Origin and distribution of thalamic somatosensory evoked potentials in humans

doi:10.1016/0013-4694(89)90004-7

Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section

Volume 74, Issue 3, May–June 1989, Pages 186-193

https://doi.org/10.1016/0013-4694(89)90004-7 Get rights and content

Summary

The distribution and generator sources of somatosensory evoked potentials (SEPs) in the thalamus and subthalamic area were studied, using a ‘semi-microelectrode’ during stereotaxic surgery on 34 patients with involuntary movements or intractable pain. Electrical stimulation was given to the median nerve at the wrist. Two distinct SEPs were evoked by contralateral stimulation. A high voltage (160 μV) positive SEP with a peak latency of 15.5 msec was strictly confined to the ventral part of the sensory relay nucleus (nucleus ventro-caudalis, V.c). A much lower voltage, positive-negative-positive triphasic SEP showed peak latencies of the initial positivity and the major negativity of 13.3 msec and 16.0 msec, respectively, and had maximal voltage (16 μV) in the ventralmost parts of the nucleus ventro-intermedius (V.in) and radiatio praelemniscalis (Ra.prl), and substantial potentials in the lemnicus medialis (L.m) and nucleus ventro-oralis posterior (V.o.p). The potential field of the triphasic SEP spread farther across the different thalamic nuclei and subthalamic region with identical configurations and peak latencies, but with decreasing amplitude. These findings suggest that the high voltage positive SEP reflects a postsynaptic potential generated by the V.c neurons, and the smaller triphasic SEP a presynaptic axonal potential generated in the rostral part of the lemniscal pathway, extending by means of volume conduction.

References (20)

Albe-FessardD. et al.
Comparison in man of short latency averaged evoked potentials recorded in thalamic and scalp hand zones of representation
Electroenceph. clin. Neurophysiol.
(1986)
ArezzoJ. et al.
Topography and intracranial sources of somatosensory evoked potentials in the monkey. I. Early components
Electroenceph. clin. Neurophysiol.
(1979)
HashimotoI.
Somatosensory evoked potentials from the human brain-stem: origins of short latency potentials
Electroenceph. clin. Neurophysiol.
(1984)
KatayamaY. et al.
Somatosensory evoked potentials from the thalamic sensory relay nucleus (VPL) in human: correlations with short latency somatosensory evoked potentials recorded at the scalp
Electroenceph. clin. Neurophysiol.
(1987)
MaccabeeP.J. et al.
Short latency somatosensory evoked potentials to median nerve stimulation: effect of low frequency filter
Electroenceph. clin. Neurophysiol.
(1983)
SuzukiI. et al.
Intracranial recording of short latency somatosensory evoked potentials in man: identification of origin of each component
Electroenceph. clin. Neurophysiol.
(1984)
ThodenU. et al.
Medial thalamic permanent electrodes for pain control in man: an electrophysiological and clinical study
Electroenceph. clin. Neurophysiol.
(1979)
TsujiS. et al.
Subcortical, thalamic and cortical somatosensory evoked potentials to median nerve stimulation
Electroenceph. clin. Neurophysiol.
(1984)
CelesiaG.G.
Somatosensory evoked potentials recorded directly from human thalamus and SmI cortical area
Arch. Neurol.
(1979)
ChangH.T.
The evoked potentials

There are more references available in the full text version of this article.

Cited by (33)

