|First a short detour. This is the original format that Psycoloquy was produced in. Here is the same paper as the previous page in plain text, and no links! BACK|
psycoloquy.95.6.27.memory-brain.3.verleger Monday 4 September 1995
ISSN 1055-0143 (8 paragraphs, 32 references, 290 lines)
PSYCOLOQUY is sponsored by the American Psychological Association (APA)
Copyright 1995 Rolf Verleger
MEMORY-RELATED EEG POTENTIALS: SLOW NEGATIVITIES,
PRIMING POSITIVITY, RECOGNITION POSITIVITY, AND Dm
Commentary on Klimesch on Memory-Brain
Department of Neurology
ABSTRACT: Klimesch's attempt at explaining memory processes by what
is known about EEG rhythms is impressive. However he fails in his
"speculative" attempt (as he calls it) to integrate event-related
EEG potentials (ERPs) into this picture. The ERP results discussed
in this commentary are presumably not incompatible with Klimesch's
approach, but require considerable differentiation of his
1. In this commentary, I focus on positivities that resemble P3
order to help differentiate this complex of results, and on slow
negative potentials because these recent findings are so impressive.
But there are many more ERP components than P3, and in particular there
are many ERP components whose association to memory processes is more
evident than P3's. These include mismatch negativity (review in
Naatanen, 1990) which is automatically evoked by auditory stimuli
that deviate in some feature from the previous stimuli, and processing
negativity (review in Naeaetaenen, 1990) which arises whenever some
sequence of tones has to be distinguished from some other sequence.
Obviously some short-term memory processing (Naeaetaenen speaks of
"rehearsal") of the auditory stimuli is involved. N400 (Kutas &
Hillyard, 1980) is the component which is preferably evoked by words
(presented visually or auditorily), being larger the less predictable
the word is. Again, some memory process is obviously involved (see
e.g., Bentin & McCarthy, 1994).
II. P3 AND MEMORY
2. P3's main portion is not within the theta band. Rather, the main
portion of P3 lies in sub-delta and delta. For example, P3 is virtually
abolished with a high-pass setting at 1.0 Hz (Duncan-Johnson & Donchin,
1979) or of 2.0 Hz (Jodo & Kayama, 1992). The importance of the slow
portion of P3, as well as the irrelevance of the faster bands, can also
be recognized from the practice found in many laboratories of measuring
P3's peak after severe low-pass filtering. For example, Donchin's group
has often used a low-pass with -3db at 8 Hz (e.g., Fabiani & Donchin,
1995) implying a relevant attenuation of the theta band, and others
have gone even further below, without any obvious loss of information
(e.g., 3.5 Hz low-pass used by Pfefferbaum, Christensen, Ford & Kopell,
3. P3 is only loosely related to the hippocampus. As Klimesch (1995)
correctly points out, integrity of the hippocampus is not necessary for
P3 (e.g., Polich & Squire, 1993) even though there is activity within
the hippocampus concurrent with, or shortly after P3, often larger than
in other areas (Smith, Halgren, Sokolik, Baudena, Musolino,
Liegois-Chauvel & Chauvel, 1990). Yet, what is necessary for P3 is
integrity of the temporo-parietal junction (Knight, Scabini, Woods &
Clayworth, 1989; Yamaguchi & Knight, 1991; Verleger, Heide, Butt &
Koempf 1994; see also Molnar, 1994).
III. MEMORY-RELATED POSITIVITIES OVERLAPPING P3
4. At least three different positivities within the P3 time window
be distinguished in the context of memory: priming positivity,
recognition positivity, and Dm. Whether any of these has a closer
relationship to theta or to the hippocampus than P3 will be noted in
the following sections.
IV. PRIMING POSITIVITY
5. When words are repeated in a task where occasional targets (e.g.,
non-words) have to be detected, then the potentials evoked by repeated
words are positively shifted (Bentin & Peled, 1990; Rugg, Pearl,
Walker, Roberts & Holdstock, 1994). This broad positivity (between 250
ms and 700 ms) has been interpreted as an attenuation of the N400,
followed by an enhancement of P3 (Rugg et al., 1994). A relationship of
this broad positive shift to theta is not obvious. Further, there is no
obvious relationship to the hippocampus, since the effect does not
differ between lobectomized and other epileptic patients (Rugg,
Roberts, Potter, Pickles & Nagy, 1991) nor between Alzheimer patients
and controls (Friedman, Hamberger, Stern & Marder, 1992; Rugg et al.,
V. RECOGNITION POSITIVITY
6. In this paradigm, two lists of words are presented, with the
list consisting of "old" items (i.e., members of the first list) and
"new" items. ERPs are recorded during the second list. Correctly
detected old items evoke a larger positivity than other items
(Sanquist, Rohrbaugh, Syndulko & Lindsley, 1980; Karis, Fabiani &
Donchin, 1984). This positivity starts later than priming positivity
(Rugg & Nagy, 1989) and is larger the more clearly the word is
remembered (Smith, 1993). It has been interpreted as enhancement of the
very P3 due to great confidence in the decision (Rugg & Nagy, 1989)
which would agree with a general regularity in P3's behavior (Johnson,
1986). But on the other hand, the topography of this effect might
differ from P3's (Smith & Guster, 1993) and the effect is more marked
with low- than with high-frequency words when confidence in the
decision is held constant (Rugg, Cox, Doyle & Wells, 1995). So the
recognition positivity might be something else than the usual P3.
