 2000; Graham et al., this volume) and severe damage around the third ventricle that blocks this projection can produce coma (e.g., case 13, Malamud, 1967). The more difficult problem is the extent to which any forebrain region is necessary for conscious cognitive information processing.

In one sense, the entire cerebral cortex is necessary for awareness of numerous sensory and motor events. In this context, the null hypothesis states that no part of the forebrain plays a disproportionate role in consciousness or information processing during wakefulness. According to the null hypothesis, the neural correlates of consciousness are fully distributed throughout the forebrain. We will attempt to reject the null hypothesis by showing first that parts of the cingulate gyrus are necessary for conscious experience, although they may not be sufficient, and second that there is a critical linkage between the brainstem arousal system and posterior cingulate (PCC) and retrosplenial (RSC) cortices that assures a close coupling between arousal and awareness. This view and its supporting facts can be extended to a few other regions that form a critical neural network correlates of consciousness (NNCC) that is both necessary and sufficient for conscious cognitive information processing.

We propose that PCC and precuneus cortex (PrCC) together are pivotal for conscious information processing. Support for this hypothesis is derived from postmortem assessments of epilepsy, stroke, monkey and human cingulotomy lesions; and vegetative state cases, functional imaging in epilepsy, amnesia, sleep states and general anesthesia, and tasks requiring consciousness for sensorimotor processing. We also emphasize a critical linkage between brainstem generated arousal and processing in the PCC/PrCC region and this dual function assures that PCC/PrCC is a key node in the NNCC.

Section snippets

Anatomical overview of posterior cingulate gyrus and precuneal cortex

Many observations are available from human imaging studies of the PCC and medial parietal lobe region; however, standardized software packages continue to use Brodmann's (1909) anatomical observations from a century ago. Fig. 1 provides a context for this region according to recent cytological observations. Fig. 1A is a co-registration of Brodmann's map with a postmortem case for which we have extensive histology. The histological case is a left hemisphere that was flipped horizontally to match

Epilepsy, stroke and vegetative state

According to Mazars (1970), the first episode of a cingulate epilepsy discharge is associated with

“absences that are often mistaken for inattention. Twenty of our patients never had convulsive seizures and their ‘absences’ did not differ much from the short spells of loss of consciousness of ‘petit mal’… the time to regain normal consciousness was longer, and a less abrupt recovery of consciousness was associated with an outburst of temper which could be so marked as to obscure the preceding

Cerebral metabolism

In humans, the highest level of cortical glucose metabolism occurs in PCC and RSC (Andreasen et al., 1995; Maquet et al., 1997; Minoshima et al., 1997; Gusnard and Raichle, 2001; Laureys et al., 2004). The highest level of basal glucose metabolism in the monkey brain is in RSC and the anterior thalamus and these levels are elevated during performance of a delayed-response task (Matsunami et al., 1989). We have discussed the close laminar association of both high levels of glucose metabolism

Anteroventral thalamic link between conscious wakefulness and cognitive awareness

Since the intralaminar thalamic nuclei are particularly important to wakefulness (Kinomura et al., 1996; Steriade, 1996), their projections might be expected to be a primary driver of information processing in critical parts of the NNCC. At first blush, this does not seem to be the case. Although PCC does receive a small projection from midline and intralaminar thalamic nuclei, the major projections of these nuclei are to MCC and ACC (Vogt et al., 1987). Although it is possible that a small

Sleep

A region critical to conscious information processing might be expected to be inactivated during sleep and area 31 of PCC has reduced regional cerebral blood flow (rCBF) during the rapid-eye movement (REM) phase of sleep (Maquet et al., 1996; also see Maquet et al., this volume). This does not prove that area 31 quiescence is pivotal to REM sleep, however, it is supportive of that conclusion because there was also a massive bilateral prefrontal inactivation during REM. Fig. 3 provides measures

Anesthetic sensitivity

Although anesthetics have general mechanisms of action such as at the GABAA receptor and these likely reduce neuron activity throughout the brain, there are also particularly susceptible regions and modulation of their activity may be most closely associated with conscious functions (for review see Alkire, this volume; Fiset, this volume). In the rat, the tuberomamillary nucleus is particularly sensitive to anesthetics that act at GABAA receptors including propofol (Nelson et al., 2002).

Self reflection and complex information processing

The PCC has a major role in visuospatial orientation, topokinesis, and navigation of the body in space (reviewed in Vogt et al., 2004). Recent functional imaging suggests this function may be specifically related to self reflection (Johnson et al., 2002; Kelley et al., 2002) and autobiographical memory (Piefke et al., 2003), and this includes assessments of objects in space in terms of a first-person orientation (Vogeley et al., 2004). Although all the previous studies engaged PCC, PrCC has

Anatomical relationships between mental and conscious information processing

The discussed role of RSC/PCC/PrCC in conscious awareness raises another issue: To what extent does the NNCC in the cingulate gyrus overlap with the neural correlates of mind (NCM)? The same view of consciousness has been argued previously for NCM (Vogt and Devinsky, 2000) to the extent that there is a part of cingulate cortex that plays a particularly important role in mental function based on lesion and functional imaging observations. The neuroscientific definition of mind in this context is

Acknowledgments

BAV is supported by National Institute of Health grant #NS44222, SL is Research Associate at the Fonds National de Recherche Scientifique (FNRS). For their kind permission to share and reanalyze previous PET data, we thank Pierre Maquet and Philippe Peigneux (sleep studies) and PM, PhP, Eric Salmon, and André Luxen from the Cyclotron Research Center of the University of Liège (healthy control rCMRGlu studies); and Vincent Bonhomme, Pierre Fiset and colleagues from the department of

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