ReviewEEG delta oscillations as a correlate of basic homeostatic and motivational processes
Highlights
► Delta oscillations dominate the EEG of waking reptiles. ► In humans, they are prominent in early developmental stages and in slow-wave sleep. ► They increase in many developmental disorders and pathological conditions. ► They are association with homeostatic processes and motivation. ► They are implicated in salience detection and subliminal perception.
Introduction
Some time ago electroencephalogram (EEG) was considered to be useful only for making inferences about global states of sleep and wakefulness (e.g. Duffy, 1962, Thayer, 1989). The recent resurgence of interest in neuronal oscillations is a result of several developments, which showed that mammalian cortical neurons form behavior-dependent oscillating networks which bias input selection, temporally link neurons into assemblies, and facilitate synaptic plasticity (Buzsaki and Draguhn, 2004). The synchronous activity of oscillating networks is now viewed as the critical “middle ground” linking single-neuron activity to behavior. Growing body of evidence suggests that different levels of cerebral integration mediated by spatial and temporal synchrony over multiple frequency bands could play a key role in the emergence of percepts, memories, emotions, thoughts, and actions (Cantero and Atienza, 2005, Nunez, 2000, Varela et al., 2001). This understanding implies that different frequency oscillations must be associated with different processes.
Ongoing and event-related oscillations are usually categorized into five frequency bands: delta (0.5–3.5 Hz), theta (4–7 Hz), alpha (8–12 Hz), beta (13–30 Hz), and gamma (>30 Hz). These five bands could be meaningfully divided into two categories. Delta, theta, and alpha oscillations are examples of the so-called global processing modes which span relatively large cortical regions and have been hypothesized to serve the purpose of integration across diverse cortical sites by synchronizing coherent activity and phase coupling across widely spatially distributed neural assemblies. Oscillations of beta and gamma ranges, or local EEG modes, are higher in frequency, lower in amplitude, and distributed over a more limited topographic area (Nunez, 1995). It is suggested that dynamic coordination at a timescale of hundreds of milliseconds (such as delta oscillation) may be essential for optimization of distributed representations in the brain, whereas patterns of synchronous local interactions may be coordinated dynamically on a faster timescale. Processes occurring at these two timescales can mutually constrain each other through mechanisms of time-dependent plasticity and experience-dependent consolidation of architectures selected by synchronization (Engel et al., 2010). Fast oscillations (beta and gamma) are essential for coordination of computations in tens of millisecond range in specific cognitive processes. Slow oscillations modulate fast oscillations on a higher level of hierarchy and thus determine the general mode of processing. Highly localized computations may be able to oscillate at higher frequencies while more complex, integrative, or inherently slower computations may result in slower oscillations (Engel et al., 2010). Therefore, oscillations are hierarchically organized with slower oscillations being at higher levels of the hierarchy (meaning they are linked to more basic and general classes of processes).
A large body of evidence suggests that oscillatory activity in all frequency bands is linked to a broad variety of perceptual, sensorimotor, and cognitive operations (Singer, 1999, Basar et al., 2000, Klimesch, 1996, Palva and Palva, 2007). This evidence, however, yields a rather complex picture. While it provides clear cases of task- or context-related modulation of different frequency bands, it does not yet allow making conclusions regarding functional significance of these bands. One way to approach this difficult question would be from an evolutionary perspective (Knyazev and Slobodskaya, 2003, Knyazev et al., 2004). Such approach is inevitably speculative, but having considerable explanatory value it allows unifying data coming from different research domains. The evolutionary interpretation of brain oscillations mostly considers the global mode oscillations of delta, theta, and alpha ranges. It suggests that these three oscillatory modes are associated with brain systems that have different significance at different evolutionary stages. Specifically, delta oscillations are associated with the most ancient system, which was dominant in the brain of lower vertebrates (reptilian, amphibian, and fish). Theta oscillations dominate in lower mammals. Alpha oscillations are associated with the most advanced system, which dominates in adult humans (Knyazev and Slobodskaya, 2003). This idea is clearly reminiscent of the well known triune brain concept by Paul MacLean (MacLean, 1990), but Knyazev et al. (2004) emphasized that the triune brain concept was used more as a metaphor and the three oscillatory systems do not have to exactly correspond to the anatomical borders of the three brains of the MacLean's model. This review will concentrate on delta oscillations. First, predictions derived from the evolutionary point of view will be formulated. Next, available empirical evidence will be matched against these predictions. But I begin by discussing the viability of the triune brain concept.