Therefore the interpretation of Smith and Halgren's (1989) finding of a
reduced recognition positivity in left-temporal-lobectomized patients
(cf. Klimesch's par. 53) is difficult. This reduction might either be a
reduction of recognition positivity or of P3. In the former case, it
would be related to memory. In the latter case, it might either be
related to memory or to the patients' generally worse performance, for
example, to their lower confidence in their decisions. Finally, whether
recognition positivity has a specific theta component is not known.
VI. DIFFERENCE RELATED TO MEMORY: Dm
7. When in the former paradigm, ERPs are recorded during presentation
of the first list, then words that will be later correctly recognized
evoke a larger positivity in the 400-800 ms range than later-
unrecognized words (e.g., Sanquist et al., 1980; Smith, 1993). An even
more marked difference (Paller, 1990) is found between later-recalled
and later-not-recalled items (e.g., Karis et al., 1984; Uhl, Franzen,
Serles, Lang, Lindinger & Deecke, 1990; Fabiani & Donchin, 1995). While
some authors interpret this positivity as enhancement of the very P3
(Karis et al., 1984, Fabiani & Donchin, 1995), many other authors are
more cautious since Paller, Kutas and Mayes (1987) reported that this
positivity (called "Dm" by these authors, i.e., difference related to
memory) is more evenly distributed across the scalp than P3, which has
a parietal maximum. Using faces as material, Sommer, Schweinberger and
Matt (1991) and Sommer, Heinz, Leuthold, Matt and Schweinberger (1995)
found an anteriorly enhanced Dm, also in contrast to P3. Dm is often a
slow long-lasting potential, so there is no obvious relationship to
theta. Its relationship to the hippocampus has not been studied so far.
Uhl et al. (1990) showed that the apparently post-stimulus Dm may be
partially due to differences in pre-stimulus levels.
VII. SLOW NEGATIVE MEMORY-RELATED SHIFTS
8. Any account of ERPs and memory would be incomplete without
mentioning the recent work by Roesler, Heil and Hennighausen (1995).
These authors recorded EEG while subjects retrieved verbal, spatial, or
color information from memory. Slow negative shifts were obtained,
extending over several seconds, with their amplitudes being larger the
more complex the information was that had to be retrieved, and with
specific topographies: left-frontal with verbal information, parietal
with spatial information, and occipital with color information. These
findings have to be integrated in any theory that relates human brain
physiology to memory.
Bentin, S. & McCarthy, G. (1994) The effects of immediate stimulus
repetition on reaction time and event-related potentials in tasks of
different complexity. Journal of Experimental Psychology: Learning,
Memory, and Cognition, 20, 130-149.
Bentin, S. & Peled, B. (1990) The contribution of task-related
to ERP repetition effects at short and long lags. Memory & Cognition,
Duncan-Johnson, C.C. & Donchin, E. (1979) The time constant
recording. Psychophysiology, 16, 53-55.
Fabiani, M. & Donchin, E. (1995) Encoding processes and memory
organization: A model of the Von Restorff effect. Journal of
Experimental Psychology: Learning, Memory, and Cognition, 21, 224-
Friedman, D., Hamberger, M., Stern, Y. & Marder, K. (1992) Event-
related potentials (ERPs) during repetition priming in Alzheimer's
patients and young and older controls. Journal of Clinical and
Experimental Neuropsychology, 14, 448-462.
Jodo, E. & Kayama, Y. (1992) Relation of a negative ERP component
response inhibition in a go/no-go task. Electroencephalography and
clinical Neurophysiology, 82, 477-482.
Johnson, R., Jr. (1986) A triarchic model of P300 amplitude.
Psychophysiology, 23, 367-384.
Karis, D., Fabiani, M. & Donchin, E. (1984) "P300" and memory:
Individual differences in the von Restorff effect. Cognitive
Psychology, 16, 177-216.
