Skip to main content
main-content
Erschienen in: Brain Structure and Function 1/2018

04.09.2017 | Original Article

Thalamic and basal ganglia regions are involved in attentional processing of behaviorally significant events: evidence from simultaneous depth and scalp EEG

verfasst von: Anne-Kathrin Beck, Götz Lütjens, Kerstin Schwabe, Reinhard Dengler, Joachim K. Krauss, Pascale Sandmann

Erschienen in: Brain Structure and Function | Ausgabe 1/2018

Einloggen, um Zugang zu erhalten

Abstract

Extensive descriptions exist on cortical responses to change in the acoustic environment. However, the involvement of subcortical regions is not well understood. Here we present simultaneous recordings of cortical and subcortical event-related potentials (ERPs) to different pure tones in patients undergoing surgery for deep brain stimulation (DBS). These patients had externalized electrodes in the subthalamic nucleus (STN), the ventrolateral posterior thalamus (VLp) or the globus pallidus internus (GPi). Subcortical and cortical ERPs were analyzed upon presentation of one frequent non-target stimulus and two infrequent stimuli, either being a target or a distractor stimulus. The results revealed that amplitudes of scalp-recorded P3 and subcortical late attention-modulated responses (AMR) were largest upon presentation of target stimuli compared with distractor stimuli. This suggests that thalamic and basal ganglia regions are sensitive to behaviorally relevant auditory events. Comparison of the subcortical structures showed that responses in VLp have shorter latency than in GPi and STN. Further, the subcortical responses in VLp and STN emerged significantly prior to the cortical P3 response. Our findings point to higher-order cognitive functions already at a subcortical level. Auditory events are categorized as behaviorally relevant in subcortical loops involving basal ganglia and thalamic regions. This label is then distributed to cortical regions by ascending projections.
Literatur
Zurück zum Zitat Allen JB (1990) Loudness growth in 1/2-octave bands (LGOB)—a procedure for the assessment of loudness. J Acoust Soc Am 88:745–753 CrossRefPubMed Allen JB (1990) Loudness growth in 1/2-octave bands (LGOB)—a procedure for the assessment of loudness. J Acoust Soc Am 88:745–753 CrossRefPubMed
Zurück zum Zitat Bell AJ, Sejnowski TJ (1995) An information-maximisation approach to blind separation and blind deconvolution. Neural Comput 7:1004–1034 CrossRef Bell AJ, Sejnowski TJ (1995) An information-maximisation approach to blind separation and blind deconvolution. Neural Comput 7:1004–1034 CrossRef
Zurück zum Zitat Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods Methods 134:9–21 CrossRef Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods Methods 134:9–21 CrossRef
Zurück zum Zitat Donchin E, Coles MGH (1988) Is the P300 component a manifestation of context updating? Behav Brain Sci 11:357–427 CrossRef Donchin E, Coles MGH (1988) Is the P300 component a manifestation of context updating? Behav Brain Sci 11:357–427 CrossRef
Zurück zum Zitat Dürschmid S, Zaehle T, Hinrichs H et al (2015) Sensory deviancy detection measured directly within the human nucleus accumbens. Cereb Cortex 26:1–8. doi: 10.​1093/​cercor/​bhu304 Dürschmid S, Zaehle T, Hinrichs H et al (2015) Sensory deviancy detection measured directly within the human nucleus accumbens. Cereb Cortex 26:1–8. doi: 10.​1093/​cercor/​bhu304
Zurück zum Zitat Fisher SD, Reynolds JNJ (2014) The intralaminar thalamus—an expressway linking visual stimuli to circuits determining agency and action selection. Front Behav Neurosci 8:1–7. doi: 10.​3389/​fnbeh.​2014.​00115 Fisher SD, Reynolds JNJ (2014) The intralaminar thalamus—an expressway linking visual stimuli to circuits determining agency and action selection. Front Behav Neurosci 8:1–7. doi: 10.​3389/​fnbeh.​2014.​00115
Zurück zum Zitat Glenn LL, Steriade M (1982) Discharge rate and excitability of cortically projecting intralaminar thalamic neurons during waking and sleep states. J Neurosci 2:1387–1404 PubMed Glenn LL, Steriade M (1982) Discharge rate and excitability of cortically projecting intralaminar thalamic neurons during waking and sleep states. J Neurosci 2:1387–1404 PubMed
Zurück zum Zitat Hari R, Aittoniemi K, Järvinen M-L et al (1980) Auditory evoked transient and sustained magnetic fields of the human brain. Exp Brain Res 40:237–240 CrossRefPubMed Hari R, Aittoniemi K, Järvinen M-L et al (1980) Auditory evoked transient and sustained magnetic fields of the human brain. Exp Brain Res 40:237–240 CrossRefPubMed