MacLean originally formulated his model in the 1960s and propounded it at length in his 1990 book (MacLean, 1990). It posits that evolutionary processes have endowed humans with essentially three brains: the reptilian complex, the paleomammalian complex, and the neomammalian complex, viewed as structures sequentially added to the forebrain in the course of evolution. The reptilian complex was the name MacLean gave to the set of brain structures comprising the brain stem including much of the reticular system and basal ganglia. MacLean contended that the reptilian complex was responsible for species typical instinctual behaviors involved in aggression, dominance, territoriality, and ritual displays. The paleomammalian complex consists of the septum, amygdala, hypothalamus, hippocampal complex, and the cingulate cortex. Most of these structures are parts of the so-called limbic system (the term coined by MacLean), and MacLean maintained that these structures were responsible for the motivation and emotion involved in feeding, reproductive behavior, and parental behavior. The neomammalian complex consists of the cerebral neocortex. MacLean regarded its addition as the most recent step in the evolution of the human brain, conferring the ability for language, abstraction, planning, and perception. Subsequent findings have invalidated the traditional neuroanatomical ideas upon which MacLean based his hypothesis. The model of evolution characterized by accretion of parts that MacLean proposed has been entirely replaced by another model that emphasizes conservation of fundamental segmental structure (Rubenstein et al., 1994, Rubenstein et al., 1998). For instance, most areas of neocortex (the neomammalian complex in the MacLean's model) have homologues in amphibian and other vertebrate brains, suggesting that the mammalian neocortex was not added like icing onto an already baked cake, but was radically transformed from a series of precursors (Striedter, 2005). Moreover, Striedter (2005) observes that “brains are like companies – they must reorganize as they increase in size in order to stay functional” (p. 127). Firstly, the brain's average connection density must decrease with increasing brain size; otherwise the number of axons would increase explosively with neuron number, racking up enormous costs in terms of space and metabolic energy (Striedter, 2005). This decrease in average connection density implies that brains become more modular, both structurally and functionally, as they increase in size (Jacobs and Jordan, 1992). Local connections alone place major constraints on global synchrony in growing brains. The densely connected local neuron networks are supplemented by a small fraction of long-range connections (Braitenberg and Schutz, 1998). Despite the progressively decreasing fraction of long-range connections in larger brains, synchronization of local and distant networks can be readily accomplished by oscillators because of the low energy costs involved in coupling rhythms (Buzsaki and Draguhn, 2004). That means that significance of oscillations must increase in large brains. Available evidence shows that this is indeed the case. Invertebrates have much more obvious unit spiking than vertebrates, but much less relative amplitude of slow (<50 Hz) waves (Bullock, 1993). EEG-like activity could be recorded in the octopus brain but not in other, less developed invertebrates (Bullock, 1984, Bullock and Basar, 1988). Among vertebrates the degree of synchronization also increases during evolution. There is evidence of less synchrony or more rapid coherence decline with distance in reptiles, amphibians, and fish than in mammals (Bullock, 1997, Bullock, 2002).
Secondly, the principle ‘late equals large’ causes late-born regions, such as the neocortex, to become disproportionately large as absolute brain size goes up (Striedter, 2005). As brain regions increase in absolute and/or proportional size, they frequently change in internal organization. Another principle that helps explain some variation in neuronal connectivity is Deacon's (1990) displacement hypothesis, which Striedter (2005) calls the rule of ‘large equals well-connected.’ It holds that, whenever a brain region increases in proportional size, it tends to receive more inputs and project to more targets than it did ancestrally. The human neocortex projects directly to and throughout the brain stem and spinal cord (Barret et al., 2007). As a result, humans (and other great apes) have greater direct and indirect cortical control over the subcortex and spinal cord than do rats, allowing greater autonomic and behavioral diversity and flexibility.
All these recent developments largely invalidate evolutionary ideas that were put in the base of the MacLean's triune model. However, this model continues to hold interest for some psychologists and members of the general public because of its focus on the recognizable differences between most reptiles, early mammals, and late mammals. Reasons for the success are its simplicity; the theory in this form recognizes three major evolutionary periods in the development of the brain that are characterized by three recognizably distinct ways of solving adaptive challenges. The three functional domains described by the original triune model, wherever located, remain useful organizing themes and concepts. Indeed, it is difficult to deny that evolution tends to preserve devices that proved to be useful at a certain stage, and late-born more advanced devices do not usually replace the old ones but coexist with them. Thus, neurobiologically, mammals are distinguished mainly by their neocortex, which has non-mammalian precursors but is highly modified and genuinely new. Looking beyond the neocortex, we find that mammal brains are similar, though not identical, to reptile brains (Striedter, 2005). These ‘old’ devices that are preserved in the mammal brain continue to do their job in much the same way they did it in lower vertebrates, though closely supervised by advanced ‘new’ devices. Much evidence shows that late-born advanced brain mechanisms are last to appear and first to extinct in the course of individual development and are more vulnerable to detrimental environmental influences. As Jackson (1958) once famously noted, “The higher nervous arrangement inhibit (or control) the lower, and thus, when the higher are suddenly rendered functionless, the lower rise in activity”. Hence, although modern advances in the field of evolutionary neuroscience show that the general picture is much more complicated than perhaps John Hughlings Jackson and even Paul MacLean once described, their core idea about coexistence in the human brain of functional domains that in the evolution were associated with distinct ways of solving adaptive challenges is still viable and productive.
