Motivation, emotion, and their inhibitory control mirrored in brain oscillations

Abstract

Recent studies suggest brain oscillations as a mechanism for cerebral integration. Such integration can exist across a number of functional domains, with different frequency rhythms associated with each domain. Here, evidence is summarized which shows that delta oscillations depend on activity of motivational systems and participate in salience detection. Theta oscillations are involved in memory and emotional regulation. Alpha oscillations participate in inhibitory processes which contribute to a variety of cognitive operations such as attention and memory. The importance of inhibitory functions associated with alpha oscillations increases during the course of evolution. In ontogenesis, these functions develop later and may be more sensitive to a variety of detrimental environmental influences. In a number of developmental stages and pathological conditions, a deficient alpha and/or increased slow-wave activity are associated with cognitive deficits and a lack of inhibitory control. It is shown that slow-wave and alpha oscillations are reciprocally related to each other. This reciprocal relationship may reflect an inhibitory control over motivational and emotional drives which is implemented by the prefrontal cortex.

Introduction

It has been shown that mammalian cortical neurons form behavior-dependent oscillating networks whose synchronous activity is now viewed as a mechanism for cerebral integration (Salinas and Sejnowski, 2001; Singer, 1999) and the critical “middle ground” linking single-neuron activity to behavior (Buzsaki and Draguhn, 2004). Growing 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 evidence implies that all frequency bands of the human EEG may have some functional significance, and each frequency band could be linked with specific processes.

The range of frequencies in the human EEG could be meaningfully divided into two subdivisions. Delta, theta, and alpha oscillations are examples of so-called global processing modes which span relatively large cortical regions. Global modes 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 (Nunez, 1995). 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. They could be considered as elementary signals of the brain, functionally related to diverse brain processes (Schurmann et al., 1999). There is consistent evidence that the global mode oscillations operate in close conjunction with the local mode oscillations. These dynamic interactions might reflect the modulation of fast activations in local circuitry by large-scale networks operating in lower frequencies (top-down integration), or it might reflect a bottom-up mechanism for propagation of local activation to other cortical regions (Demiralp et al., 2006). This review will mostly deal with the global mode oscillations of delta, theta, and alpha ranges.

There is some controversy in the literature as to whether all the global modes oscillations are uniformly linked with active processes. Some authors suggest that alpha could be opposed to slow oscillations (particularly theta) in that former tend to decrease and latter to increase during activation (e.g. Klimesch, 1999). An important implication could be that slow waves are linked with activation whereas alpha with a cessation of activity or inhibition (e.g. Pfurtscheller and Lopes da Silva, 1999). Thus, alpha and slow oscillations appear to be reciprocally connected with each other. This notion is in line with abundant evidence showing that a deficient alpha and/or increased slow-wave activity is associated with a lack of inhibitory control over behavior. This paper aimed to discuss the apparent dissimilarity of alpha and slow waves in relation to behavioral signs of activation and inhibition. First, a review of evidence showing that in a number of states and conditions a lack of alpha and/or prevalence of slow oscillations are associated with inhibitory deficits and behavioral signs of disinhibition will be presented. Next, functional correlates of delta, theta, and alpha oscillations will be briefly discussed. Evidence on interactions and reciprocal relationships between different oscillatory modes and a possible role of the prefrontal cortex (PFC) in their regulation will finally be presented.

In a number of developmental stages and pathological conditions, an apparent parallelism between a deficient alpha and/or increased slow-wave activity on the one hand and a lack of inhibitory control on the other hand could be observed. Firstly, such parallelism is evident during normal development. The relative contribution of low frequencies (i.e. delta and theta) to the EEG power spectrum decreases with age in typical development, and the contribution of higher frequencies (mostly alpha) increases (John et al., 1980; Matousek and Petersen, 1973). This dynamic, which is generally considered as a sign of maturation (Clarke et al., 2001), is accompanied by development of inhibitory control. The literature on childhood development shows many physiological and behavioral phenomena suggesting that the relative strength of inhibitory control increases during childhood (for a review, see Clark, 1996).

The most consistent finding in EEG studies of Attention-Deficit/Hyperactivity Disorder (ADHD) has been increased low-frequency activity, predominantly theta, in children with ADHD compared with control children (for a review, see Barry et al., 2003). Reduced amounts of relative alpha and beta have also frequently been noted. The diagnostic specificity of increased relative theta and decreased alpha and beta power has not been established (Barry et al., 2003). There appears to be a distinct similarity between EEG patterns in children with ADHD and children subject to poverty and other environmental risk factors which raises the possibility that excess relative slow-waves power and reductions of alpha and beta power may be an electrophysiological signature of deviations in brain development common to a variety of disorders or contexts. Excess of spectral power in low-frequency bands and a deficit in power at higher frequencies are associated with disorders of learning and attention in children (Barry et al., 2003; Chabot et al., 2001). Studies which have examined the influence of adverse early rearing conditions or sociocultural risk factors on the development of the EEG in children have generally reported higher EEG power at low frequencies to be associated with detrimental aspects of the child's living environment (Harmony et al., 1990; Kreppner et al., 2001; Marshall et al., 2004; Otero et al., 1997; Raine et al., 2001; Vorria et al., 1998). Moreover, increases in delta and theta and decreases in alpha activity were found in the EEGs of fetal alcohol syndrome and Down syndrome children (Kaneko, 1995). Beyond lower cognitive abilities, all these conditions are associated with impaired motor control, poor attention (high distractibility), and general tendency to impulsive and disinhibited behavior, which imply deficits in inhibitory functions.

This apparent similarity of outcomes of seemingly different influences prompts one to assume that brain mechanisms underlying both the inhibitory control and the maintenance of relative prevalence of alpha oscillations are particularly sensitive to a variety of detrimental influences. Existing evidence shows that this is indeed the case. As just one example, let us consider hypoxia, which is implicated in a broad array of conditions. Hypoxia can result from diverse events or physiological conditions that compromise delivery of oxygen to the brain, including myriad diseases, various kinds of brain trauma, and unfavorable environmental circumstances (Clark, 1996). Existing evidence shows that the brain is particularly sensitive with respect to its oxygen requirement (Sudarsky, 1990), and hypoxia may have particularly damaging effects on inhibitory functioning (Clark, 1996). Hypoxia is associated with diverse behavioral changes that suggest behavioral disinhibition (Caplan, 1982; Clark, 1996). Of particular interest here is that hypoxia is associated with a distinct EEG pattern similar to the one described earlier for disadvantaged children and ADHD patients: decrease of alpha and prevalence of slow waves (Kraaier et al., 1988; Ozaki et al., 1995; Tolonen and Sulg, 1981).

Thus, in a variety of developmental stages and pathological conditions a lack of inhibitory control and concomitant behavioral problems are associated with a relative decrease of alpha and/or increase of slow waves. Apparently, both inhibitory control and alpha oscillations develop later during the ontogenesis and are particularly vulnerable to a variety of detrimental influences. A straightforward interpretation of this evidence would be that oscillations of delta and theta ranges are associated with activation whereas alpha oscillations are a correlate of inhibition. In order to explicate what kind of activation and inhibition processes they are related to, functional correlates of delta, theta, and alpha activity will be briefly discussed in the following sections. Particularly, it will be shown that delta oscillations correlate with motivational processes and salience detection, theta oscillations correlate with emotional processes and memory, and alpha oscillations correlate with inhibitory processes which contribute to a variety of cognitive operations such as attention and memory.