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EEG alpha-wave in the visual cortex: check of the hypothesis of the scanning process
International 0 1991
PSYCHO
11 (1991)
Journul of Psychophysiology,
Elsevier
Science
Publishers
195
195-201
B.V. 0167.8760/91/$03.50
00343
EEG alpha-wave
in the visual cortex: check of the hypothesis of the scanning process
Igor A. Shevelev, Nina B. Kostelianetz, Victorina and George A. Sharaev Department
of Sensory Physiology, Institute of Higher Neruous Activity and Neurophysrology. Moscow 117865 (U.S.S.R.) (Accepted
Key words: EEG;
In computer-controlled of different The onset criterion from
experiments
of figures presentation of an increase
the gaze
(up
better
peripherally phases
localized
was revealed.
with different
and
the
phases
succession
figures - at earlier phases.
At 16 degrees
the whole
visual
cortex
simulation
of the mentioned
scanning
are discussed
possibilities
as a reflection
confirmed
that
imitated
readout
over
of an information
the
visual
cortex
for
and for its subsequent
transmission to other cortical fields. They supposed that this process takes place every 100 ms or with a frequency of the EEG alpha-activity (10 Hz). The neuronal signals that are reflected in a
Correspondence:
I.A. Shevelev,
ology,
Institute
of Higher
ology,
U.S.S.R.
Academy
Moscow
117865.
U.S.S.R.
Department
Nervous of Sciences,
Activity
of Sensory
Physi-
and Neurophysi-
Butlerova
presented
Possibility
the spreading
region.
the distance
or more
centrally
localized
while
dependence
of recognition
(1947) is also Pitts’s
bigger
hypothesis
of a synchronous
and thus confirmed
figures
According
of the figures
alpha-wave,
process
geometrical
in the visual field was studied.
figures
or relatively
were more
on the alpha-wave about
excitability
discussed.
to the contour
Data
and McCulloch’s
a periodical fluctuation obtained
in and
ideas on the
in the visual cortex.
More than 40 years ago Pitts and McCulloch (1947) suggested that an excitatory scanning wave spreads
Small
of EEG
process
in the occipital
between
with Pitts and McCulloch
the first explanation
process
of tachistoscopically
from the gaze no reliable
INTRODUCTION
periodically
phases
Scanning
3 up to 16 degrees)
was revealed
over the visual cortex.
frequency
of the scanning
(from
of alpha-wave.
earlier
in connection
wave spreading
with alpha-rhythm
Visual cortex;
of the EEG alpha-wave
dependence
of phases
at relatively
The data obtained
eccentricity
an inverse
Acudem_y of Sciences,
1990)
by seven human observers
or of different
probability,
when
4 September
Visual recognition;
presented
frequency)
alpha-wave
coincided
to 9 degrees) recognized
Phase;
the recognition degrees)
of recognition
(with alpha-wave
EEG
Alpha-wave;
size (from 0.5 to 9 angular
significantly
M. Kamenkovich
St 5a. GSP-7,
supposed wave are algebraically summated with PSPs of each cortical unit or with excitatory-inhibitory cortical spatial pattern (for their population) formed by the visual resulting PSPs sum exceeds
afferentation. If the the firing threshold
level, an output signal will be transmitted from the 17th field to other cortical areas. So, in accordance with the concentric wave propagation, more and more units concentrically located in the visual cortex increase their firing probability that looks like sequential readout of information from the cortical ‘screen’. Up to now this idea has not been proved. Meanwhile, it seems to be of great importance because of the supposed high-specific operational function of the EEG alpha-rhythm in the visual cortex. According to some demonstrations
196
METHODS 36 computer-controlled experiments and 12 control ones were performed with seven healthy adult observers of both sex. In a sound- and light-proof chamber, pictures were presented to young (19-25 years) volunteers with normal vision on the screen of a three-channels tachistoscope (Takei, Japan). Sets of the stimuli are shown on Fig. 2. Each of them included 10 contour-type geometrical figures (black on white 12.7 cd/m’. the line width 4’). In experiments with different
Fig. 1 Schemes (a-c) demonstrating relation between sile of the optimally recognized figure (e.g.. triangle) and moments of the alpha-wave spreading (widened scratched ripg) over the visual cortex in accordance with Pitts’s and McCulloch’s hypothesis (1947). d-assumed dependence between time (T) or succession of the EEG alpha-wave phases and figures’ sze (D) by the criterion of their best recognition.
