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     MindNet Journal - Vol. 1, No. 62c * [Part 3 of 4 parts]
     V E R I C O M M / MindNet         "Quid veritas est?"

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Editor: Mike Coyle 

Assistant Editor: Rick Lawler

Research: Darrell Bross

[Continued from part 2]


34. Some researchers have suggested that the EEG frequency within
the alpha band (of about 8-13 Hz) stems from the thalamus and
induces synchronized neuronal activity in the cortex (Andersen &
Andersson, 1968). In terms of EEG frequencies, the ideas
described so far can be summarized as follows. A search processes
in LTM starts if thalamo-cortical pathways are selectively
activated, which means that a particular subset of these pathways
shift their resting frequency within the alpha band. This shift
in frequency serves as input frequency f to the cortical storage
network where the search process spreads between different access
points. In response to the search process, different cell
assemblies start to oscillate with different frequencies f'
within the alpha, beta and gamma bands. The status of the search
process is constantly fed back by each activated cortical field
(alpha field) that is served by a thalamo-cortical feedback loop
oscillating within the range of alpha frequency. The higher
cortical frequency f' is, the stronger is the concomitant
increase in alpha frequency. The relevant information can be read
out via those feedback loops responding with the highest
frequency. Because we have assumed that alpha oscillations
reflect the information processing in thalamocortical feedback
loops, whereas gamma oscillations reflect pure cortical
processing, a specific transition or interface between alpha and
gamma oscillations must be postulated. The following two facts
support this idea. First, Steriade et al. (1990, p. 147) report
that the gamma rhythm (the 40 Hz rhythm in particular) is driven
by neurons located in that cortical layer, which receives
thalamic afferents. They conclude that thalamic input to the
cortex serves as a trigger for rhythmic activation of specific
cortical columns. Second, Pfurtscheller et al. (1994) observed a
reciprocal relationship between alpha and the 40 Hz rhythm: If
the 40 Hz rhythm synchronizes, alpha desynchronizes and vice


35. If we proceed from the idea that memory codes are retrieved
via longitudinal pathways linking thalamic nuclei with the
cortex, and that alpha is the predominant rhythm reflecting the
activity of these pathways, we arrive at the hypothesis that
alpha frequency should be related to memory performance (see
section I). We have tested this hypothesis (Klimesch, Schimke,
Ladurner & Pfurtscheller, 1990; Klimesch, Schimke &
Pfurtscheller, 1993) and found that - as compared to bad memory
performers - good performers show a significantly higher alpha
frequency. This result was found even in a resting state where
subjects relaxed with eyes closed, but was most pronounced during
actual retrieval attempts (Klimesch et al., 1990, Experiments 1
and 2). Furthermore, it could be demonstrated that attentional
demands or interindividually different responses to increasing
memory load (as an indicator of STM-span) are not responsible for
the higher alpha frequency of good memory performers (Klimesch et
al., 1993).

36. In a recently performed study, Klimesch, Schimke and
Schwaiger (1994) were able to demonstrate that alpha power
selectively responds to semantic LTM demands, whereas theta power
selectively responds to episodic STM demands. In this study, an
experimental design was used, that already proved useful in
distinguishing semantic LTM from episodic STM (Kroll & Klimesch,
1992). The experimental design consisted of two parts. Subjects
first performed a semantic congruency task in which they had to
judge whether or not the sequentially presented words of
concept-feature pairs (such as "eagle-claws" or "pea-huge") were
semantically congruent. Then, without prior warning, they were
asked to perform an episodic recognition task. This was done in
an attempt to prevent subjects from using semantic encoding
strategies and thus to increase episodic memory demands. In the
episodic task, the same concept-feature pairs were used as
targets and were presented together with distractor pairs
(generated by repairing known concept-feature pairs). Now
subjects had to judge whether or not a particular concept-feature
pair was already presented during the semantic task. The results
of Kroll and Klimesch (1992) indicated that semantic features
speeded up semantic, but slowed down episodic decision times (for
an extensive review on this topic see also Klimesch, 1994). With
respect to the purpose of the present study, this result
indicates that semantic and episodic memory processes can
effectively be differentiated by using the design underlying
Experiment 4 in Kroll and Klimesch (1992). According to the
proposed hypothesis, it is expected that only in the semantic
task should the most pronounced desynchronization (decrease in
alpha band power) be observed in the alpha band. Because pairs of
items are presented and because a subject can only perform the
episodic and semantic task after the second item of a pair (i.e.,
the feature) is presented, a decrease in alpha band power as a
response to increasing semantic task demands is expected only for
the time period following the presentation of the feature. It is
important to keep in mind that alpha power is well known to
decrease (desynchronize) with increasing task difficulty and
attentional demands. From the results found in Kroll and Klimesch
(1992) we know that the episodic task is much more difficult than
the semantic task. Thus, if task difficulty would be the only
factor which is reflected by a decrease in alpha power, we would
expect the most pronounced response to be observed during the
presentation of the feature in the episodic task. This, however,
was not the case. In support of our hypothesis it was found that
alpha desynchronizes during the presentation of the feature in
the semantic task. In the episodic task, on the other hand, theta
power increased (synchronized) during the processing of the


