Neurology -- Correspondence for Paradiso et al., 61 (11) 1538-1545

Correspondence published:

Reply to Priori et al: Robert Chen, Guillermo Paradiso (13 January 2004)

Movement-related potentials and movement-related spectral changes in the human subthalamic nucleus: Alberto Priori, Guglielmo Foffani (13 January 2004)

Reply to Priori et al 13 January 2004

Robert Chen,
Toronto Western Hospital, University of Toronto
5W445, 399 Bathurst St., Toronto, Ontario, Canada M5T 1S8,
Guillermo Paradiso
Send Correspondence to journal:
Re: Reply to Priori et al

robert.chen{at}uhn.on.ca Robert Chen, et al.

We thank Priori et al for their interest in our paper. [1] We were not aware of their preliminary report in three patients showing movement-related synchronization in the beta range (20 – 30 Hz) before movement onset in the on-medication state. [4] These findings differ from those reported by Cassidy et al [3] since those authors found changes in the 70 Hz range rather than the 20 Hz range in the on-medication state. As we state [1], we agree with Priori et al that changes in high frequency synchronized firing can contribute to the movement-related potentials (MRP) we recorded in the subthalamic nucleus (STN). However, the premovement changes in the beta rhythm [3, 4] occurred considerably later than the onset of MRP [1], suggesting that they do not represent the same phenomenon. This is consistent with scalp EEG studies showing that slow potentials and spectral changes represent different aspects of cortical electrical activity. [6,7]
Priori et al also point out that MRP are closely related to low frequency (less than 5 Hz) spectral changes and these changes in the STN were reported in a previous study. [3] We reviewed the paper by Cassidy et al. [3] Changes in 20 Hz and 70 Hz activities preceding self-paced movement are presented, and Fig. 6 shows spectral changes in the low frequency band after a warning signal in an externally triggered movement task and with passive movement in one patient. This likely represents reaction to the warning signal. However, we were unable to find documentation of spectral changes in the low frequency (less than 5 Hz) band preceding self-paced movement in the STN, which would represent movement preparation.
Priori et al confirm that it is not possible to perform spectral analysis with only zero frequency. Spectral analysis involve induced activity are likely related to oscillations of neuronal network whereas averaging techniques (e.g. MRP analysis) involve evoked, phase- locked activity and therefore likely measures different neural responses. [8] We also agree that MRP and low frequency spectral changes are likely related. How they are related will need further examination but they are clearly not identical on theoretical grounds.
References
6. Stancak A, Jr., Feige B, Lucking CH, Kristeva-Feige R. Oscillatory cortical activity and movement-related potentials in proximal and distal movements. Clin Neurophysiol 2000; 111:636-650.
7. Filipovic SR, Jahanshahi M, Rothwell JC. Uncoupling of contingent negative variation and alpha band event-related desynchronization in a go/no-go task. Clin Neurophysiol 2001; 112:1307-1315.
8. Pfurtscheller G, Lopes da Silva FH. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 1999; 110:1842-1857.

Movement-related potentials and movement-related spectral changes in the human subthalamic nucleus 13 January 2004

Alberto Priori,
Department of Neurological Sciences, University of Milan, IRCCS Ospedale Maggiore di Milano
Padiglione Ponti, Via F. Sforza 35, Milano, 20122 Italy,
Guglielmo Foffani
Send Correspondence to journal:
Re: Movement-related potentials and movement-related spectral changes in the human subthalamic nucleus

alberto.priori{at}unimi.it Alberto Priori, et al.

We read with interest the paper by Paradiso et al. [1] The authors report the movement-related potentials recorded through electrodes for deep brain stimulation implanted in the subthalamic nucleus (STN) of patients with Parkinson’s disease “in the on state”. We agree with the notion of STN involvement in movement preparation, but we believe that the relationship between movement-related potentials (i.e. averaging) and previous findings obtained by frequency analysis (i.e. movement-related spectral changes) needs consideration.
First, frequency analysis shows a movement-related desynchronization in the beta range (20-30Hz) starting before movement onset in the human STN not only off-medication [2,3], but also on- medication. [4] Movement-related beta desynchronization, therefore, contributes to the “involvement of the human subthalamic nucleus in movement preparation” in the on state.
Second, the authors [1] state that their findings “may not be comparable to frequency analysis” because the two approaches differ “fundamentally” and they do not discuss previous results concerning frequencies <5Hz. [3] At low frequencies, a direct relationship between movement-related potentials and movement-related spectral changes exists, as the movement-related potentials and the movement-related spectral changes at zero-frequency are theoretically equivalent. In fact, the movement-related potential detected by averaging techniques represents a phase-locked modulation of the statistical mean of the signal. Conversely, the mean corresponds to the zero-frequency component of the spectrum. In movement-related frequency analysis, one has to consider not only the zero-frequency component but also a broader band of low frequencies (e.g. <5Hz) because, by the Heisenberg inequality, time and frequency resolutions cannot be both arbitrarily small.[5] From a theoretical point of view, movement-related potentials [1] are closely comparable to movement-related low-frequency (<5Hz) spectral changes [3] observed in the human subthalamic nucleus during movement preparation.
References
1. Paradiso G, Saint-Cyr JA, Lozano AM, et al. Involvement of the human subthalamic nucleus in movement preparation. Neurology 2003; 61:1538-1545.
2. Foffani G, Priori A, Rohr M, et al. Event-related desynchronization (ERD) in the human subthalamus and internal globus pallidus. J Physiol 2002; 539.P:39P.
3. Cassidy M, Mazzone P, Oliviero A, et al. Movement-related changes in synchronization in the human basal ganglia. Brain 2002; 125:1235-1246.
4. Priori A, Foffani G, Pesenti A, et al. Movement-related modulation of neural activity in human basal ganglia and its L-DOPA dependency: recordings from deep brain stimulation electrodes in patients with Parkinson's disease. Neurol Sci 2002; 23(S2): S101-S102.
5. Foffani G, Priori A, Egidi M, et al. 300-Hz subthalamic oscillations in Parkinson's disease. Brain 2003; 126:2153-2163. Guglielmo Foffani and Alberto Priori
For the Policlinico-San Paolo-Politecnico Deep Brain Stimulation Study Group, Milan, Italy.
(Department of Neurological Sciences, University of Milan, IRCCS Ospedale Maggiore di Milano, 20122 Milano, Italy: G. Ardolino, S. Barbieri, M. Egidi, M. Locatelli, A. Pesenti, A. Priori, P. Rampini, R.M. Villani; Department of Clinical Neurology, Ospedale San Paolo, 20142 Milano, Italy: E. Caputo, F. Tamma; Department of Biomedical Engineering, Politecnico di Milano, 20133 Milano, Italy: G. Baselli, A.M. Bianchi, S. Cerutti, G. Foffani, B. Meda, M. Pellegrini)