Encyclopedia of Evolutionary Psychological Science

Living Edition
| Editors: Todd K. Shackelford, Viviana A. Weekes-Shackelford

Self-Monitoring

  • Hans C. LouEmail author
Living reference work entry
DOI: https://doi.org/10.1007/978-3-319-16999-6_3125-1

Keywords

Autism Spectrum Disorder Transcranial Magnetic Stimulation Pyramidal Cell Gamma Oscillation Dopaminergic Tone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Synonyms

Definitions and Conclusions

Consciousness research is today one of the cornerstones in neuroscience. Almost all studies in the field have focused on identifying neural events accompanying appearences in the outer world, the “qualia,” like the redness of wine. These attemps have typically neglected the issue of the “Self.” Obviously, the self and qualia are two sides of the same coin. As formulated by Ramachandran (2004, p. 96):“You cannot have free-floating sensations, with no one to experience them.” Self-awareness is the essential tool for conscious metacognition. Metacognition monitors and controls behavior, the “self,” and thereby adjusts our beliefs of the world, essential for learning by conscious experience. This occurs not only within ourselves, but, importantly, also between individuals. Self-awareness is a primordial human capacity and is of decisive importance by giving humans an upper hand in phylogenetic development of culture and society (Frith 2012).

Self-awareness, or conscious self-monitoring, is the focus of this entry, based on a recent review (Lou et al. 2016a). It was until recently considered off-limits for the natural sciences. Neurobiological research shunned the “hard question of how consciousness and self-awareness arise from a physical basis,” influenced by the philosopher David Chalmers in the late 1990s (referenced by Lou et al. 2016a). Therefore, it has been fashionable to limit the quest for understanding the workings of the brain in consciousness and self-awareness to the task of identifying neural “correlates” of these mental functions. The limitation clearly involves the risk of arriving at two parallel worlds: a mental and a physical, without understanding how they interact. The consequence of this would be severe impediment of our understanding of the biological function of self-awareness and how it may account for disease in default.

However, using electrophysiological and pharmacological manipulations we have discovered that highly connected “hubs” of medial prefrontal and parietal are associated with self-awareness. They are not only linked to that function but indeed instrumental in its generation: Transcranial magnetic stimulation (TMS) targeting the hubs impedes specific aspects of self-awareness (Lou et al. 2004; Luber et al. 2012). Conversely, self-awareness is increased by dopaminergic challenge, primarily via GABA neurotransmission directly in the medial prefrontal cortex (Joensson et al. 2015; Lou et al. 2016b). The hubs are provided by an exceptionally rich assembly of fast-spiking parvalbumin interneurons assuring synchronization of their pyramidal cells for generation of self-awareness. The exceedingly high metabolic rate of these hubs makes them vulnerable in penuria of oxygen and/or glucose as a common final path in the pathophysiology of the many disorders with deficient self-awareness, like autism, attention deficit disorder, schizophrenia, and dementia.

Investigating Self-Awareness

Gallagher (2000), following Wittgenstein and the phenomenologists, claims that we are selfaware whenever we are conscious. Accordingly, self-awareness is an indispensible part of our experience of the world, whether it is minimal self-awareness (pre-reflective, with an automatic sense of ownership of the experience) or narrative (extended and reflective, based on retrieval of episodic (personal) memory). Minimal self-awarenes may be investigated using rapidly presented stimuli, which become aware to the observer when presentation time exceeds a certain threshold (Weiskrantz et al. 1995; Kjaer et al. 2001) or by comparing first person perspective with third person perspective (Vogeley et al. 2004). Narrative (extended) self-awareness may be investigated using retrieval of episodic memory of previous judgment of self versus another person (Lou et al. 2004). Both minimal and narrative self-awareness may be ranked according to the degree of self-reference (Craik et al. 1999).

