Clinical Neurophysiology 126 (2015) 1643–1644
Contents lists available at ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Editorial
Somatosensory high frequency oscillations: A useful tool to analyze dynamic changes in somatosensory pathways? See Article, pages 1769–1779
In their article in this issue of Clinical Neurophysiology, Götz et al. demonstrate that during a simple auditory oddball task, eliciting a standard P300 event-related response, High-Frequency oscillations (HFOs) evoked by median nerve stimulation are significantly reduced (Götz et al., 2015). Moreover, the authors built a model consisting of one thalamic dipole and two cortical dipoles, located in the S1 area. In this model, the cortical dipoles show a radial and a tangential orientation respectively. Cortical dipoles are connected in a 3-node network model, which allowed them to describe their reciprocal influences. The modification in the connections between these dipoles allows the thalamo-cortical feedback to be quantified. Indeed, their findings strongly suggest that the HFO reduction is due to a cortico-thalamic feedback from both cortical Brodman areas 1 and 3b to the thalamus. In the last three decades the study of HFOs following peripheral nerve stimulation has gained increasing interest. While pioneer papers focused on the anatomical basis of these responses (Hashimoto et al., 1996; Gobbelé et al., 1999), in the following years more and more attention was paid to their functional meaning. Several researchers demonstrated that, differently from standard Somatosensory Evoked Potentials (SEPs), HFOs are strictly related to arousal-related structures, since they are dramatically reduced during sleep (Yamada et al., 1988; Hashimoto et al., 1996; Halboni et al., 2000), are increased by eye opening (Gobbelé et al., 2000; Restuccia et al., 2004), and are increased by cholinergic drug administration (Restuccia et al., 2003). In this view, HFO generators could represent a subsystem by which somatosensory input processing is modulated, according to the vigilance status. Further studies either on healthy humans or in pathologic conditions lend substance to this hypothesis. Until now, HFO behavior has been analysed in several diseases, such as migraine (Sakuma et al., 2004; Coppola et al., 2005; Lai et al., 2011; Restuccia et al., 2012), epilepsy (Restuccia et al., 2007a), amyotrophic lateral sclerosis (ALS; Hamada et al., 2007), schizophrenia (Norra et al., 2004), cervical dystonia (Inoue et al., 2004), Parkinson’s disease (Inoue et al., 2001), cortical myoclonus (Alegre et al., 2006), writer’s cramp (Cimatti et al., 2007), and multiple sclerosis (Gobbelé et al., 2003). Interestingly, in most of these studies, HFO abnormalities seem to be related to dynamic changes of the central nervous system (CNS) rather than to stable anatomical lesions of the somatosensory pathways. Studies on migraine
patients disclosed somewhat conflicting results, since early HFOs were found reduced (Sakuma et al., 2004; Coppola et al., 2005), or increased (Lai et al., 2011), or of variable amplitude, in turn depending on the stage of disease (Restuccia et al., 2012). However, despite the discrepancies, these papers converge in suggesting that HFOs reflect the action of a mechanism devoted to modulating the somatosensory thalamic drive, in order to modify cortical responsivity. Analogously, early HFOs are increased in seizure-free patients suffering from Idiopathic Generalized Epilepsy (Restuccia et al., 2007a). Also this finding has been interpreted as a compensatory modulation of the somatosensory thalamo-cortical drive, able to reduce cortical excitability. However, a strict relationship between HFOs and cortical excitability has been demonstrated by studies showing the influence of repetitive transcranial magnetic stimulation on these responses (Restuccia et al., 2007b; Katayama et al., 2010). A mechanism oriented to compensate motor deficit has been also suggested to explain HFO modifications in ALS patients, since these modifications are significantly related to motor deficit as well as to the stage of disease (Hamada et al., 2007). The role played by HFOs’ generators in subserving dynamic changes in the CNS has been also disclosed in many studies on healthy subjects. In general, arousal-related structures are known to modulate simple physiologic mechanisms, such as habituation or sensitization, which are defined as the reduction of the response after repetition of the stimulus or the increase of the response when another stimulus is applied in other parts of the body, respectively (Groves and Thompson, 1970). In turn, habituation and sensitization are commonly considered as the physiological basis of learning and memory (Thompson and Spencer, 1966). Probably due to their strict relationship with arousal-promoting structures, HFOs do not undergo habituation to repeated stimulation (Restuccia et al., 2011); moreover, unlike standard tibial nerve SEPs, HFOs following lower limb stimulation do not show an amplitude reduction during stance (Restuccia et al., 2008). These findings suggest that HFOs participate in a more complex mechanism, by which arousal related structures do not exert an indiscriminate activation of the CNS, but contribute to a contextual selection of relevant somatosensory inputs. In this view, the article of Götz et al. represents a further step in our understanding of such a mechanism, by suggesting that this selection occurs in the thalamus and is driven by cortifugal efferences.
