Invited ReviewA review of alpha activity in integrative brain function: Fundamental physiology, sensory coding, cognition and pathology
Highlights
► This review includes physiologic fundamentals and theories of alpha activity. ► Alpha activity in evolution, aging and in the vegetative system is discussed. ► Event related desynchronization versus alpha response is described. ► This review opens the way to understand alpha activity in a general frame.
Introduction
The present review and the companion report (Başar and Güntekin, in press) aim, where possible, to combine analyses related to the spontaneous alpha activity, evoked alpha responses, event-related alpha responses, ERDs; and also, ideally, they aim to encompass applications of these measuring strategies over the entire cortex, by also taking into account resting states and evoked coherencies. Namely, to understand sensory-cognitive processes, it is almost imperative to attain reliable information over the whole brain, and information concerning evolving brain (neuroethology), aging brain and pathologic brain. Basic studies of “alpha at the cellular level” are also most pertinent for understanding the crucial role of alpha in the integrative brain machinery. This view will be further considered in Section 2. A review of the history of work on alpha oscillations is also necessary to illuminate the basic views.
According to Storm van Leeuwen (1977), if one understands the alpha rhythm, one will most probably understand the other EEG phenomena. Alpha rhythm was first observed and described by the German psychiatrist Hans Berger (1929). Mountcastle (1992) described that, after Berger's first report of electroencephalogram, a great excitement pervaded the neurological word, in the late 1920s and early 1930s. The use of electroencephalography reached a peak in the 1940s; thereafter, such studies plateaued and ceased to be attractive to most experimental neuroscientists. The significance of the alpha rhythm was also poorly understood, and Ross Adey reported that several neuroscientists previously considered this pattern as a “noise”, “smoke” or idling of the brain.1
Thirty years ago, a paradigm shift occurred: According to Mountcastle (1992), our percepts are generated by the integration of the brain activity triggered by sensory stimuli with the activation of the neural images of past or current experience. This meant that brain mechanisms involved in perception could be studied directly, by measuring changes in the electrical activity of the human brain via a large number of EEG recordings, or the use of multiple microelectrodes implanted in primates. Furthermore, Mountcastle, 1992, Mountcastle, 1998 states that the paradigm change introduced by using brain oscillations has become one of the most important conceptual and analytic tools for the understanding of cognitive processes. He proposes that a major task for neuroscience is to devise ways to study and analyze the activity of distributed systems in waking brains, in particular, human brains.
There remain many misconceptions about alpha rhythm, in relation to the functions of the brain and states of consciousness that need to be addressed and put in perspective. The literature shows that alpha rhythm is not a unitary phenomenon; rather, it demonstrates considerable variation and changes, depending on age, mental state, the cognitive task being performed and the cerebral location from which the EEG signal is being recorded.
Although between the 1950s and 1980s, EEG was regarded as noise and human alpha activity only as the idling state of the brain, during the two decades between 1990 and 2010, a significant number of reports were published related to cognitive correlates of alpha activity. Most of the recent work on “alpha” seems to be focused on psychological work that is often detached from physiological and clinical observations. The newly developed hypotheses are mostly based on new strategies and do not take into consideration the most general findings or framework established a few decades ago. More than 50 years ago, Gray Walter (1950) already pointed out that the alpha rhythm in one subject is composed of, and is the end product of, many alpha rhythms. In 1964, Walter stated:
“We have managed to check the alpha band rhythm with intracerebral electrodes in the occipital–parietal cortex; in regions which are practically adjacent and almost congruent, one finds a variety of alpha rhythms, some of which are blocked by opening and closing the eyes, some are not; some are driven by flicker, some are not; some respond in some way to mental activity, some do not. What one can see on the scalp is a spatial average of a large number of components, and whether you see an alpha rhythm of a particular type or not depends on which component happens to be the most highly synchronized process over the largest superficial area; there are complex rhythms in everybody.”