The Paralimbic Network as a Signature of Self-Awareness and Conscious Self-Monitoring

“Mind wandering,” where the person is shifting his attention to changing states and objects, is associated with shifting patterns of brain activation (Lou et al. 1999). In spite of this variability, a set of medial paralimbic regions, including medial parietal (precuneus) and medial prefrontal regions, are continuously active as measured by principal component analysis (Fig. 1) (Kjaer and Lou 2000). The network is similar to the network activated by focusing on one-self versus another person in a dark room without intended sensory stimulation or motor activity (Fig. 2) (Kjaer et al. 2002). This medial paralimbic network has proved to be a common neural signature for widely different aspects of self-awareness and concious experiences in all functional domains examined. This was evident in a large meta-analysis of investigations using 15O-H2O positron emission tomography or functional magnetic resonance imaging (fMRI) (Northoff et al. 2006).
Fig. 1

Cerebral activation patterns vary with shifting contents of consciousness. All conditions include a paralimbic network. The four upper rows represent cerebral blood flow patterns measured with 15O-H2O-positron emission tomography (PET) during yoga nidra meditation on weight of own body part (upper row) abstract perception of joy (second row) visual imagery of landscape (third row), and symbolic representation of self (lower row) (Lou et al. 1999) (a) (With permission). The right medial parietal cortex (precuneus), prefrontal cortex, and right striatum are coactivated in all meditative states and the control state (Lou and Kjaer 2005) (b) (With permission). Visual presentation of single words long enough to be perceived consciously activates medial orbital, medial prefrontal, and medial parietal cortices when compared to subliminal presentation (c) (Kjaer et al. 2001) (With permission)

Fig. 2

The paralimbic network in self-awareness. Retrieval of previous judgment of oneself activates dramatically the paralimbic network of medial prefrontal (anterior “hub”) and medial parietal cortices (posterior hub), together with thalamus (15O-H2O PET) (Lou et al. 2004; Changeux and Lou 2011) (With permission)

The midline cortical “hubs” of the paralimbic network are usually linked with activity in the angular gyri, right insula, and subcortical regions (e.g., Joensson et al. 2015). The two midline hubs interact by means of recurrent oscillations in the entire frequency range measured, i.e., from less than 5 Hz to 100 Hz, with a maximum at 40 Hz. The network is active at rest without intended sensory or motor activity. That condition is characterized by a fairly large proportion of spontaneous self-referential thinking (Kjaer et al. 2002). When self-referential thinking becomes dominant, for instance, during relevant tasks in an experimental setting, a large increment is seen in the entire frequency spectrum (Fig. 3) (Lou et al. 2011).
Fig. 3

Recurrent information flow between medial prefrontal and parietal hubs. Granger causality [magnetic encephalographic (MEG) amplitudes] is seen in the entire frequency range (5–100 Hz, maximal at 40 Hz) in the prestimulus state (rest), a condition characterized by mind-wandering and self-referential thoughts (see Fig. 1). During retrieval of episodic memory (previous self-judgment), power is increased throughout the frequency spectrum (Lou et al. 2011) (With permission)

From Association to Causality

The ascription of the medial paralimbic network to self-awareness is essentially based on imaging data and can, as such, only be correlative. Accordingly, the significance of these findings for self-awareness has been disputed (e.g., Smith 2012). To test whether the paralimbic network is indeed instrumental in the generation of self-awareness, a series of intervention studies has been carried out. The investigations included behavioral consequences of electromagnetic as well as neurotransmitter manipulation of the network: Directly targeting the medial parietal and medial prefrontal region with TMS showed unequivocally that the former region is instrumental in retrieval of self-related episodic memory (narrative self-awareness), while the latter region is instrumental in self-evaluation (Lou et al. 2004; Luber et al. 2012). The effect was simultaneous at the two disparate sites, with a latency of 160 ms after sensory stimulation (Fig. 4). This confirmed the global neuronal network hypothesis for access to consciousness and the simultaneous “ignition” of separate brain regions in the course of conscious processing (for review, see Lou et al. 2016a). Magneto-encephalography and Granger causality computation show that interaction between the prefrontal and parietal “hubs” occurs with oscillations mainly in the gamma range. Causality of lower gamma oscillations in the frontal regions for self-awareness has subsequently been confirmed by application of synchronous oscillations around 25 and 40 Hz over the frontal skull, showing stimulation induced self-reflective awareness in dreams during REM sleep (Voss et al. 2014).
Fig. 4

