Rolf Verleger (1995) Memory-related EEG Potentials: Slow Negativities,. Psycoloquy: 6(27) Memory Brain (3)

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PSYCOLOQUY (ISSN 1055-0143) is sponsored by the American Psychological Association (APA).
Psycoloquy 6(27): Memory-related EEG Potentials: Slow Negativities,

Commentary on Klimesch on Memory-Brain

Rolf Verleger
Department of Neurology
Medical University
D-23538 Luebeck



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 approach.


Alpha, EEG, Hippocampus, Memory, Oscillation, Thalamus, Theta.


1. In this commentary, I focus on positivities that resemble P3 in 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).


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, 1986).

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).


4. At least three different positivities within the P3 time window may 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.


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., 1994).


6. In this paradigm, two lists of words are presented, with the second 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.


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.


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 factors to ERP repetition effects at short and long lags. Memory & Cognition, 18, 359-366.

Duncan-Johnson, C.C. & Donchin, E. (1979) The time constant in P300 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- 240.

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 to 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) memory.brain.1.klimesch.

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: Brain 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, 201-288.

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 of encoding in an incidental learning paradigm. Electroencephalography and Clinical Neurophysiology, 67, 360-371.

Pfefferbaum, A., Christensen, C., Ford, J.M. & Kopell, B.S. (1986) Apparent response incompatibility effects on P3 latency depend on the task. Electroencephalography and Clinical Neurophysiology, 64, 424-437.

Polich, J. & Squire, L.E. (1993) P300 from amnesic patients with 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, 51-65.

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, J.S. (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, M.E. (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. (1980) 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 memory event-related potentials yields target, repetition, and retrieval effects. Electroencephalography and Clinical Neurophysiology, 86, 335-343.

Smith, M.E. & Halgren, E. (1989) Dissociation of recognition memory 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, S.R. (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. & Deecke, L. (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 of P3b in patients with temporo-parietal lesions. Cognitive Brain Research, 2, 103-116.

Yamaguchi, S. & Knight, R.T. (1991) Anterior and posterior association cortex contributions to the somatosensory P300. The Journal of Neuroscience, 11, 2039-2054.

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