(see, for example, Bechtereva and Zontov, 1962; Plotkin, 1976; Varela et al., 1981; Bohdanecky et al., 1983; Radil et al., 1984) alpha-activity and its phases have influence on the sensory processes, but these authors do not take into account spatial properties of the wave process.
the
Recently, we advanced a conclusion from Pitt’s and McCulloch’s hypothesis (Shevelev, 1988; Shevelev et al., 1985; 1988a,b). If the scanning wave spreads from the central to the peripheral part of the visual cortical projection, as the authors supposed (Fig. la-c), then: (i) the visual figure, the contours of which are located at some distance from the gaze, must be better recognized at some phases of the EEG alpha-wave; and (ii) there must be a certain relation between the succession of eccentricities of these contours and the succession of alpha-wave phases when the figures are better recognized. In other words, the best recognition of figures of different sizes or with different eccentricities in the visual field must coincide with different and successive phases of the EEG alpha-wave in the human occipital region (Fig. Id). Our study is devoted
to confirming
sion and thus Pitts and McCullochs
this concluidea.
eccentricities (3, 6. 9 and 16 angular degrees of the figure’s center from the gaze) the size of the same figures was 30’. Figures were presented on a imagined diagonal line initiated at the fixation point in the left lower corner of the tachistoscope screen (Fig. 2b). In another experimental paradigm, the set of figures of different sizes (0.5. 1.5. 5 and 9 degrees) centered in the visual field were used (Fig. 2a). The eccentricities of their contours were equal to 0.25, 0.75, 2.5 and 4.5 degrees, correspondingly. The data obtained in two experimental sessions (with sizes and eccentricities) were combined and averaged. Subjects were previously trained in recognition of used figures (two sessions). They were instructed to fixate their gaze at the fixation point after a sound present for l-3 s before the figure appeared. The exposition time was adjusted individually for stimuli of different size or eccentricity by a criterion 0.660.7.
of recognition
probability
about
The exact moment of stimulus onset was controlled by a computer (IN-90, Intertechnic, France), that found in randomized order one of four phases of the EEG alpha-wave (Fig. 2c) and switched on the tachistoscope. To synchronize the stimuli presentation we used the following phases of the alpha-wave: (1) a zero-line crossing on the descending phase; (2) a negative peak; (3) a zeroline crossing on the ascending phase and; (4) a positive peak. A monopolar EEG recording was performed (an active electrode in the right occipital region placed at 3 cm higher and 3 cm to the right from the inion; a reference electrode on the left ear). The power spectrum of the EEG was obtained
197
16' / a / ,/ b
C
/ /4.3 +’
-u1
3
2
Fig. 2. Methods: (a) Sets of figures of different size centered in the visual field; (b) of constant size but different eccentricities in the visual field; and (c) EEG alpha-wave phases used fpr stimuli synchronization.
previously and the dominant frequency in the alpha-range was determined with the precision of 1 Hz. The alpha-activity was extracted from the EEG by a individually adjusted selective frequency filter with a central frequency equal to the peak value in the EEG power spectrum. Then the output signal of the filter was fed into the computer through its ADC. So, the computer treated a filtered EEG in a frequency region of the dominated alpha-activity. Before each session, the peak amplitudes of the filtered EEG were measured, its absolute maximum was estimated and the triggering threshold for visual stimulation was
determined at the level of 0.7 of this absolute maximum. Each stimulus presentation was performed according to the following rules. First of all, the computer measured the signal amplitude in the current sample (30 ps) of filtered EEG and compared it with the threshold. If this signal was higher than the threshold, the computer looked for a point corresponding to one of four phases in a signal (see Fig. 2, c) and triggered the tachistoscope with a delay of no more than 1 ms. The experiment lasted for 60-70 min with two intervals for a rest; during the session 160 figures were presented in randomized order at four different eccentricities (or of four sizes) and at four phases of the alpha-wave. Thus, for each combination of size (or eccentricity) and phase, we used ten presentations of different figures. After the subject’s report about the stimulus form (reports “I don’t know” were banned) the experimenter informed the computer about a true or an untrue recognition. After the experiment the computer plotted a recognition mistake matrix (stimulus eccentricity versus alpha-wave phase). This matrix was then normalized: the sum of errors for each eccentricity was taken as 100%. This was done to rule out the effects of a possible error in equalizing the levels of the recognition probability for different stimuli sizes or eccentricities. The source of such an error was an impossibility of an extremely precise exposition adjustment by the criterion of equal recognition level. In control experiments figures were presented by the computer with the same mean rate but irrespective of EEG parameters. The mean level of recognition probability and its error (0.59 k 0.015) were determined in such control conditions. For comparison of experimental and control data, the t-criterion was used.
RESULTS Average results of our study are presented in Table I and in Fig. 3 for all 36 experiments with seven subjects. A reliable connection may be seen between the figures contour eccentricity and alpha-wave phase succession by the criterion of their recognition probability. Typically, (six ob-
19x TABLE
II
Change
of recogmtion
of the the figures
prohohrht_~
contows
from
on dependence gaze
and
on the drstance
the EEG
alpha-wuw
phuse. (Mean errors
data
for
10 experiments
in %. * marks estimations
estimations
that correspond Distance
Fig.