37. Since Scoville and Milner (1957) reported a severe
anterograde amnesia for patient H.M. who had undergone a
bilateral temporal lobectomy, including the hippocampal
formation, and since Green and Arduini (1954) have found a
dominant rhythmic electrical activity within the theta band in
the hippocampus of rats, it has become obvious that theta
activity of the hippocampus might be related to the encoding
and/or retrieval of new information. Positive evidence came from
studies which have documented that there is a preference for
long-term potentiation (LTP) to occur in the hippocampal
formation, and that theta activity induces or at least enhances
LTP (e.g., Larson, Wong & Lynch, 1986; and Greenstein, Pavlides &
Winson, 1988). The fact that LTP is considered the most important
electrophysiological correlate for encoding new information,
underlines the potential importance of hippocampal theta for
memory processes in the WMS.

38. In trying to explain the possible functional significance of
the theta rhythm in the human EEG, we assume that synchronized
bursts of a small set of hippocampal pyramidal cells induce theta
activity in selected but distributed cortical regions which are
relevant for performing a particular task. Empirical findings
support this view and indicate that theta band power increases
with increasing (episodic) task demands (Klimesch, Schimke &
Schwaiger, 1994). Research in animals also indicates that during
behavioral activity, theta power increases (e.g., the review in
Lopes da Silva, 1992).

39. One of the first questions that may arise when considering
the proposed hypothesis is, why - in contrast to animals - theta
is not a dominant rhythm in the human EEG. In an attempt to
answer this question we first proceed from a theoretical
consideration that is similar to the mechanisms that were
proposed for accessing and retrieving LTM codes. It is assumed
that hippocampo-cortical feedback loops induce synchronized
rhythmic theta activity onto different regions of the neocortex
where (e.g., by means of LTP) new information is encoded or
freshly encoded information is retrieved. Given the basic
assumption that new information always will be "added" or
"attached" to related but already encoded information, only a
small subset of the hippocampo-cortical feedback loops which are
related to relevant cortical areas will be needed and thus will
actually show synchronized theta activity. Because the human
cortex is much larger than those in lower mammals and, as a
consequence, holds much more LTM-information, the encoding of new
information is a much more distributed process than in animals.
Thus, if the percentage of synchronized hippocampo-cortical
feedback loops is related to the size of the cortex (and to the
hippocampus too, which is relatively much smaller in humans),
this percentage will be orders of magnitudes smaller for humans
as compared to animals.

40. Evidence for the view that only a small percentage of
hippocampo-cortical feedback loops is synchronized comes from a
re-examination of the pacemaker role of the septum in the
production of the hippocampal theta rhythm (Petsche, Stumpf &
Gogolak, 1962; Stewart & Fox, 1990). In addition to cholinergic
projections, a large fraction of the septo-hippocampal
projections terminate on inhibitory (GABA-ergic) hippocampal
interneurons (Freund & Antal, 1988; see also the reviews in Lopes
da Silva, 1992; and Stewart & Fox, 1990). Based on these and
related findings, Stewart and Fox (1990) assume that the septal
input might organize the hippocampal theta activity via rhythmic
inhibition of hippocampal interneurons. This view is in agreement
with the fact that hippocampal interneurons are more likely to
behave as theta cells (Fox & Ranck, 1981) than burst firing
pyramidal neurons. In agreement with this fact, a simulation
model (Traub, Miles & Wong, 1989) reveals that in contrast to
interneurons, only a small percentage of the pyramidal cells
display synchrony.

41. With respect to the question, whether theta activity can be
observed in the EEG, these findings which were obtained from
microelectrodes in the hippocampus are of outstanding importance.
Biophysically, theta frequency in the hippocampus, deep inside
the brain, would be difficult to detect from scalp electrodes.
The crucial condition to detect theta as a dominant rhythm in the
EEG would be that most of the burst firing hippocampal pyramidal
cells that project to other parts of the cortex would fire in
synchrony. However, as we have already noted, according to Leung
(1980), Traub et al. (1989) and Lopes da Silva (1992), this is
not the case. And indeed, as judged by visual inspection but in
contrast to spectral analysis, theta activity usually is absent
in the EEG of normal, wake adults.

42. The fact that only a small percentage of the pyramidal
neurons displays synchrony, agrees with the idea that
hippocampo-cortical feedback loops induce synchronous theta
activity into selected cortical areas where new information is
encoded or fresh information is retrieved. This is type 2 or
selective synchronization that means activation. Given the fact
that theta frequency induces or at least enhances LTP (see also
Lopes da Silva, 1992), it seems tempting to assume that theta
activity, induced into selected cortical areas, reflects a
process to encode or retrieve new information by keeping or
putting selected cortical areas into a state of resonance. This
assumption comes very close to a theory of resonant phase-locked
hippocampo-cortical loops, proposed by Miller (1991).