http://dx.doi.org/10.1016/j.clinph.2015.01.004 1388-2457/Ó 2015 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1644
Editorial / Clinical Neurophysiology 126 (2015) 1643–1644
Another important point raised by the article of Götz et al. is the need to improve HFO analysis. Two reasons account for the difficulty in analyzing somatosensory HFOs. The first reason is related to the physiologically low signal-to-noise ratio. Classically, signalto-noise ratio is raised by greater averaging of EEG responses, in contrast with the above-mentioned main characteristic of the HFOs, that is their sensitivity to rapid dynamic changes of CNS functions. To enhance the signal-to-noise ratio of HFOs, eventually enabling single-trial analysis, recently a new method has been suggested (Waterstraat et al., 2015), the use of which seems highly promising, although it should be still validated in large population studies. The second reason is related to the difficulty in establishing the time course of HFO generators as well as their reciprocal interactions, since the visual analysis of traces hardly allows onset and the ending of any single burst to be recognized, because they are often merged in the noise or in the activity of other bursts. Although highly sophisticated and not easy-to-perform in many neurophysiological laboratories, the method introduced by Götz et al. offers the possibility to analyze both time course and reciprocal interactions of subcortical and cortical HFO generators. In conclusion, this study confirms that dynamic changes in somatosensory pathways, aimed at modifying the cortical responsivity as well as optimizing input processing, can be reliably assessed by HFOs’ studies. Moreover, this paper introduces new methods of analysis, which could, in the next future, disclose interesting and unexpected insights on the somatosensory system functions. Conflict of interest None of the authors have potential conflicts of interest to be disclosed. References Alegre M, Urriza J, Valencia M, Muruzábal J, Iriarte J, Artieda J. High-frequency oscillations in the somatosensory evoked potentials of patients with cortical myoclonus: pathophysiologic implications. J Clin Neurophysiol 2006;23:265–72. Cimatti Z, Schwartz DP, Bourdain F, Meunier S, Bleton JP, Vidailhet M, et al. Timefrequency analysis reveals decreased high-frequency oscillations in writer’s cramp. Brain 2007;130:198–205. Coppola G, Vandenheede M, Di Clemente L, Ambrosini A, Fumal A, De Pasqua V, et al. Somatosensory evoked high-frequency oscillations reflecting thalamocortical activity are decreased in migraine patients between attacks. Brain 2005;128:98–103. Gobbelé R, Buchner H, Scherg M, Curio G. Stability of high-frequency (600 Hz) components in human somatosensory evoked potentials under variation of stimulus rate. evidence for a thalamic origin. Clin Neurophysiol 1999;110:1659–63. Gobbelé R, Waberski TD, Kuelkens S, Sturm W, Curio G, Buchner H. Thalamic and cortical high-frequency (600 Hz) somatosensory-evoked potentials (SEP) components are modulated by slight arousal changes in awake subjects. Exp Brain Res 2000;133:506–13. Gobbelé R, Waberski TD, Dieckhöfer A, Kawohl W, Klostermann F, Curio G, et al. Patterns of disturbed impulse propagation in multiple sclerosis identified by low and high frequency somatosensory evoked potential components. J Clin Neurophysiol 2003;20:283–90. Götz T, Milde T, Curio G, Debener S, Lehmann T, Leistritz L, et al. Primary somatosensory contextual modulation is encoded by oscillation frequency change. Clin Neurophysiol 2015;126:1769–79.