Now, at the turn of the 21st century, a number of publications on alpha oscillations consider “alpha” as an almost pure cognitive signal. Further, only thalamic pacemakers are discussed as generators of alpha activity. Fundamental and still valid works of Ross Adey et al. (1960), Rémond and Lesèvre (1967), Hernandez-Peon (1961), and Moruzzi and Magoun (1949) are usually not considered in new theories. Further, new generalizing results on animal physiology and clinical neurophysiology experiments have become rare.
According to Gasser et al. (1985), the alpha band has the best test–retest reliability compared with other EEG bands, and can therefore be treated as an intra-individually-stable trait. In the last decade of the 20th century, an efficient trend was initiated by several authors for understanding the functional correlates of alpha (Lehmann, 1989, Von Stein and Sarnthein, 2000, Başar et al., 2001, Nunez et al., 2001), as also reviewed by Başar et al. (1997b) and Klimesch (1999). Further, it is described that alpha activity is the most common component of the human brain's electrical activity (Başar and Güntekin, 2006, Shaw, 2003).
The major aim of this review is to follow the fundamental questions posed by Gray Walter and Storm van Leeuwen by considering the following structural descriptions:
- 1)
Extracellular recordings of the spontaneous and evoked alphas;
- 2)
Intracellular recordings of alpha activity;
- 3)
Selectively distributed alpha system of the brain;
- 4)
Neuro-clinical bases and neurotransmitters.
Further, a survey of publications on functional correlates of alpha activity and alpha responses will be provided, including:
- a)
Alpha in sensory function;
- b)
Alpha in evolution of species;
- c)
Alpha in vegetative functions;
- d)
Alpha in the maturing brain;
- e)
Alpha in cognitive processes (companion report);
- f)
Alpha in cognitive impairment (companion report).
The present review also strongly emphasizes the observation of Gray Walter (1950), presented in the previous section, and also that, according to measurements, alpha oscillations or “alphas” are correlated with several basic functions. Research also suggests that a profound understanding of alpha activity can be only achieved by encompassing observations in the maturing brain, evolving brains, emotional brain and pathologic brains (Başar, 2011). During the last twenty years, 10-Hz observations were also recorded in the vegetative system (Barman and Gebber, 1993, Barman and Gebber, 2009) and, in the future, this observation will be of considerable importance for the understanding of brain–body integration.
The present review includes around 180 references in an attempt to address the questions: Can the level of presented results and related theories lead to a new general “alpha theory”? Can new progress be achieved in the light of the above-mentioned critics? Is the time ripe for pronouncing a general alpha theory? Başar (2011) concluded that “Alpha is one of the fundamental functional operators of the brain for signal processing and communication in sensory/cognitive processes in the brain”. Further, according to results from the research group of Barman and Geber, “alphas are operating oscillations also in the spinal cord and the organs of the vegetative system”.
The final question will be: Is the time ripe for a general theory of alpha?
This question will be repeated at the end of the companion report.
The results of present studies generally depict a number of divergent results, indicating that it is still too early to launch an alpha theory. Therefore, at the end of the review, we include only a chain of “reasonings and suggestions for understanding alpha” that may provide the basic steps for establishing tenable hypotheses in the future.
Section snippets
Some fundamental remarks on single cell recording and EEG: from Ramon y Cajal (1911) to Mountcastle (1992)
At the turn of the 20th century, the morphological studies carried out by Ramon y Cajal's (1911) and Charles Sherrington's (1948) physiological approach opened the way to the “single-neuron doctrine” by introducing the notion of “one ultimate pontifical nerve-cell” that integrates the CNS function. In this concept, integration was related to motor activity; the functional mapping was a type of movement mapping. Although this approach dominated 20th century-neuroscience, it had a major
Studies at the cellular level
Creutzfeldt et al., 1966, Creutzfeldt et al., 1969 analyzed post-stimulus time histograms (PSTHs) of lateral geniculate cells and of cortical cells and cortical visual EPs following light flashes. The single cell responses may vary with recording depth, but a common type of response is seen at all levels of the cortex. The experimental data revealed a good correlation between the 10-Hz components of the surface EP and cellular events. A phase reversal of all components is observed at a depth
Spontaneous alpha distributed in the whole cortex
Fig. 2 shows the power spectra that were simultaneously evaluated from four different locations of a subject (vertex, parietal, occipital and frontal) during waking stage with eyes closed. During the analysis of such compressed arrays of power spectra, the following observation was usually made: In the central electrode (vertex), the power was usually centered between 7 and 10 Hz, with large peaks in frequencies lower than 10 Hz. In occipital locations, the subjects usually showed high amplitude
10-Hz activity in sympathetic nerves of the heart, the spinal cord and cerebellum
In recent decades, the group led by Gebber and Barman in Michigan studied the frequency links of the spinal cord to the heart and kidneys. Such studies are rare; however, they provide core information for the oscillatory integration between the central nervous system and the vegetative system.
