Brain electric microstates and momentary conscious mind states as building blocks of spontaneous thinking: I. Visual imagery and abstract thoughts
Introduction
Brain electric field recording allows the monitoring of brain work continually and non-invasively with that very high time resolution which is needed to study cognitive–emotional processes. At each time instant, the data yield a map of the potential distribution on the head surface (Lehmann, 1971). Thus, brain activity can be visualized as a series of momentary brain electric field maps. An instantaneous map reflects the sum of all momentarily active brain processes, superficial and deep (Smith et al., 1983). If the map's spatial configuration (the momentary landscape) changes, different neural elements must have become active. It appears reasonable to assume that different sets of active neural elements perform different functions.
Using data-driven analysis strategies we found that the changes of the spatial configuration of the brain field are discontinuous; they occur in a step-wise fashion. Accordingly, the continuous stream of maps of momentary electric field potential distributions can be segmented into time epochs of varying durations in the sub-second range during which the field shows a near-stable landscape (Lehmann and Skrandies, 1980, Lehmann, 1984). These epochs of quasi-stable field landscape were called microstates and were observed with very different analysis approaches and experimental conditions during event-related brain activity (Lehmann and Skrandies, 1980, Brandeis and Lehmann, 1989, Michel et al., 1992, Brandeis et al., 1995, Pascual-Marqui et al., 1995, Koenig and Lehmann, 1996, Fallgatter et al., 1997, Kondakor et al., 1997Pegna et al., in press) as well as during spontaneous brain activity (Lehmann, 1984, Lehmann et al., 1987, Merrin et al., 1990, Strik and Lehmann, 1993, Wackermann et al., 1993, Koukkou et al., 1994, Kinoshita et al., 1995).
It thus appears that continuous brain electric activity consists of a concatenation of building blocks, the microstates, which are defined by their quasi-stable field landscapes and which are suggested to incorporate different modes, contents or steps of information processing. This raises the suggestion that the subjective experience of what William James called the `stream of consciousness' actually consists of discernible elements. Of course it is clear that this stream of consciousness over time carries varying contents as has been studied repeatedly (see Pope and Singer, 1978). During free-floating, no-task conditions (so-called day dreaming), experiences of visual imagery are frequent and reports of subjective experiences involving visual imagery are easy to distinguish from reports of non-imaginal thoughts which concern abstract topics such as planning (Foulkes and Fleisher, 1975, Lehmann et al., 1995). The PET cerebral correlate of visual imagery was also reported to differ from that of non-imaginal thinking (Goldenberg et al., 1989).
The brain mechanisms of visual imagery were the topic of many studies (see Pylyshyn, 1981, Paivio, 1986, Kunzendorf and Sheikh, 1990, Kosslyn, 1994). Early general hypotheses on right hemispheric specialization for visual imagery, typically based on EEG power measurements (for a very critical overview see Ehrlichman and Barrett, 1983) were replaced by proposals that different modes of visual imagery utilize different brain mechanisms involving not solely the occipital regions (Roland and Friberg, 1985, Petsche et al., 1992) and involved left- as well as right-predominant mechanisms. Input-driven imagery tasks were reported to cause left-sided occipital event-related potential maxima (Farah et al., 1989), similar to PET studies where task solution or attention to images caused stronger left-sided activity, but instruction-less or memory-based imagery was more right-sided (e.g. Goldenberg et al., 1987, Kosslyn et al., 1995). Mental rotation, a particularly well studied imagery operation, typically showed a right-hemisphere preponderance (e.g. Papanicolaou et al., 1987, Corballis and Sergent, 1989Pegna et al., in press), similar to other examined imagery conditions (e.g. Sergent, 1989) and to task-free visual input event-related potentials (Mecacci et al., 1990).
Investigations of the microstate structure of event-related potential map series lead to the identification of certain microstates with certain processing steps (e.g. by Brandeis and Lehmann, 1989, subjective visual contours; Brandeis et al., 1995, congruent vs. incongruent sentence endings; Koenig and Lehmann, 1995, reading of abstract vs. imagery words; Koenig and Lehmann, 1996, reading of verbs vs. nouns; Pegna et al., in press, mental rotation).
The topic of the present article is the functional significance of different types of brain electric microstates during spontaneous, `free-running' brain activity. A no-task, no-input, no-response paradigm was chosen in order to avoid overlays of potentially influential brain subroutines that are necessary for continual remembering of and attending to a task, task execution and preparation and implementation of motor acts (Antrobus, 1987) and in order to examine mind states as such without externally driven representations of information. Hence, the article examines the concept that spontaneous, conscious states of the mind experienced as recallable thoughts can be described as physical states of the brain.
The present study presents evidence suggesting that two specific, spontaneous, conscious mind states are associated with two different classes of brain microstates that are defined in the brain electric field. In our no-input, no-task, no-response paradigm, subjects (when hearing a random prompt) reported recall of their immediately preceding spontaneous, conscious, unconstrained, private experiences. The reports were classified into experiences involving visual imagery or abstract thinking. An earlier analysis which used the entire 2-s epochs before the prompts showed that the two classes of subjective reports were associated with different locations of frequency domain EEG source models (Lehmann et al., 1993). The present analysis shows that the two mentation classes were associated with two different classes of brief brain electric field microstates immediately before the prompt signal, but not 2 s earlier.
Section snippets
Subjects
Thirteen male volunteer subjects participated, recruited from the students at Zurich University by an advertisement. They had a mean age of 26 years (S.D. 3.8, range 21–36). The subjects were sequentially accepted into the study without pre-screening for EEG patterns. Smokers and persons with a history of drug use, neurological or psychiatric disease and on current medication were not accepted.
The analysis reported here concerns the placebo data set of a double blind, placebo-controlled study
Results
The mean values of the spatial parameters of the microstates associated with the two classes of subjective reports are illustrated in Fig. 3, in the right panel for the last microstates before the prompt and at the left for the earliest microstates of the 2-s epochs before the prompt (numerical values in Table 1).
For the last microstates before the prompt, the four landscape-describing microstate parameters (angle, distance between window locations, gravity center location on the left–right
Discussion
The two classes of recalled, spontaneous, subjective experiences distinguished, across subjects, between two different classes of the brief, brain electric microstates that were observed immediately before the recall prompt. This distinction did not exist 2 s before the prompt signal. The microstates were defined by their mapped, brain electric landscapes. Different landscapes of the potential distributions must have been generated by geometrically different active neural populations. Thus, the
Acknowledgements
The work was partly supported by grants to D.L from the Swiss National Science Foundation, the EMDO Foundation (Zurich) and the Hartmann–Mueller Foundation (Zurich). W.K.S. had a Fellowship from the Deutsche Forschungsgemeinschaft. B.H. had a stipend from the Gertrud–Ruegg Foundation (Zurich).
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