Groves PM, Thompson RF. Habituation: a dual-process theory. Psychol Rev 1970;77:419–50. Halboni P, Kaminski R, Gobbelé R, Züchner S, Waberski TD, Herrmann CS, et al. Sleep stage dependant changes of the high-frequency part of the somatosensory evoked potentials at the thalamus and cortex. Clin Neurophysiol 2000;111:2277–84. Hamada M, Hanajima R, Terao Y, Sato F, Okano T, Yuasa K, et al. Median nerve somatosensory evoked potentials and their high-frequency oscillations in amyotrophic lateral sclerosis. Clin Neurophysiol 2007;118:877–86. Hashimoto I, Mashiko T, Imada T. Somatic evoked high-frequency magnetic oscillations reflect activity of inhibitory interneurons in the human somatosensory cortex. Electroencephalogr Clin Neurophysiol 1996;100:189–203. Inoue K, Hashimoto I, Nakamura S. High-frequency oscillations in human posterior tibial somatosensory evoked potentials are enhanced in patients with Parkinson’s disease and multiple system atrophy. Neurosci Lett 2001;297:89–92. Inoue K, Hashimoto I, Shirai T, Kawakami H, Miyachi T, Mimori Y, et al. Disinhibition of the somatosensory cortex in cervical dystonia. Decreased amplitudes of highfrequency oscillations. Clin Neurophysiol 2004;115:1624–30. Katayama T, Suppa A, Rothwell JC. Somatosensory evoked potentials and high frequency oscillations are differently modulated by theta burst stimulation over primary somatosensory cortex in humans. Clin Neurophysiol 2010;121:2097–103. Lai KL, Liao KK, Fuh JL, Wang SJ. Subcortical hyperexcitability in migraineurs: a high-frequency oscillation study. Can J Neurol Sci 2011;38:309–16. Norra C, Waberski TD, Kawohl W, Kunert HJ, Hock D, Gobbelé R, et al. Highfrequency somatosensory thalamocortical oscillations and psychopathology in schizophrenia. Neuropsychobiology 2004;49:71–80. Restuccia D, Della Marca G, Valeriani M, Rubino M, Paciello N, Vollono C, et al. Influence of cholinergic circuitries in generation of high-frequency somatosensory evoked potentials. Clin Neurophysiol 2003;114:1538–48. Restuccia D, Della Marca G, Valeriani M, Rubino M, Scarano E, Tonali P. Brain-stem components of high-frequency somatosensory evoked potentials are modulated by arousal changes: nasopharyngeal recordings in healthy humans. Clin Neurophysiol 2004;115:1392–8. Restuccia D, Valeriani M, Della Marca G. Giant subcortical high-frequency SEPs in idiopathic generalized epilepsy: a protective mechanism against seizures? Clin Neurophysiol 2007a;118:60–8. Restuccia D, Ulivelli M, De Capua A, Bartalini S, Rossi S. Modulation of highfrequency (600 Hz) somatosensory-evoked potentials after rTMS of the primary sensory cortex. Eur J Neurosci 2007b;26:2349–58. Restuccia D, Micoli B, Cazzagon M, Fantinel R, Piero ID, Della Marca G. Dissociated effects of quiet stance on standard and high-frequency (600 Hz) lower limb somatosensory evoked potentials. Clin Neurophysiol 2008;119:1408–18. Restuccia D, Del Piero I, Martucci L, Zanini S. High-frequency oscillations after median-nerve stimulation do not undergo habituation: a new insight on their functional meaning? Clin Neurophysiol 2011;122:148–52. Restuccia D, Vollono C, Del Piero I, Martucci L, Zanini S. Somatosensory high frequency oscillations reflect clinical fluctuations in migraine. Clin Neurophysiol 2012;123:2050–6. Sakuma K, Takeshima T, Ishizaki K, Nakashima K. Somatosensory evoked highfrequency oscillations in migraine patients. Clin Neurophysiol 2004;115:1857–62. Thompson RF, Spencer WA. Habituation: a model phenomenon for the study of neuronal substrates of behaviour. Psychol Rev 1966;73:16–43. Waterstraat G, Burghoff M, Fedele T, Nikulin V, Scheer HJ, Curio G. Non-invasive single-trial EEG detection of evoked human neocortical population spikes. NeuroImage 2015;15(105):13–20. Yamada T, Kameyama S, Fuchigami Y, Nakazumi Y, Dickins QS, Kimura J. Changes of short latency somatosensory evoked potential in sleep. Electroencephalogr Clin Neurophysiol 1988;70:126–36.