A new potential specifically marks the sensory thalamus in anaesthetised patients
2019, Clinical Neurophysiology
Citation Excerpt :
Therefore, we cannot conclude that both kinds of recordings, although phenomenologically similar, correspond to the same generators. The most detailed descriptions of the analysis of VHFOs were made with macroelectrodes (Morioka et al., 1989; Hanajima et al., 2004a, 2004b; Klostermann et al., 2002, Shima et al., 1991). The characteristics described are similar to those in our study in terms of latency and frequency (1408 ± 170 Hz) and less for duration and amplitude, which were approximately one-tenth of those in our study.
During deep brain stimulation (DBS) surgery, we analysed somatosensory evoked potentials (SSEPs) using microelectrode recordings (MERs) in patients under general anaesthesia.
We obtained MERs from 5 patients with refractory epilepsy. Off-line analysis isolated local field potentials (LFPs, 2–200 Hz) and high frequency components (HFCs, 0.5–5 kHz). Trajectories were reconstructed off-line.
The ventral caudate (V.c.) nucleus was most frequently recorded from (171 mm). Very high frequency oscillations (VHFOs) were recorded up to 8 mm in length from all 4 electrodes but were most frequently recorded from the V.c. The properties of VHFOs were similar among all nuclei (frequency >1500 Hz, amplitude ∼3 µV, starting time ∼14 ms, duration 8–9 ms). Consecutive recordings did not show any synchronization or propagation, but a new kind of potential (high frequency oscillation, HFO) appeared abruptly inside the V.c. (frequency = 848 ± 66 Hz, amplitude = 5.2 ± 1.8 µV starting at 17.7 ± 0.5 ms, spanning 3.4 ± 0.3 ms).
VHFOs are widely extending and cannot be ascribed to the V.c. HFOs in patients under general anaesthesia can serve as a landmark to identify the V.c. in thalamic DBS surgery.
Thalamic processing involves nuclei other than the V.c, and HFO can be used to improve DBS surgery.
Low- and high-frequency subcortical SEP amplitude reduction during pure passive movement
2015, Clinical Neurophysiology
Citation Excerpt :
According to these studies, the responses recorded from the VIM could be generated within the VPL nucleus itself. However, VIM SEPs can also reflect far-field potentials suggestive of volume conduction from the lemniscal pathway (Morioka et al., 1989; Shima et al., 1991). In humans, high-frequency activities have been recorded by electrodes implanted in the central nervous system for neuromodulation such as in the primary somatosensory cortex (Barba et al., 2004; Insola et al., 2012b), in deep brain nuclei (Klostermann et al., 2002a; Hanajima et al., 2004b; Insola et al., 2004, 2012b, 2014; Yeh et al., 2010), and in cervical spinal cord (Insola et al., 2008, 2010).
To investigate the effect of pure passive movement on both cortical and subcortical somatosensory evoked potentials (SEPs).
Median nerve SEPs were recorded in 8 patients suffering from Parkinson’s disease (PD) and two patients with essential tremor. PD patients underwent electrode implantation in the subthalamic (STN) nucleus (3 patients) and pedunculopontine (PPTg) nucleus (5 patients), while 2 patients with essential tremor were implanted in the ventral intermediate nucleus (VIM) of the thalamus. In anesthetized patients, SEPs were recorded at rest and during a passive movement of the thumb of the stimulated wrist from the intracranial electrode contacts and from the scalp. Also the high-frequency oscillations (HFOs) were analyzed.
Amplitudes of both deep and scalp components were decreased during passive movement, but the reduction was higher at cortical than subcortical level. Also the HFOs were reduced by movement.
The different amount of the movement-related decrease suggests that the cortical SEP gating is not only the result of a subcortical somatosensory volley attenuation, but a further mechanism acting at cortical level should be considered.
Our results are important for understanding the physiological mechanism of the sensory–motor interaction during passive movement.
Low and high-frequency somatosensory evoked potentials recorded from the human pedunculopontine nucleus
2014, Clinical Neurophysiology
Citation Excerpt :
There are 4 main elements that make unlikely the possibility that the P16 potential may originate from other neural structures, caudal or rostral to PPTg electrode, such as the dorsal column nuclei (DCN) and the thalamus. First, previous studies recording SEPs from the DCN and the thalamus after median nerve stimulation (Hsieh et al., 1995; Mazzone and Scarnati, 2009b; Møller et al., 1986; Morioka et al., 1989, 1991a,b; Shima et al., 1991) showed that the responses originated from the DCN and from the thalamus have latencies, respectively, shorter and longer than the present P16 latency. Second, the DCN and thalamic waveforms have morphologies differing from that of the biphasic potential recorded from the PPTg lead.
To investigate the generators of the somatosensory evoked potential (SEP) components recorded from the Pedunculopontine Tegmental nucleus (PPTg).
Twenty-two patients, suffering from Parkinson’s disease (PD), underwent electrode implantation in the PPTg area for deep brain stimulation (DBS). SEPs were recorded from the DBS electrode contacts to median nerve stimulation.
SEPs recorded from the PPTg electrode contacts could be classified in 3 types, according to their waveforms. (1) The biphasic potential showed a positive peak (P16) whose latency (16.05 ± 0.61 ms) shifted of 0.18 ± 0.07 ms from the lower to the upper contact of the electrode. (2) The triphasic potential showed an initial positive peak (P15) whose latency (15.4 ± 0.2 ms) did not change across the DBS electrode contacts. (3) In the last SEP configuration (mixed biphasic and triphasic waveform), the positive peak was bifid including both the P15 and P16 potentials.