Causality of paralimbic network evidenced by transcranial magnetic stimulation (TMS). Efficiency of retrieval of self-judgment is selectively impaired at medial parietal (Lou et al. 2004) and both angular gyri, while preference for allocating positively rated adjectives to one-self rather than best friend is selectively impaired with TMS targeting the medial prefrontal cortex (Luber et al. 2012) (With permission). The results demonstrate that the different aspects of self-awareness “ignite” access simultaneous at a latency of 160 ms

Generation of gamma frequency oscillations depends on fast-spiking parvalbumin GABA-ergic interneurons. Experiments with transgenic mice deficient in these interneurons have shown deficient gamma oscillations and behavioral defects, which may be restored by opto-genetically stimulating prefrontal cortical interneurons. In humans, Hall et al. (2010) found that GABA-ergic stimulation induces power increase predominantly in pyramidal cells of the prefrontal cortex. Such power increase depends on synchronization of pyramidal cell output. Recently, we have demonstrated that dopamine increases self-awareness in humans (Joensson et al. 2015) (Fig. 5) via increased GABA activity (Lou et al. 2016b) (Figs. 6 and 7). This occurs mainly in the medial prefrontal/anterior cingulate cortex, and, as a trend, in the right insula, explaining our previous finding that dopamine regulates self-awareness via medial prefrontal cortex (Fig. 5). It also explains that self-awareness is preferentially dependent on right hemisphere activity, as demonstrated by Keenan et al. by carotid infusion of anesthetics (see Lou et al. 2016a).
Fig. 5

Dopamine increases self-awareness and gamma power. Dopamine challenge (sinemet 100 mg) decreases error rate in retrieval of previous judgment on whether adjectives fitted one-self or not compared to placebo (a), while retrieval of judgment of a control person is not changed significantly (b). (c) Whole brain MEG showing distribution of dopamine-induced power increase (gamma range (30–100 Hz). Preferential power increase in prefrontal region is documented and is likely due to the distribution of dopamine receptors in the brain (Joensson et al. 2015) (With permission). The blue cross shows location of peak increase with dopamine at the MNI coordinates (0, 36, 36 mm). (d) Z - values> 2 (Monte Carlo simulation of the difference between placebo and dopamine medication groups)

Fig. 6

Dopamine activates the GABA system in paralimbic network. The distribition of the GABA receptor PET ligand [11C]Ro15-4513 binding, with placebo, dopamine challenge, and placebo minus dopamine. With placebo, the ligand is bound primarily in the medial prefrontal/anterior cingulate region, and in left and right insula. After L-dopa, the binding is reduced, seen clearly by subtraction. There is a reduction of between 5% and 20% throughout most of gray matter, indicating widespread cortical activation of the GABA-ergic interneurons. (Lou et al. 2016b) (With permission)

Fig. 7

GABA-receptor molecule at pyramidal cell membrane. Molecular model of the GABA-A receptor on pyramidal cell and of the main categories of binding sites for pharmacological agents. The GABA binds to defined subunit interfaces in the extracellular domain (violet region). Activation of this molecule is the final common path for generating gamma synchrony and self-awareness (With permission). For details, see (Li et al. 2006; Nury et al. 2011; Bocquet et al. 2009; Changeux and Lou 2011)

Also acetylcholine, an agonist of dopamine activity, may directly activate subsets of inhibitory interneurons, with synchronization of pyramidal cells as a result. This has recently been demonstrated at the cellular level in layer II/III in prefrontal cortex of mice using in vivo two-photon imaging (Koukouli et al. 2016). Figure 8 schematically illustrates the transmitter regulation of self-awareness.
Fig. 8

Overview of neurotransmitter regulation of self-awareness. Fast spiking GABA-ergic interneurons are activated by dopamine and acetylcholine and quite possibly other neurotransmitters at receptors located at or near the soma. Via GABA receptors in the pyramidal cell membrane dopamine enhances paralimbic synchrony for self-reference, a crucial constituent of any conscious experience (Changeux and Lou 2011) (With permission)

Thus neural system, cellular, electromagnetic, and transmitter physiology all testify that the paralimbic system is instrumental in self-awareness. It is tantalizing how closely this discovery, based on experimental data, fits with suggestions based on bedside clinical observations by Ramachandran (2004, p. 112).