3. Increase
ability
eccentricity angular
(a) and decrease
(ordinate)
in
relation
(b) of the recognition
to
the
of the figures contours
degrees)
control
level
and with phases of EEG
alpha-wave
(diagonal
phases
(Mean
WO”e
gore (degrees)
0.75
2.5
4.5
2
+ 6.4
+ 3.5
~ 1.8
- 3.4
3
+ 1.0
+ 2.0
+ 1.7
-5.5
*
4
~ 0.9
- 3.4
- 3.5
+6.5
*
1
~ 6.4 *
~ 3.1
+ 3.5
+ 2.4
outer sides (upper left and lower right matrix corners). Table I shows that a reliable recognition minima (+AP) as well as its maxima (-A P) are grouped in a diagonal direction right to the lower left corner).
(from
the upper
I of recogmtion
prohabilrty
data for 48 experiments
are estimations Alpha-
contourfromthe
0.25
ability not only separated two diagonal branches of its increase, but also surrounded them on both
of the alpha-
degrees eccentricity, no reliable changes of recognition were observed. On the time-space matrix (Fig. 3a) two parallel branches of increased recognition probability were
Change
improvement)
between two positive successions (arrow 3). Fig. 3b shows that the decrease in recognition prob-
wave, whereas centrally localized ones - at relatively later phases. In the case of the 16 angular
TABLE
of are
crease of the recognition probability in comparison with the control level is seen on the matrix
succession: images, the contours of which are relatively far from the gaze, are reliably better recognized as compared with mean control level (25.0 earlier
of the figures
dP
Evidence of the separate existence of these two branches may be seen in Fig. 3b: a reliable de-
servers from seven and the mean data) there exists an inverse relation between eccentricity and phase
at relatively
to recognition
I.M..
underlined
revealed (1 and 2). One of them (the main diagonal) goes from 9 to 0.25 degrees in the alpha-wave phases succession 2-3-4-l (arrow l), the second from 9 to 3 degrees in succession 3-4-l (arrow 2).
the axis,
axis, see Fig. 2~).
f 0.3%)
observer
prob-
with
from gaze (horizontal
wth
with P > 0.95.
on dependence
that correspond Distnnce
0.25
on the dtstance
with seven observers, to recognition
of the figures
contours
from
gaze
m %, * marks estimations
and the EEG
with P > 0.95,
alpha-waoe
phase
* * P > 0.99, underlined
improvement)
contour from
0.75
of the figures
3 P of errors
the gaze (degrees)
2.5
3
4.5
6
9
16
phase 2
+ 1.3
+1.0
3
+ 0.8
+2.1
4
+ 0.3
1
-2.0
**
+2.9 **
**
-1.6
*
-2.7
i2.2
**
PO.1
+1.7
*
-1.2
+0.3 **
+3.1
+ 1.0
- 2.3 * *
- 0.8
+1.0
~ 1.2
-0.2
+0.1
~ 3.2 * *
+ 2.0 *
-0.5
+1.4
+ 0.2
+ 2.2 * *
+0.4
-3.2 **
- 3.6 * *
+2.1 **
**
199
TABLE
DISCUSSION
III
Change of recognition probability on dependence on the distance of Ihe the figures contours from gaze and the EEG alpha-wave phase (Mean data for 10 experiments with observer A.M., A P of errors in %, * marks estimations with P > 0.95, * * P > 0.99, underlined are estimations that correspond to recognition improvement) Alphawave
phase
Distance of the figures contour from the gaze (degrees) 0.25
0.75
2.5
4.5
2
- 6.2 * *
-5.5
+5.9 *
+ 2.6
3
-0.2
+1.6
-5.0
+0.8
*
4
+ 2.2
- 0.4
- 4.8
-4.3
1
+ 4.0
+4.1
+ 3.8
+0.5
Table II shows average data for 10 experiments with typical observer I.M. It can be seen that these results in principle coincide with data of Table I. But in one of the seven observers (A.M.), we obtained a direction opposite to the typical direction of recognition probability increase on the space-time matrix (Table III). In this case small figures at earlier alpha-wave phases and bigger figures at relatively later phases are recognized better. In other words: here, the size-phase relation is direct, while in typical cases it is inverted.
According to the original idea of Pitts and McCulloch (1947) the excitation wave, spreading over the visual cortex, first of all will increase the recognition probability for small figures (Fig. la and Fig. 4a,l). Concentric widening of the wave front in next moments will lead to an increase of recognition probability for bigger and bigger images (Fig. lb, c and Fig. 4a, 2-4). The data presented confirmed the existence of the spreading wave process, because both of two direct conclusions from Pitts’s and McCulloch’s hypothesis were proved. Indeed, all observers show existence of relation between the succession of alpha-wave phases and the succession of the figures contour eccentricity by the criterion of their recognition probability. From our point of view it is very strong, albeit indirect evidence, of the validity of their hypothesis. According to the original hypothesis, however, the scanning wave in the visual cortex should initially improve the recognition of the small figures and then of the bigger ones (Fig. 1 and 4a). In our study, only one from seven observers showed such tendency of changes (Table III) predicted on the basis of Pitts’s and McCulloch’s (1947) idea. Data presented in Fig. 3a and Tables I and II, show that the inverted space-time relation (Fig. 4b) in appropriate matrix was typical. Thus, it may be assumed that every 80-120 ms
Fig. 4. Schemes of excitability dynamics in the visual cortex according to: (a) Pitts’ and McCulloch’ hypothesis; (b) our data; and (c) the possibility of the excitability synchronous modulation. Visual cortex of one hemisphere is shown. l-4: moments corresponding to successive phases of the EEG alpha-wave (see Fig. 2~). Excitability increase is shown as an upward deflection, decrease - as a downward one.