Klimesch, W. (1995). Memory Processes Described as Brain Oscillations
in the EEG-Alpha and Theta Bands. PSYCOLOQUY 95(6)
Knight, R.T., Scabini, D., Woods, D.L. & Clayworth, C.C. (1989)
Contributions of temporal-parietal junction to the human auditory P3.
Brain Research, 502, 109-116.
Kutas, M. & Hillyard, S.A. (1980) Reading senseless sentences:
potentials reflect semantic incongruity. Science, 207, 203-205.
Molnar, M. (1994) On the origin of the P3 event-related potential
component. International Journal of Psychophysiology, 17, 129-144.
Naatanen, R. (1990) The role of attention in auditory information
processing as revealed by event-related potentials and other brain
measures of cognitive function. Behavioral and Brain Sciences, 13,
Paller, K.A. (1990) Recall and stem-completion priming have different
electrophysiological correlates and are modified differentially by
directed forgetting. Journal of Experimental Psychology: Learning,
Memory, and Cognition, 16, 1021-1032.
Paller, K.A., Kutas, M. & Mayes, A.R. (1987) Neural correlates
encoding in an incidental learning paradigm. Electroencephalography and
Clinical Neurophysiology, 67, 360-371.
Pfefferbaum, A., Christensen, C., Ford, J.M. & Kopell, B.S.
Apparent response incompatibility effects on P3 latency depend on the
task. Electroencephalography and Clinical Neurophysiology, 64,
Polich, J. & Squire, L.E. (1993) P300 from amnesic patients
bilateral hippocampal lesions. Electroencephalography and Clinical
Neurophysiology, 86, 408-417.
Roesler, F., Heil, M. & Hennighausen, E. (1995) Distinct cortical
activation patterns during long-term memory retrieval of verbal,
spatial, and color information. Journal of Cognitive Neuroscience, 7,
Rugg, M.D. & Nagy, M.E. (1989) Event-related potentials and
recognition memory for words. Electroencephalography and Clinical
Neurophysiology, 72, 395-406.
Rugg, M.D., Cox, C.J.C., Doyle, M.C. & Wells, T. (1995) Event-related
potentials and the recollection of low and high frequency words.
Neuropsychologia, 33, 471-484.
Rugg, M.D., Pearl, S., Walker, P., Roberts, R.C. & Holdstock,
(1994) Word repetition effects on event-related potentials in healthy
young and old subjects, and in patients with Alzheimer-type dementia.
Neuropsychologia, 32, 381-398.
Rugg, M.D., Roberts, R.C., Potter, D.D., Pickles, C.D. & Nagy,
(1991) Event-related potentials related to recognition memory.
Effects of unilateral temporal lobectomy and temporal lobe epilepsy.
Brain, 114, 2313-2332.
Sanquist, T.F., Rohrbaugh, J.W., Syndulko, K. & Lindsley, D.B.
Electrocortical signs of levels of processing: Perceptual analysis and
recognition memory. Psychophysiology, 17, 568-576.
Smith, M.E. (1993) Neurophysiological manifestations of recollective
experience during recognition memory judgments. Journal of Cognitive
Neuroscience, 5, 1-13.
Smith, M.E. & Guster, K. (1993) Decomposition of recognition
event-related potentials yields target, repetition, and retrieval
effects. Electroencephalography and Clinical Neurophysiology, 86,
Smith, M.E. & Halgren, E. (1989) Dissociation of recognition
components following temporal lobe lesions. Journal of Experimental
Psychology: Learning, Memory, and Cognition, 15, 50-60.
Smith, M.E., Halgren, E., Sokolik, M., Baudena, P., Musolino, A.,
Liegois-Chauvel, C. & Chauvel, P. (1990) The intracranial topography of
the P3 event-related potential elicited during auditory oddball.
Electroencephalography and Clinical Neurophysiology, 76, 235-248.
Sommer, W., Heinz, A., Leuthold, H., Matt, J. & Schweinberger,
(1995) Metamemory, distinctiveness, and event-related potentials in
recognition memory for faces. Memory & Cognition, 23, 1-11.
Sommer, W., Schweinberger, S.R. & Matt, J. (1991) Human brain
potential correlates of face encoding into memory. Electro-
encephalography and Clinical Neurophysiology, 79, 457-463.
Uhl, F., Franzen, P., Serles, W., Lang, W., Lindinger, G. &
(1990) Anterior frontal cortex and the effect of proactive
interference in paired associate learning. A DC-potential study.
Journal of Cognitive Neuroscience, 2, 373-382.
Verleger, R., Heide, W., Butt, C. & Koempf, D. (1994) Reduction
in patients with temporo-parietal lesions. Cognitive Brain Research, 2,
Yamaguchi, S. & Knight, R.T. (1991) Anterior and posterior association
cortex contributions to the somatosensory P300. The Journal of
Neuroscience, 11, 2039-2054.