Ontogenesis of Self-Awareness and Metacognition

The infant is probably aware only of events in the present time, while the adult capacity to put these sensations into a time perspective, with ability to plan for the future, has to await later development (Lagercrantz and Changeux 2009). Similarly, the development of metacognition does not seem to occur until after 3 years of age.

This development occurs concomitantly with the development of resting state activity in the medial prefrontal and medial parietal hubs and insula, i.e., the paralimbic network (Fransson et al. 2011).

Pathophysiology

Due to the fundamental biological importance for the individual and society of self-awareness, self-monitoring, and metacognition, their disturbance is likely to be linked to severe pathology. Thus, frontal and medial parietal cortices are dysfunctional in a monosymptomatic condition with deficient conscious self-monitoring such as behavioral addiction (Rømer Thomsen et al. 2013) (Fig. 9). It is also the case for more complex disorders involving poor self-awareness and self-monitoring such as substance abuse, ADHD, autism spectrum disorder, schizophrenia, and the dementias, and also traumatic brain injury. Even in a pervasive dysfunctional state such as the vegetative state, recovery of the paralimbic network is tightly linked to clinical recovery (For review see Lou et al. 2016a).
Fig. 9

Abnormal gamma synchronization (SI) in pathological gamblers. At rest, pathological gamblers have lower synchronization than controls in gamma band (30–100 Hz) (b vs a). (Subgroup analysis showed that this difference was present both for gamblers with and without a history of comorbid stimulant addiction (both P < 0.05)) (a) (Rømer Thomsen et al. 2013). This illustrates abnormal function in the paralimbic network of self-reference linked to abnormal conscious self-monitoring and metacognition in individuals susceptible to pathological gambling (With permission)

The widespread dysfunction of self-awareness in pathology is the result of the exceedingly high oxygen demand of the paralimbic default network (Kann 2016).This makes self-awareness, conscious self-monitoring, and metacognition particularly vulnerable to deficient oxygen and glucose supply. The high metabolic requirement is mainly due to dense concentrations of interneurons in the richly connected “hubs” of the paralimbic default network, their GABA-ergic synapses being instrumental for pyramidal cell synchronization in the paralimbic network. In particular, gamma oscillations are vulnerable to metabolic disruptions, a promising venue in the treatment and prevention of disorders of self-awareness.

Perspectives for Prevention and Treatment

The new understanding of the physiology and pathophysiology may lead to the application of novel or recently developed therapeutical strategies to increase dopaminergic activity and to improve neural interactions. These strategies may include meditation, which in independent studies have been shown to increase dopaminergic tone and induce growth in paralimbic structure, and targeted training aiming at increasing the availability of dopaminergic receptor. Also improvement of sensory input may be an important venue to increase dopaminergic tone and induce growth in relevant structures. Likewise frontal electromagnetic stimulation of oscillations may have a role. More generally, the new discoveries provide impetus to efforts to maintain oxygen homeostasis in neural tissue ranging from decreasing oxygen demand by cooling, for instance, in distressed neonates, to controlling cerebral perfusion pressure and autoregulation of cerebral blood flow, and obtaining optimal cerebral blood flow distribution via the capillary network (for review, see Lou et al. 2016a).

Cross-References

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Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Center for Integrative NeuroscienceAarhus UniversityAarhus CDenmark

Section editors and affiliations

  • Catherine Salmon
    • 1
  1. 1.University of RedlandsRedlandsUSA