200
(alpha-rhythm period in different subjects) two concentric circular waves (this configuration seems to us most probable) are generated in the cortical projection of the visual field. Even the place of their generation in the cortex can be indicated: it is the cortical projection of the near periphery of the visual field (9912 degrees from gaze). The first wave begins moving from the near periphery toward the center of the cortical representation of the visual field. It reaches the center during 3/4 of alpha-wave period (about 75 ms) with a mean angular speed of approx. 120 deg./s. The second wave spreads in the same direction with the same speed and with some delay but travels only in the near periphery of the field (993 deg.). In the cortical space linearized in accordance with a magnification factor, the spreading of the two waves is practically even. This can be seen in Fig. 3a where the abscissa (space) is plotted non-linearly and the law of this non-linearity takes into account the magnification factor for the human visual cortex (Cowey and Rolls, 1974). Let us discuss the correspondence between our filtered EEG and native EEG signal. It is important because, if current alpha frequency of EEG and tuning frequency of our filter do not coincide, the inevitable phase shift between both signals will result in some errors of phase estimation. But if we choose a proper (most probable or dominant alpha frequency) value as a filter tuning frequency, this distortion would act uniformly in both ‘directions’ (increasing and decreasing current phase angle). That is true for a drift of a current EEG alpha frequency around its dominant value. The fact that even in this ‘distorted’ situation we could show statistically significant differences in figure recognition presented at different phases of alpha-wave can support the described phenomenon. It must be noted, additionally, that the phase shift to some extent is not of great importance for our conclusions. In fact, not the exact phase value but their succession matters. That is why here we discuss ‘later’ or ‘earlier’ phases and can not assert their angle value purely quantitatively. Mean individual and mean group results show that different disturbances that can potentially mask the revealed phenomenon (shift in maximum of EEG power spectrum during ex-
periment, possible but rare eye movement during figure exposition, as well as phase shift between filtered and unfiltered EEG) failed to do it that proved it to be of a non-accidential nature. It is difficult to discuss now neurophysiological mechanisms of triggering and of spreading of the supposed wave process in the visual cortex. Up to now it is not the common view and there is strong evidence in favour of the cortical or, contrary, subcortical localization of alpha-rhythm pacemaker (see for review: Plotkin, 1976; Guselnikov and Iznak, 1983). The fact that there is an initial appearance of the excitatory wave in the peripheral circular zone of the cortex can tell us about the external, non-cortical source of its generation. As to the mechanism of the wave spreading over the cortex, it can be explained theoretically on the same basis, as the location of the alpha-wave generator: either by the subcortical (external) control of such activity and movement or by pure intracortical generation and spread of excitation as in continuous media (Gelfand and Tseitlin, 1960, Griffith, 1965). It must be noted that up to now the waves spreading over the cortex with a speed of some meters per second (value calculated from the known size of the human visual cortex and the time of the wave propagation estimated here) were not found, although their speed up to 33 mm/s was demonstrated in the rat by thermoencephaloscopy (Gorbach et al., 1989; Shevelev et al., 1986, 1989a,b). In principle the obtained data might be due to a non-spreading wave process. In this case (Fig. 4c) the excitability of all visual cortex elements is supposed to be modulated synchronously with the alpha-rhythm, while the illusion of the wave spreading is due to difference in delay of the afferentation to different parts of the cortical field. Simulation shows that such supposition contradicts the known temporal properties of the Xand Y-visual channels (Enroth-Cugell and Robson, 1966) and is, thus, unlikely. Thus, for an illusion of the wave spreading from peripheral to the central part of the cortical field (direction that was typically revealed in our study) it is necessary to have a slower afferentation propagation in the Y-channel, than in the X one, and that is not the case in reality.
201
Functional meaning of the periodical readout process in the visual cortex was previously postulated (Pitts and McCulloch, 1947). The authors of the original hypothesis believed that it ensured an invariance of visual recognition to the size, rotation and retinal localization of recognized figures as well as leading to the possibility of necessary volume reduction in the information channel between the 17th and other visual fields in the cortex. The last consequence is of essential importance because it ensures a very profitable spatiotemporal information presentation at the output of the visual cortex instead of a pure spatial one and consents the necessary volume of this output with the reality. It must be emphasized that the obtained data and the hypothesis that they confirm, provide an alternative to the commonly accepted interpretations of the EEG alpha-wave functions because it takes into account not only temporal, but also spatio-temporal aspects of the visual recognition and informational meaning of the EEG.