43. A possible objection against our central hypothesis that
brain oscillations are the basic phenomenon of cortical
information processing may come from researchers using event
related potentials (ERPs) to study cognitive and memory processes
in particular. They may argue that late components of ERPs
reflect completely different types of cortical processes such as,
for example, time locked threshold changes that regulate the
degree of excitability in neuronal networks (e.g., Birbaumer &
Elbert, 1988; Elbert, 1992). Given the fact that almost all of
the memory studies in cognitive electrophysiology focus on late
components of ERPs, this objection could seriously threaten the
general validity of our hypothesis.

44. However, it may also be argued that late components of ERPs
are the result of synchronous oscillations that are transiently
phase locked in response to a relevant event or stimulus. Summed
up over several trials, a waveform (the ERP) would be generated
that shows the typical succession of positive and negative
"peaks" (or ERP components). If we proceed from this idea, it
becomes evident that only (or at least primarily) those types of
oscillations would be capable of generating late ERP components
that indeed respond with coupled type 2 synchronization to an
increase in respective task demands. Note that alpha and beta
tend to desynchronize with increasing task demands.
Hypothetically, there are only two possible candidates (see
section II.3; paragraph 15): theta and gamma frequency. Because
gamma frequency is much too high and its amplitudes much too
small to generate a typical ERP, theta frequency remains the most
plausible candidate.

45. This proposal, of course, does not mean that theta is the
only generator for ERPs. In addition, there may be other
processes such as very slow oscillations in the delta band (below
4 Hz) and/or threshold changes in large parts of the cortical
network that also may have a strong influence on the waveform of
ERPs. Weak influences may even be due to type 2 synchronizations
within the alpha band.

46. The most obvious ERP component that might reflect phase
locked evoked theta activity is the P300 for the following two
reasons: First, because of the (typical) latency and form of the
P300, this ERP component shows the most significant power in the
theta band as frequency decompositions indicate (Basar &
Stampfer, 1985). Second, the (typical) functional meaning of the
P300, particularly the process of "updating" (Donchin & Coles,
1988), is well related to central functions of the WMS.

47. Now, let us consider the most speculative part of our
proposal which links phase locked theta activity to the P300
component of event related potentials (ERPs). Keeping in mind
that a single cycle of the theta rhythm consists of an inhibitory
and a disinhibited or excitatory phase and that only in the
latter, bursts of action potentials are sent to selected cortical
areas, the question arises: With which phase of the cycle does
task related (episodic) processing start? Does it start with the
inhibitory or the excitatory phase? In referring to the argument
that theta is induced in selected parts of the cortical network,
it seems plausible to assume that episodic processing starts with
the inhibitory phase in order to maximize the impact of the
distributed activation of the relevant parts of the network by
reducing irrelevant background activity through the inhibitory
phase. As a result of this assumption, and because only a small
percentage of the burst firing pyramidal cells are synchronized
through the excitatory phase, the outcome should be a positive
going deflection in the EEG, time locked to the presentation of
an adequate stimulus.

48. If this is true, it should be possible to record evoked theta
activity from the scalp in response to an appropriate stimulus or
event. Based on theoretical considerations and experimental
evidence (e.g., Leung, 1980), Lopes da Silva (1992, p. 93)
concludes that appropriate stimuli or events induce evoked
responses that depend on the phase of theta frequency. Therefore,
evoked theta activity may be viewed as synchronized phase locked
and thus amplified theta frequency which occurs in response to an
appropriate event. The issue of interest is whether evoked or
event-related theta activity can be detected as a response to
increased episodic memory demands.

49. We have emphasized that one of the most important functions
of the WMS that we have related to hippocampal information
processing is the encoding of contextual or episodic information.
Thus, if the P300 really stems from phase-locked hippocampal
theta activity, the (typical) functional meaning of the P300
should be related to the encoding of contextual and the encoding
of new information.

50. There is some evidence for this view. Donchin's updating
hypothesis (e.g., Donchin & Coles, 1988) is one of the best
examples. It is well established that the P300 amplitude is
related to the degree of contextual encoding (e.g., Donchin &
Coles, 1988), expectancy (or subjective probability), and the
amount of effort which is also reflected by the amount of
information transmitted to a subject (see e.g., Johnson's
triarchic model in Johnson, 1986; and the summary in Verleger,
1988, p. 351). It is important to note that Verleger (1988), who
is challenging Donchin's updating hypothesis, is not challenging
the significance of the P300 with respect to contextual encoding.
His argument basically is that the P300 does not reflect the
"updating" but instead the "closure" of expectancies.

[Continued to part 4]
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