⇑
Domenico Restuccia Giacomo Della Marca Department of Neurosciences, Catholic University, Rome, Italy ⇑ Corresponding author at: Department of Neurosciences, Catholic University, Policlinico A. Gemelli, L.go A. Gemelli 8, 00168 Rome, Italy. E-mail address: [email protected] (D. Restuccia) Available online 23 January 2015
Contents lists available at ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Editorial
Somatosensory high frequency oscillations: A useful tool to analyze dynamic changes in somatosensory pathways? See Article, pages 1769–1779
In their article in this issue of Clinical Neurophysiology, Götz et al. demonstrate that during a simple auditory oddball task, eliciting a standard P300 event-related response, High-Frequency oscillations (HFOs) evoked by median nerve stimulation are significantly reduced (Götz et al., 2015). Moreover, the authors built a model consisting of one thalamic dipole and two cortical dipoles, located in the S1 area. In this model, the cortical dipoles show a radial and a tangential orientation respectively. Cortical dipoles are connected in a 3-node network model, which allowed them to describe their reciprocal influences. The modification in the connections between these dipoles allows the thalamo-cortical feedback to be quantified. Indeed, their findings strongly suggest that the HFO reduction is due to a cortico-thalamic feedback from both cortical Brodman areas 1 and 3b to the thalamus. In the last three decades the study of HFOs following peripheral nerve stimulation has gained increasing interest. While pioneer papers focused on the anatomical basis of these responses (Hashimoto et al., 1996; Gobbelé et al., 1999), in the following years more and more attention was paid to their functional meaning. Several researchers demonstrated that, differently from standard Somatosensory Evoked Potentials (SEPs), HFOs are strictly related to arousal-related structures, since they are dramatically reduced during sleep (Yamada et al., 1988; Hashimoto et al., 1996; Halboni et al., 2000), are increased by eye opening (Gobbelé et al., 2000; Restuccia et al., 2004), and are increased by cholinergic drug administration (Restuccia et al., 2003). In this view, HFO generators could represent a subsystem by which somatosensory input processing is modulated, according to the vigilance status. Further studies either on healthy humans or in pathologic conditions lend substance to this hypothesis. Until now, HFO behavior has been analysed in several diseases, such as migraine (Sakuma et al., 2004; Coppola et al., 2005; Lai et al., 2011; Restuccia et al., 2012), epilepsy (Restuccia et al., 2007a), amyotrophic lateral sclerosis (ALS; Hamada et al., 2007), schizophrenia (Norra et al., 2004), cervical dystonia (Inoue et al., 2004), Parkinson’s disease (Inoue et al., 2001), cortical myoclonus (Alegre et al., 2006), writer’s cramp (Cimatti et al., 2007), and multiple sclerosis (Gobbelé et al., 2003). Interestingly, in most of these studies, HFO abnormalities seem to be related to dynamic changes of the central nervous system (CNS) rather than to stable anatomical lesions of the somatosensory pathways. Studies on migraine
patients disclosed somewhat conflicting results, since early HFOs were found reduced (Sakuma et al., 2004; Coppola et al., 2005), or increased (Lai et al., 2011), or of variable amplitude, in turn depending on the stage of disease (Restuccia et al., 2012). However, despite the discrepancies, these papers converge in suggesting that HFOs reflect the action of a mechanism devoted to modulating the somatosensory thalamic drive, in order to modify cortical responsivity. Analogously, early HFOs are increased in seizure-free patients suffering from Idiopathic Generalized Epilepsy (Restuccia et al., 2007a). Also this finding has been interpreted as a compensatory modulation of the somatosensory thalamo-cortical drive, able to reduce cortical excitability. However, a strict relationship between HFOs and cortical excitability has been demonstrated by studies showing the influence of repetitive transcranial magnetic stimulation on these responses (Restuccia et al., 2007b; Katayama et al., 2010). A mechanism oriented to compensate motor deficit has been also suggested to explain HFO modifications in ALS patients, since these modifications are significantly related to motor deficit as well as to the stage of disease (Hamada et al., 2007). The role played by HFOs’ generators in subserving dynamic changes in the CNS has been also disclosed in many studies on healthy subjects. In general, arousal-related structures are known to modulate simple physiologic mechanisms, such as habituation or sensitization, which are defined as the reduction of the response after repetition of the stimulus or the increase of the response when another stimulus is applied in other parts of the body, respectively (Groves and Thompson, 1970). In turn, habituation and sensitization are commonly considered as the physiological basis of learning and memory (Thompson and Spencer, 1966). Probably due to their strict relationship with arousal-promoting structures, HFOs do not undergo habituation to repeated stimulation (Restuccia et al., 2011); moreover, unlike standard tibial nerve SEPs, HFOs following lower limb stimulation do not show an amplitude reduction during stance (Restuccia et al., 2008). These findings suggest that HFOs participate in a more complex mechanism, by which arousal related structures do not exert an indiscriminate activation of the CNS, but contribute to a contextual selection of relevant somatosensory inputs. In this view, the article of Götz et al. represents a further step in our understanding of such a mechanism, by suggesting that this selection occurs in the thalamus and is driven by cortifugal efferences.