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PSYCHO
11 (1991)
Journul of Psychophysiology,
Elsevier
Science
Publishers
195
195-201
B.V. 0167.8760/91/$03.50
00343
EEG alpha-wave
in the visual cortex: check of the hypothesis of the scanning process
Igor A. Shevelev, Nina B. Kostelianetz, Victorina and George A. Sharaev Department
of Sensory Physiology, Institute of Higher Neruous Activity and Neurophysrology. Moscow 117865 (U.S.S.R.) (Accepted
Key words: EEG;
In computer-controlled of different The onset criterion from
experiments
of figures presentation of an increase
the gaze
(up
better
peripherally phases
localized
was revealed.
with different
and
the
phases
succession
figures - at earlier phases.
At 16 degrees
the whole
visual
cortex
simulation
of the mentioned
scanning
are discussed
possibilities
as a reflection
confirmed
that
imitated
readout
over
of an information
the
visual
cortex
for
and for its subsequent
transmission to other cortical fields. They supposed that this process takes place every 100 ms or with a frequency of the EEG alpha-activity (10 Hz). The neuronal signals that are reflected in a
Correspondence:
I.A. Shevelev,
ology,
Institute
of Higher
ology,
U.S.S.R.
Academy
Moscow
117865.
U.S.S.R.
Department
Nervous of Sciences,
Activity
of Sensory
Physi-
and Neurophysi-
Butlerova
presented
Possibility
the spreading
region.
the distance
or more
centrally
localized
while
dependence
of recognition
(1947) is also Pitts’s
bigger
hypothesis
of a synchronous
and thus confirmed
figures
According
of the figures
alpha-wave,
process
geometrical
in the visual field was studied.
figures
or relatively
were more
on the alpha-wave about
excitability
discussed.
to the contour
Data
and McCulloch’s
a periodical fluctuation obtained
in and
ideas on the
in the visual cortex.
More than 40 years ago Pitts and McCulloch (1947) suggested that an excitatory scanning wave spreads
Small
of EEG
process
in the occipital
between
with Pitts and McCulloch
the first explanation
process
of tachistoscopically
from the gaze no reliable
INTRODUCTION
periodically
phases
Scanning
3 up to 16 degrees)
was revealed
over the visual cortex.
frequency
of the scanning
(from
of alpha-wave.
earlier
in connection
wave spreading
with alpha-rhythm
Visual cortex;
of the EEG alpha-wave
dependence
of phases
at relatively
The data obtained
eccentricity
an inverse
Acudem_y of Sciences,
1990)
by seven human observers
or of different
probability,
when
4 September
Visual recognition;
presented
frequency)
alpha-wave
coincided
to 9 degrees) recognized
Phase;
the recognition degrees)
of recognition
(with alpha-wave
EEG
Alpha-wave;
size (from 0.5 to 9 angular
significantly
M. Kamenkovich
St 5a. GSP-7,
supposed wave are algebraically summated with PSPs of each cortical unit or with excitatory-inhibitory cortical spatial pattern (for their population) formed by the visual resulting PSPs sum exceeds
afferentation. If the the firing threshold
level, an output signal will be transmitted from the 17th field to other cortical areas. So, in accordance with the concentric wave propagation, more and more units concentrically located in the visual cortex increase their firing probability that looks like sequential readout of information from the cortical ‘screen’. Up to now this idea has not been proved. Meanwhile, it seems to be of great importance because of the supposed high-specific operational function of the EEG alpha-rhythm in the visual cortex. According to some demonstrations
196
METHODS 36 computer-controlled experiments and 12 control ones were performed with seven healthy adult observers of both sex. In a sound- and light-proof chamber, pictures were presented to young (19-25 years) volunteers with normal vision on the screen of a three-channels tachistoscope (Takei, Japan). Sets of the stimuli are shown on Fig. 2. Each of them included 10 contour-type geometrical figures (black on white 12.7 cd/m’. the line width 4’). In experiments with different
Fig. 1 Schemes (a-c) demonstrating relation between sile of the optimally recognized figure (e.g.. triangle) and moments of the alpha-wave spreading (widened scratched ripg) over the visual cortex in accordance with Pitts’s and McCulloch’s hypothesis (1947). d-assumed dependence between time (T) or succession of the EEG alpha-wave phases and figures’ sze (D) by the criterion of their best recognition.