While the P16 potential is probably generated by the somatosensory volley travelling along the medial lemniscus, the P15 response represents a far-field potential probably generated at the cuneate nucleus level.
Our results show the physiological meaning of the somatosensory responses recorded from the PPTg nucleus area.
Laser evoked potential recording from intracerebral deep electrodes
2009, Clinical Neurophysiology
Citation Excerpt :
During the days immediately following the implant, the stimulator is kept switched off but the IC lead is still accessible, so that the four contacts can be connected to the neurophysiological equipment and used as IC recording sites. In a previous study, we could record both low- and high-frequency subcortical SEP components from IC electrodes placed in the STN and GPi (Insola et al., 2004), thus confirming what found with IC leads placed within or near the thalamus (Celesia, 1979; Hashimoto, 1984; Suzuki and Mayanagi, 1984; Tsuji et al., 1984; Albe-Fessard et al., 1986; Katayama and Tsubokawa, 1987; Morioka et al., 1989; Insola et al., 1999; Pinter, 1999; Klostermann et al., 1999). Our present study aimed at recording LEPs from IC electrodes placed in STN (close to the thalamus), GPi, and PPN (close to the ascending spino-thalamic pathway) in Parkinsonian patients submitted to electrode implantation for DBS.
To investigate whether recording from deep intracerebral (IC) electrodes can disclose laser evoked potential (LEP) components generated under the cerebral cortex.
LEPs were recorded to hand and/or perioral region stimulation from 7 patients suffering from Parkinson’s disease, who underwent implant of IC electrodes in the globus pallidum pars interna (GPi), in the subthalamic nucleus (STN) and in the pedunculopontine nucleus (PPN). LEPs were obtained from the IC electrode contacts and from the Cz vertex, referred to the nose.
The scalp traces showed a triphasic response (P1-N2-P2). The IC electrodes recorded two main components (ICP2 and ICN2), showing the same latencies as the scalp N2 and P2 potentials, respectively. The ICP2-ICN2 complex was sometimes preceded by a ICP1 wave at the same latency of the scalp P1 response.
The LEP components recorded from the IC electrodes mirrored the ones picked up from the Cz lead, thus suggesting that they are probably generated by the opposite pole of the same cortical sources producing the scalp responses.
In the IC traces, there was no evidence of earlier potentials possibly generated within the thalamus or of subcortical far-field responses. This means that the nociceptive signal amplification occurring within the cerebral cortex is necessary to produce identifiable LEP components.
Dissociation of thalamic high frequency oscillations and slow component of sensory evoked potentials following damage to ascending pathways
2006, Clinical Neurophysiology
Somatosensory evoked potentials (SEPs) recorded from the thalamus have a slow component and high frequency (∼1000 Hz) oscillations (HFOs). In this study, we examined how lesions in the sensory afferent pathway affect these components.
Thalamic SEPs to contralateral median nerve stimulation were recorded from deep brain stimulation electrodes in two patients. Patient 1 had spinal cord injury at the C4/5 level. Patient 2 had multiple sclerosis with mid brain lesions. Seven patients with no brain or cervical spinal cord lesions served as controls.
In both patients, the low frequency component of the SEP (LF SEP) was delayed and/or prolonged and greatly decreased in amplitude compared with controls. HFOs were recorded in both patients. The latencies of onset and peak of the HFOs were approximately the same as those of the LF SEPs and their amplitudes were similarly reduced. However, their frequency was similar to that of the control group. Cortical SEPs were absent in both patients.
Normal frequencies of thalamic HFOs in association with increased peak latencies, and decreased amplitudes provide further evidence that the HFOs are likely due to intrinsic oscillations in the thalamus rather than high frequency synchronous inputs.
Thalamic HFOs are closely associated with the LF SEP but are generated by a different mechanism.
Chapter 17 Intraoperative recording of the very fast oscillatory activities evoked by median nerve stimulation in the human thalamus
2006, Supplements to Clinical Neurophysiology
This chapter characterizes thalamic very fast oscillations (VFOs) and their relationship with thalamic neuronal firing. VFOs at a frequency of 500–700 Hz are superimposed on scalp-recorded cortical potentials from the human sensory cortex (S1). VFOs have also been observed as small notches superimposed on positive SEPs recorded with electrodes in the human thalamus. In the chapter, microstimulation is performed at regular intervals and perceptual and/or motor effects are determined. This strategy allowed a physiological map to be constructed relative to the imaged coordinates. The recorded VFOs showed phase reversal at the anterior commisure (AC)–posterior commisure (PC) line and their amplitudes were largest near the AC–PC line. Tactile neuron firing was closely correlated with VFOs. The chapter suggests that either VFOs may determine the exact time of neuron firing in ventrocaudal nucleus (Vc) or that Vc neuron firing is somehow time-locked in a repetitive pattern, giving rise to oscillatory VFO.

View all citing articles on Scopus

: This study was supported in part by a Grant-in-Aid for Scientific Research on Priority Areas, Ministry of Education, Science and Culture, Japan.

View full text

Origin and distribution of thalamic somatosensory evoked potentials in humans

Summary

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Somatosensory evoked potentials recorded directly from human thalamus and SmI cortical area

Arch. Neurol.

The evoked potentials