The most important difference between the MacLean's model and the evolutionary interpretation of brain oscillations is that the former deals with anatomically defined parts of the human brain whereas the latter deals with brain oscillations whose relation to specific brain structures is a complicated and not fully resolved question. Contemporary neuroanatomy emphasizes conservation of fundamental segmental structure as the main principle of the evolution of vertebrates (Rubenstein et al., 1994, Rubenstein et al., 1998). Even neocortex, the most advanced part of the mammalian brain, is hypothesized to evolve from tri-laminar reptilian dorsal cortex (Puelles, 2001, Reiner, 1993). Applying this principle to oscillations, it is reasonable to suggest that the three oscillatory systems should exist at all stages of vertebrate evolution. Indeed, delta, theta and alpha frequencies could be found in each vertebrate (Basar, 1998), but their relative amplitudes are remarkably different in different species. Accordingly, functions, which are presumably linked with the three global oscillatory systems, should be present in all vertebrates, but emphasis and dominance of some functional and behavioral patterns should differ across different species.
In this review I will try to defend the thesis that delta oscillations manifest the most ancient oscillatory mode, comparative to higher frequency oscillations. To comply with this thesis, delta oscillations must (1) dominate in EEGs of lower vertebrates (particularly reptiles, the direct mammal's ancestors). ‘Dominate’ in this context means that they not only must have the highest power in the spectrum (comparative to theta and alpha frequencies), but be the most functionally ‘active’ oscillations, which are more pronounced during typical to these species activity and in response to environmental challenges. (2) In humans, in compliance with the principle first formulated by Jackson (1958), delta oscillations must be more pronounced in conditions that are associated with diminished activity of the ‘higher’, or more advanced ‘nervous arrangements’. These conditions include: (a) earlier developmental stages, when ‘higher nervous arrangements’ are yet in the process of maturation; (b) deep sleep, when the brain is in a state of functional decortications (Rial et al., 2007b); (c) pathological states caused by detrimental environmental factors, developmental pathology, or damage to brain tissue.
Besides these general predictions, evolutionary interpretation allows a number of more specific predictions about association of delta oscillations with behavior and physiological processes. These predictions could be derived basing on the main premise of the evolutionary interpretation, namely, that the oscillatory system, which dominates the EEG of particular species, should be linked to functions and behavioral patterns that dominate the behavior of these species. The behavior of lower vertebrates is dominated by patterns directly oriented to the acquisition of biologically important goals such as physical maintenance, survival, dominance, and mating. To be adaptive, such behavior requires constant feedback from sensors signaling deviation from optimal homeostasis. Hence, delta activity is expected to be sensitive to internal stimuli signaling such deviations (e.g., during hypoxia, hypoglikemia, fatigue, pain), as well as to the stimuli signaling a need for sexual activity (e.g. the level of sexual hormones). It should be implicated in monitoring of autonomic functions, such as breathing and heartbeat, because these functions are critical for survival. Since behavior that is oriented to satisfaction of basic biological needs is mostly guided by activity of the brain reward systems, delta oscillations are expected to be sensitive to signals coming from these systems. In particular, that should be evident with respect to drugs of abuse which directly influence the brain reward systems. Because the detection of motivational salience of environmental stimuli is supposed to be the main function of the brain reward systems (Gray, 1999), delta activity is expected to play a leading part in this process. Besides, delta activity is expected to be associated with primitive defense mechanisms which in humans are mostly rudimentary.
In the following text, available empirical evidence will be matched against these predictions. This text will be divided into two sections. The first section will review the evidence on the presence of delta oscillations in lower vertebrates and at different developmental and circadian cycle stages, as well as the evidence on association of delta oscillations with autonomic regulation and pathological processes. The second section will review the evidence on the place of generation of delta activity and its association with motivation and cognitive processes.
Section snippets
Delta oscillations in lower vertebrates
If delta oscillations indeed represent an evolutionary old oscillatory mode, they must dominate in EEGs of lower vertebrates, particularly during typical for these species behavior. During his fruitful career, Theodor Bullock has undertaken the most considerable effort to collect comparative EEG data. Analysis of these data allowed him to formulate two basic generalizations. The first one reflects a drastic difference in the EEGs between all vertebrates and all invertebrates (with the exception
The place of generation of delta activity
If we suppose that the function of delta oscillations is somehow linked with motivation, we should expect that the generation of delta activity should be associated with motivational brain circuits. Unfortunately, most of these circuits are located deep in the brain and their electrical activity is not directly accessible on the scalp. Although we may learn much from findings that come from fMRI, PET, and animal research, caution should be exercised when these findings are applied to the
General conclusion
In this review, the evidence on functional correlates of delta oscillations has been reviewed from an evolutionary point of view. Predictions derived from the evolutionary interpretation were formulated and matched against existing empirical evidence. In spite of scarceness of this evidence, the general pattern appears to fit the idea that delta oscillations represent an evolutionary old oscillatory mode that dominated in lower vertebrates, but in waking adult humans it is overshadowed by more
Acknowledgements
This work was supported by a grant of the Russian Foundation for Basic Research (RFBR) no. 11-06-00041-a. Author is grateful to Kimberly Barchard for careful reading and helpful comments on the first version of the manuscript.
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