(see, for example, Bechtereva and Zontov, 1962; Plotkin, 1976; Varela et al., 1981; Bohdanecky et al., 1983; Radil et al., 1984) alpha-activity and its phases have influence on the sensory processes, but these authors do not take into account spatial properties of the wave process.
the
Recently, we advanced a conclusion from Pitt’s and McCulloch’s hypothesis (Shevelev, 1988; Shevelev et al., 1985; 1988a,b). If the scanning wave spreads from the central to the peripheral part of the visual cortical projection, as the authors supposed (Fig. la-c), then: (i) the visual figure, the contours of which are located at some distance from the gaze, must be better recognized at some phases of the EEG alpha-wave; and (ii) there must be a certain relation between the succession of eccentricities of these contours and the succession of alpha-wave phases when the figures are better recognized. In other words, the best recognition of figures of different sizes or with different eccentricities in the visual field must coincide with different and successive phases of the EEG alpha-wave in the human occipital region (Fig. Id). Our study is devoted
to confirming
sion and thus Pitts and McCullochs
this concluidea.
eccentricities (3, 6. 9 and 16 angular degrees of the figure’s center from the gaze) the size of the same figures was 30’. Figures were presented on a imagined diagonal line initiated at the fixation point in the left lower corner of the tachistoscope screen (Fig. 2b). In another experimental paradigm, the set of figures of different sizes (0.5. 1.5. 5 and 9 degrees) centered in the visual field were used (Fig. 2a). The eccentricities of their contours were equal to 0.25, 0.75, 2.5 and 4.5 degrees, correspondingly. The data obtained in two experimental sessions (with sizes and eccentricities) were combined and averaged. Subjects were previously trained in recognition of used figures (two sessions). They were instructed to fixate their gaze at the fixation point after a sound present for l-3 s before the figure appeared. The exposition time was adjusted individually for stimuli of different size or eccentricity by a criterion 0.660.7.
of recognition
probability
about
The exact moment of stimulus onset was controlled by a computer (IN-90, Intertechnic, France), that found in randomized order one of four phases of the EEG alpha-wave (Fig. 2c) and switched on the tachistoscope. To synchronize the stimuli presentation we used the following phases of the alpha-wave: (1) a zero-line crossing on the descending phase; (2) a negative peak; (3) a zeroline crossing on the ascending phase and; (4) a positive peak. A monopolar EEG recording was performed (an active electrode in the right occipital region placed at 3 cm higher and 3 cm to the right from the inion; a reference electrode on the left ear). The power spectrum of the EEG was obtained
197
16' / a / ,/ b
C
/ /4.3 +’
-u1
3
2
Fig. 2. Methods: (a) Sets of figures of different size centered in the visual field; (b) of constant size but different eccentricities in the visual field; and (c) EEG alpha-wave phases used fpr stimuli synchronization.
previously and the dominant frequency in the alpha-range was determined with the precision of 1 Hz. The alpha-activity was extracted from the EEG by a individually adjusted selective frequency filter with a central frequency equal to the peak value in the EEG power spectrum. Then the output signal of the filter was fed into the computer through its ADC. So, the computer treated a filtered EEG in a frequency region of the dominated alpha-activity. Before each session, the peak amplitudes of the filtered EEG were measured, its absolute maximum was estimated and the triggering threshold for visual stimulation was
determined at the level of 0.7 of this absolute maximum. Each stimulus presentation was performed according to the following rules. First of all, the computer measured the signal amplitude in the current sample (30 ps) of filtered EEG and compared it with the threshold. If this signal was higher than the threshold, the computer looked for a point corresponding to one of four phases in a signal (see Fig. 2, c) and triggered the tachistoscope with a delay of no more than 1 ms. The experiment lasted for 60-70 min with two intervals for a rest; during the session 160 figures were presented in randomized order at four different eccentricities (or of four sizes) and at four phases of the alpha-wave. Thus, for each combination of size (or eccentricity) and phase, we used ten presentations of different figures. After the subject’s report about the stimulus form (reports “I don’t know” were banned) the experimenter informed the computer about a true or an untrue recognition. After the experiment the computer plotted a recognition mistake matrix (stimulus eccentricity versus alpha-wave phase). This matrix was then normalized: the sum of errors for each eccentricity was taken as 100%. This was done to rule out the effects of a possible error in equalizing the levels of the recognition probability for different stimuli sizes or eccentricities. The source of such an error was an impossibility of an extremely precise exposition adjustment by the criterion of equal recognition level. In control experiments figures were presented by the computer with the same mean rate but irrespective of EEG parameters. The mean level of recognition probability and its error (0.59 k 0.015) were determined in such control conditions. For comparison of experimental and control data, the t-criterion was used.
RESULTS Average results of our study are presented in Table I and in Fig. 3 for all 36 experiments with seven subjects. A reliable connection may be seen between the figures contour eccentricity and alpha-wave phase succession by the criterion of their recognition probability. Typically, (six ob-
19x TABLE
II
Change
of recogmtion
of the the figures
prohohrht_~
contows
from
on dependence gaze
and
on the drstance
the EEG
alpha-wuw
phuse. (Mean errors
data
for
10 experiments
in %. * marks estimations
estimations
that correspond Distance
Fig.