In their early studies, Barman and Gebber (1993) recorded a variable mixture of 10-Hz and 2- to 6-Hz discharges from sympathetic nerves in decerebrate cats. The data supported the view that lateral
What is neuroethology?
Neuroethology is the biological approach to the study of the neural basis of behavior. The ethological approach emphasizes the causation, development, evolution and the function of behavior. Neuroethologists seek to understand this in terms of neural circuits. Neuroethology is the study of natural behavior, which, in the older scientific literature, was called “innate behavior”. The neural approaches used in neuroethology are as diverse as the field of neuroscience itself. Often,
Alpha in the maturing brain
There are important changes in the structure and electrical activity of the human brain from the fetus to the brain of elderly subjects. How do these changes affect the transfer functions, i.e. communication processes, in the maturing brain? A two-year-old child does not have a full command of their native language and cannot solve mathematical problems; and neither does a two-year-old child does show alpha activity. Furthermore, the frontal lobes are not completely developed; synaptic
Event-related desynchronization (ERD)
An important property of the alpha activity is the phenomenon of “alpha blocking”, first described in the early days of EEG research. Opening the eyes blocks the existent alpha-activity; a simple light stimulation triggers the same effect. One of the first demonstrations related to the possibility of functional effect was provided by interesting measurements of Creutzfeldt (1993), who showed that, during mental arithmetic operations, the alpha activity of subjects was blocked, whereas beta
Selectively distributed alpha responses and alpha coherences in the whole brain
Ross Adey's (1960) group undertook pioneering work on the theta rhythms of the limbic system of the cat brain during conditioning. These authors were the first to use spectral and coherence functions, performing relevant experiments demonstrating that rhythmic field potentials of the cat brain are related to behavior (see also Elazar and Adey, 1967, Miller, 1991).
The use of the coherence function in comparing EEG activity between various nuclei of the brain was useful in refuting the view that
Acknowledgments
We thank Ms. Elif Tulay for carefully reading and correcting the manuscript, and Mrs. Melis Diktaş for her valuable secretarial help.
References (194)
- et al.
Measurement of maximum variability within event-related potentials in schizophrenia
Psychiatry Research
(1991) - et al.
Frontal white matter volume and delta EEG sources negatively correlate in awake subjects with mild cognitive impairment and Alzheimer's disease
Clinical Neurophysiology
(2006) - et al.
Hippocampal volume and cortical sources of EEG alpha rhythms in mild cognitive impairment and Alzheimer disease
NeuroImage
(2009) - et al.
A 10-Hz rhythm reflects the organization of a brainstem network that specifically governs sympathetic nerve discharge
Brain Research
(1995) - et al.
EEG alpha activity and the ERP to target stimuli in an auditory oddball paradigm
International Journal of Psychophysiology
(2000) - et al.
Preferred EEG brain states at stimulus onset in a fixed interstimulus interval auditory oddball task and their effects on ERP components
International Journal of Psychophysiology
(2003) - et al.
Age and gender effects in EEG coherence. I. Developmental trends in normal children
Clinical Neurophysiology
(2004) - et al.
Alpha oscillations in brain functioning: an integrative theory
- et al.
Oscillatory brain dynamics, wavelet analysis, and cognition
Brain and Language
(1999) - et al.
Gamma, alpha, delta, and theta oscillations govern cognitive processes
International Journal of Psychophysiology
(2001)