http://dx.doi.org/10.1016/j.clinph.2015.01.004 1388-2457/Ó 2015 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1644
Editorial / Clinical Neurophysiology 126 (2015) 1643–1644
Another important point raised by the article of Götz et al. is the need to improve HFO analysis. Two reasons account for the difficulty in analyzing somatosensory HFOs. The first reason is related to the physiologically low signal-to-noise ratio. Classically, signalto-noise ratio is raised by greater averaging of EEG responses, in contrast with the above-mentioned main characteristic of the HFOs, that is their sensitivity to rapid dynamic changes of CNS functions. To enhance the signal-to-noise ratio of HFOs, eventually enabling single-trial analysis, recently a new method has been suggested (Waterstraat et al., 2015), the use of which seems highly promising, although it should be still validated in large population studies. The second reason is related to the difficulty in establishing the time course of HFO generators as well as their reciprocal interactions, since the visual analysis of traces hardly allows onset and the ending of any single burst to be recognized, because they are often merged in the noise or in the activity of other bursts. Although highly sophisticated and not easy-to-perform in many neurophysiological laboratories, the method introduced by Götz et al. offers the possibility to analyze both time course and reciprocal interactions of subcortical and cortical HFO generators. In conclusion, this study confirms that dynamic changes in somatosensory pathways, aimed at modifying the cortical responsivity as well as optimizing input processing, can be reliably assessed by HFOs’ studies. Moreover, this paper introduces new methods of analysis, which could, in the next future, disclose interesting and unexpected insights on the somatosensory system functions. Conflict of interest None of the authors have potential conflicts of interest to be disclosed. References Alegre M, Urriza J, Valencia M, Muruzábal J, Iriarte J, Artieda J. High-frequency oscillations in the somatosensory evoked potentials of patients with cortical myoclonus: pathophysiologic implications. J Clin Neurophysiol 2006;23:265–72. Cimatti Z, Schwartz DP, Bourdain F, Meunier S, Bleton JP, Vidailhet M, et al. Timefrequency analysis reveals decreased high-frequency oscillations in writer’s cramp. Brain 2007;130:198–205. Coppola G, Vandenheede M, Di Clemente L, Ambrosini A, Fumal A, De Pasqua V, et al. Somatosensory evoked high-frequency oscillations reflecting thalamocortical activity are decreased in migraine patients between attacks. Brain 2005;128:98–103. Gobbelé R, Buchner H, Scherg M, Curio G. Stability of high-frequency (600 Hz) components in human somatosensory evoked potentials under variation of stimulus rate. evidence for a thalamic origin. Clin Neurophysiol 1999;110:1659–63. Gobbelé R, Waberski TD, Kuelkens S, Sturm W, Curio G, Buchner H. Thalamic and cortical high-frequency (600 Hz) somatosensory-evoked potentials (SEP) components are modulated by slight arousal changes in awake subjects. Exp Brain Res 2000;133:506–13. Gobbelé R, Waberski TD, Dieckhöfer A, Kawohl W, Klostermann F, Curio G, et al. Patterns of disturbed impulse propagation in multiple sclerosis identified by low and high frequency somatosensory evoked potential components. J Clin Neurophysiol 2003;20:283–90. Götz T, Milde T, Curio G, Debener S, Lehmann T, Leistritz L, et al. Primary somatosensory contextual modulation is encoded by oscillation frequency change. Clin Neurophysiol 2015;126:1769–79.