3. Increase
ability
eccentricity angular
(a) and decrease
(ordinate)
in
relation
(b) of the recognition
to
the
of the figures contours
degrees)
control
level
and with phases of EEG
alpha-wave
(diagonal
phases
(Mean
WO”e
gore (degrees)
0.75
2.5
4.5
2
+ 6.4
+ 3.5
~ 1.8
- 3.4
3
+ 1.0
+ 2.0
+ 1.7
-5.5
*
4
~ 0.9
- 3.4
- 3.5
+6.5
*
1
~ 6.4 *
~ 3.1
+ 3.5
+ 2.4
outer sides (upper left and lower right matrix corners). Table I shows that a reliable recognition minima (+AP) as well as its maxima (-A P) are grouped in a diagonal direction right to the lower left corner).
(from
the upper
I of recogmtion
prohabilrty
data for 48 experiments
are estimations Alpha-
contourfromthe
0.25
ability not only separated two diagonal branches of its increase, but also surrounded them on both
of the alpha-
degrees eccentricity, no reliable changes of recognition were observed. On the time-space matrix (Fig. 3a) two parallel branches of increased recognition probability were
Change
improvement)
between two positive successions (arrow 3). Fig. 3b shows that the decrease in recognition prob-
wave, whereas centrally localized ones - at relatively later phases. In the case of the 16 angular
TABLE
of are
crease of the recognition probability in comparison with the control level is seen on the matrix
succession: images, the contours of which are relatively far from the gaze, are reliably better recognized as compared with mean control level (25.0 earlier
of the figures
dP
Evidence of the separate existence of these two branches may be seen in Fig. 3b: a reliable de-
servers from seven and the mean data) there exists an inverse relation between eccentricity and phase
at relatively
to recognition
I.M..
underlined
revealed (1 and 2). One of them (the main diagonal) goes from 9 to 0.25 degrees in the alpha-wave phases succession 2-3-4-l (arrow l), the second from 9 to 3 degrees in succession 3-4-l (arrow 2).
the axis,
axis, see Fig. 2~).
f 0.3%)
observer
prob-
with
from gaze (horizontal
wth
with P > 0.95.
on dependence
that correspond Distnnce
0.25
on the dtstance
with seven observers, to recognition
of the figures
contours
from
gaze
m %, * marks estimations
and the EEG
with P > 0.95,
alpha-waoe
phase
* * P > 0.99, underlined
improvement)
contour from
0.75
of the figures
3 P of errors
the gaze (degrees)
2.5
3
4.5
6
9
16
phase 2
+ 1.3
+1.0
3
+ 0.8
+2.1
4
+ 0.3
1
-2.0
**
+2.9 **
**
-1.6
*
-2.7
i2.2
**
PO.1
+1.7
*
-1.2
+0.3 **
+3.1
+ 1.0
- 2.3 * *
- 0.8
+1.0
~ 1.2
-0.2
+0.1
~ 3.2 * *
+ 2.0 *
-0.5
+1.4
+ 0.2
+ 2.2 * *
+0.4
-3.2 **
- 3.6 * *
+2.1 **
**
199
TABLE
DISCUSSION
III
Change of recognition probability on dependence on the distance of Ihe the figures contours from gaze and the EEG alpha-wave phase (Mean data for 10 experiments with observer A.M., A P of errors in %, * marks estimations with P > 0.95, * * P > 0.99, underlined are estimations that correspond to recognition improvement) Alphawave
phase
Distance of the figures contour from the gaze (degrees) 0.25
0.75
2.5
4.5
2
- 6.2 * *
-5.5
+5.9 *
+ 2.6
3
-0.2
+1.6
-5.0
+0.8
*
4
+ 2.2
- 0.4
- 4.8
-4.3
1
+ 4.0
+4.1
+ 3.8
+0.5
Table II shows average data for 10 experiments with typical observer I.M. It can be seen that these results in principle coincide with data of Table I. But in one of the seven observers (A.M.), we obtained a direction opposite to the typical direction of recognition probability increase on the space-time matrix (Table III). In this case small figures at earlier alpha-wave phases and bigger figures at relatively later phases are recognized better. In other words: here, the size-phase relation is direct, while in typical cases it is inverted.
According to the original idea of Pitts and McCulloch (1947) the excitation wave, spreading over the visual cortex, first of all will increase the recognition probability for small figures (Fig. la and Fig. 4a,l). Concentric widening of the wave front in next moments will lead to an increase of recognition probability for bigger and bigger images (Fig. lb, c and Fig. 4a, 2-4). The data presented confirmed the existence of the spreading wave process, because both of two direct conclusions from Pitts’s and McCulloch’s hypothesis were proved. Indeed, all observers show existence of relation between the succession of alpha-wave phases and the succession of the figures contour eccentricity by the criterion of their recognition probability. From our point of view it is very strong, albeit indirect evidence, of the validity of their hypothesis. According to the original hypothesis, however, the scanning wave in the visual cortex should initially improve the recognition of the small figures and then of the bigger ones (Fig. 1 and 4a). In our study, only one from seven observers showed such tendency of changes (Table III) predicted on the basis of Pitts’s and McCulloch’s (1947) idea. Data presented in Fig. 3a and Tables I and II, show that the inverted space-time relation (Fig. 4b) in appropriate matrix was typical. Thus, it may be assumed that every 80-120 ms
Fig. 4. Schemes of excitability dynamics in the visual cortex according to: (a) Pitts’ and McCulloch’ hypothesis; (b) our data; and (c) the possibility of the excitability synchronous modulation. Visual cortex of one hemisphere is shown. l-4: moments corresponding to successive phases of the EEG alpha-wave (see Fig. 2~). Excitability increase is shown as an upward deflection, decrease - as a downward one.
200
(alpha-rhythm period in different subjects) two concentric circular waves (this configuration seems to us most probable) are generated in the cortical projection of the visual field. Even the place of their generation in the cortex can be indicated: it is the cortical projection of the near periphery of the visual field (9912 degrees from gaze). The first wave begins moving from the near periphery toward the center of the cortical representation of the visual field. It reaches the center during 3/4 of alpha-wave period (about 75 ms) with a mean angular speed of approx. 120 deg./s. The second wave spreads in the same direction with the same speed and with some delay but travels only in the near periphery of the field (993 deg.). In the cortical space linearized in accordance with a magnification factor, the spreading of the two waves is practically even. This can be seen in Fig. 3a where the abscissa (space) is plotted non-linearly and the law of this non-linearity takes into account the magnification factor for the human visual cortex (Cowey and Rolls, 1974). Let us discuss the correspondence between our filtered EEG and native EEG signal. It is important because, if current alpha frequency of EEG and tuning frequency of our filter do not coincide, the inevitable phase shift between both signals will result in some errors of phase estimation. But if we choose a proper (most probable or dominant alpha frequency) value as a filter tuning frequency, this distortion would act uniformly in both ‘directions’ (increasing and decreasing current phase angle). That is true for a drift of a current EEG alpha frequency around its dominant value. The fact that even in this ‘distorted’ situation we could show statistically significant differences in figure recognition presented at different phases of alpha-wave can support the described phenomenon. It must be noted, additionally, that the phase shift to some extent is not of great importance for our conclusions. In fact, not the exact phase value but their succession matters. That is why here we discuss ‘later’ or ‘earlier’ phases and can not assert their angle value purely quantitatively. Mean individual and mean group results show that different disturbances that can potentially mask the revealed phenomenon (shift in maximum of EEG power spectrum during ex-
periment, possible but rare eye movement during figure exposition, as well as phase shift between filtered and unfiltered EEG) failed to do it that proved it to be of a non-accidential nature. It is difficult to discuss now neurophysiological mechanisms of triggering and of spreading of the supposed wave process in the visual cortex. Up to now it is not the common view and there is strong evidence in favour of the cortical or, contrary, subcortical localization of alpha-rhythm pacemaker (see for review: Plotkin, 1976; Guselnikov and Iznak, 1983). The fact that there is an initial appearance of the excitatory wave in the peripheral circular zone of the cortex can tell us about the external, non-cortical source of its generation. As to the mechanism of the wave spreading over the cortex, it can be explained theoretically on the same basis, as the location of the alpha-wave generator: either by the subcortical (external) control of such activity and movement or by pure intracortical generation and spread of excitation as in continuous media (Gelfand and Tseitlin, 1960, Griffith, 1965). It must be noted that up to now the waves spreading over the cortex with a speed of some meters per second (value calculated from the known size of the human visual cortex and the time of the wave propagation estimated here) were not found, although their speed up to 33 mm/s was demonstrated in the rat by thermoencephaloscopy (Gorbach et al., 1989; Shevelev et al., 1986, 1989a,b). In principle the obtained data might be due to a non-spreading wave process. In this case (Fig. 4c) the excitability of all visual cortex elements is supposed to be modulated synchronously with the alpha-rhythm, while the illusion of the wave spreading is due to difference in delay of the afferentation to different parts of the cortical field. Simulation shows that such supposition contradicts the known temporal properties of the Xand Y-visual channels (Enroth-Cugell and Robson, 1966) and is, thus, unlikely. Thus, for an illusion of the wave spreading from peripheral to the central part of the cortical field (direction that was typically revealed in our study) it is necessary to have a slower afferentation propagation in the Y-channel, than in the X one, and that is not the case in reality.
201
Functional meaning of the periodical readout process in the visual cortex was previously postulated (Pitts and McCulloch, 1947). The authors of the original hypothesis believed that it ensured an invariance of visual recognition to the size, rotation and retinal localization of recognized figures as well as leading to the possibility of necessary volume reduction in the information channel between the 17th and other visual fields in the cortex. The last consequence is of essential importance because it ensures a very profitable spatiotemporal information presentation at the output of the visual cortex instead of a pure spatial one and consents the necessary volume of this output with the reality. It must be emphasized that the obtained data and the hypothesis that they confirm, provide an alternative to the commonly accepted interpretations of the EEG alpha-wave functions because it takes into account not only temporal, but also spatio-temporal aspects of the visual recognition and informational meaning of the EEG.
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