Groves PM, Thompson RF. Habituation: a dual-process theory. Psychol Rev 1970;77:419–50. Halboni P, Kaminski R, Gobbelé R, Züchner S, Waberski TD, Herrmann CS, et al. Sleep stage dependant changes of the high-frequency part of the somatosensory evoked potentials at the thalamus and cortex. Clin Neurophysiol 2000;111:2277–84. Hamada M, Hanajima R, Terao Y, Sato F, Okano T, Yuasa K, et al. Median nerve somatosensory evoked potentials and their high-frequency oscillations in amyotrophic lateral sclerosis. Clin Neurophysiol 2007;118:877–86. Hashimoto I, Mashiko T, Imada T. Somatic evoked high-frequency magnetic oscillations reflect activity of inhibitory interneurons in the human somatosensory cortex. Electroencephalogr Clin Neurophysiol 1996;100:189–203. Inoue K, Hashimoto I, Nakamura S. High-frequency oscillations in human posterior tibial somatosensory evoked potentials are enhanced in patients with Parkinson’s disease and multiple system atrophy. Neurosci Lett 2001;297:89–92. Inoue K, Hashimoto I, Shirai T, Kawakami H, Miyachi T, Mimori Y, et al. Disinhibition of the somatosensory cortex in cervical dystonia. Decreased amplitudes of highfrequency oscillations. Clin Neurophysiol 2004;115:1624–30. Katayama T, Suppa A, Rothwell JC. Somatosensory evoked potentials and high frequency oscillations are differently modulated by theta burst stimulation over primary somatosensory cortex in humans. Clin Neurophysiol 2010;121:2097–103. Lai KL, Liao KK, Fuh JL, Wang SJ. Subcortical hyperexcitability in migraineurs: a high-frequency oscillation study. Can J Neurol Sci 2011;38:309–16. Norra C, Waberski TD, Kawohl W, Kunert HJ, Hock D, Gobbelé R, et al. Highfrequency somatosensory thalamocortical oscillations and psychopathology in schizophrenia. Neuropsychobiology 2004;49:71–80. Restuccia D, Della Marca G, Valeriani M, Rubino M, Paciello N, Vollono C, et al. Influence of cholinergic circuitries in generation of high-frequency somatosensory evoked potentials. Clin Neurophysiol 2003;114:1538–48. Restuccia D, Della Marca G, Valeriani M, Rubino M, Scarano E, Tonali P. Brain-stem components of high-frequency somatosensory evoked potentials are modulated by arousal changes: nasopharyngeal recordings in healthy humans. Clin Neurophysiol 2004;115:1392–8. Restuccia D, Valeriani M, Della Marca G. Giant subcortical high-frequency SEPs in idiopathic generalized epilepsy: a protective mechanism against seizures? Clin Neurophysiol 2007a;118:60–8. Restuccia D, Ulivelli M, De Capua A, Bartalini S, Rossi S. Modulation of highfrequency (600 Hz) somatosensory-evoked potentials after rTMS of the primary sensory cortex. Eur J Neurosci 2007b;26:2349–58. Restuccia D, Micoli B, Cazzagon M, Fantinel R, Piero ID, Della Marca G. Dissociated effects of quiet stance on standard and high-frequency (600 Hz) lower limb somatosensory evoked potentials. Clin Neurophysiol 2008;119:1408–18. Restuccia D, Del Piero I, Martucci L, Zanini S. High-frequency oscillations after median-nerve stimulation do not undergo habituation: a new insight on their functional meaning? Clin Neurophysiol 2011;122:148–52. Restuccia D, Vollono C, Del Piero I, Martucci L, Zanini S. Somatosensory high frequency oscillations reflect clinical fluctuations in migraine. Clin Neurophysiol 2012;123:2050–6. Sakuma K, Takeshima T, Ishizaki K, Nakashima K. Somatosensory evoked highfrequency oscillations in migraine patients. Clin Neurophysiol 2004;115:1857–62. Thompson RF, Spencer WA. Habituation: a model phenomenon for the study of neuronal substrates of behaviour. Psychol Rev 1966;73:16–43. Waterstraat G, Burghoff M, Fedele T, Nikulin V, Scheer HJ, Curio G. Non-invasive single-trial EEG detection of evoked human neocortical population spikes. NeuroImage 2015;15(105):13–20. Yamada T, Kameyama S, Fuchigami Y, Nakazumi Y, Dickins QS, Kimura J. Changes of short latency somatosensory evoked potential in sleep. Electroencephalogr Clin Neurophysiol 1988;70:126–36.
⇑
Domenico Restuccia Giacomo Della Marca Department of Neurosciences, Catholic University, Rome, Italy ⇑ Corresponding author at: Department of Neurosciences, Catholic University, Policlinico A. Gemelli, L.go A. Gemelli 8, 00168 Rome, Italy. E-mail address: [email protected] (D. Restuccia) Available online 23 January 2015