Zurück zum Zitat Knight RT (1984) Decreased response to novel stimuli after prefrontal lesions in man. Electroencephalogr Clin Neurophysiol 59:9–20 CrossRefPubMed Knight RT (1984) Decreased response to novel stimuli after prefrontal lesions in man. Electroencephalogr Clin Neurophysiol 59:9–20 CrossRefPubMed
Zurück zum Zitat Knight RT, Scabini D, Woods DL, Clayworth CC (1989) Contributions of temporal-parietal junction to the human auditory P3. Brain Res 502:109–116 CrossRefPubMed Knight RT, Scabini D, Woods DL, Clayworth CC (1989) Contributions of temporal-parietal junction to the human auditory P3. Brain Res 502:109–116 CrossRefPubMed
Zurück zum Zitat Krauss JK, Jankovic J, Grossman RG (2001) Surgery for Parkinson’s disease and movement disorders. Lippincott Williams & Wilkins, Philadelphia Krauss JK, Jankovic J, Grossman RG (2001) Surgery for Parkinson’s disease and movement disorders. Lippincott Williams & Wilkins, Philadelphia
Zurück zum Zitat Kropotov JD, Ponomarev VA (1991) Subcortical neuronal correlates of component P300 in man. Electroencephalogr Clin Neurophysiol 78:40–49 CrossRefPubMed Kropotov JD, Ponomarev VA (1991) Subcortical neuronal correlates of component P300 in man. Electroencephalogr Clin Neurophysiol 78:40–49 CrossRefPubMed
Zurück zum Zitat Lee T, Sejnowski TJ (1999) Independent component analysis using an extended infomax algorithm for mixed subgaussian and supergaussian sources. Neural Comput 441:417–441 CrossRef Lee T, Sejnowski TJ (1999) Independent component analysis using an extended infomax algorithm for mixed subgaussian and supergaussian sources. Neural Comput 441:417–441 CrossRef
Zurück zum Zitat Matsumoto N, Minamimoto T, Graybiel AM, Kimura M (2001) Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. J Neurophysiol 85:960–976 CrossRefPubMed Matsumoto N, Minamimoto T, Graybiel AM, Kimura M (2001) Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. J Neurophysiol 85:960–976 CrossRefPubMed
Zurück zum Zitat McCarthy G, Donchin E (1981) A metric for thought: a comparison of P300 latency and reaction time. Science 211:77–80 CrossRefPubMed McCarthy G, Donchin E (1981) A metric for thought: a comparison of P300 latency and reaction time. Science 211:77–80 CrossRefPubMed
Zurück zum Zitat Nicola SM, Surmeier DJ, Malenka RC (2000) Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23:185–215 CrossRefPubMed Nicola SM, Surmeier DJ, Malenka RC (2000) Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23:185–215 CrossRefPubMed
Zurück zum Zitat Portas CM, Rees G, Howseman AM et al (1998) A specific role for the thalamus in mediating the interaction of attention and arousal in humans. J Neurosci 18:8979–8989 PubMed Portas CM, Rees G, Howseman AM et al (1998) A specific role for the thalamus in mediating the interaction of attention and arousal in humans. J Neurosci 18:8979–8989 PubMed
Zurück zum Zitat Redgrave P, Prescott TJ, Gurney K (1999b) Is the short latency dopamine burst too short to signal reinforcement error? Trends Neurosci 22:146–151 CrossRefPubMed Redgrave P, Prescott TJ, Gurney K (1999b) Is the short latency dopamine burst too short to signal reinforcement error? Trends Neurosci 22:146–151 CrossRefPubMed
Zurück zum Zitat Reiner A (2010) The conservative evolution of the vertebrate basal ganglia. In: Steiner H, Tseng KY (eds) Handbook of basal ganglia structure and function. Elsevier, pp 29–62 Reiner A (2010) The conservative evolution of the vertebrate basal ganglia. In: Steiner H, Tseng KY (eds) Handbook of basal ganglia structure and function. Elsevier, pp 29–62
Zurück zum Zitat Schierholz I, Finke M, Kral A et al (2017) Auditory and audio-visual processing in patients with cochlear, auditory brainstem, and auditory midbrain implants: an EEG study. Hum Brain Mapp 2225:2206–2225. doi: 10.​1002/​hbm.​23515 CrossRef Schierholz I, Finke M, Kral A et al (2017) Auditory and audio-visual processing in patients with cochlear, auditory brainstem, and auditory midbrain implants: an EEG study. Hum Brain Mapp 2225:2206–2225. doi: 10.​1002/​hbm.​23515 CrossRef
Zurück zum Zitat Stanzione P, Fattapposta F, Giunti P et al (1991) P300 variations in parkinsonian patients before and during dopaminergic monotherapy: a suggested dopamine component in P300. Electroencephalogr Clin Neurophysiol 80:446–453 CrossRefPubMed Stanzione P, Fattapposta F, Giunti P et al (1991) P300 variations in parkinsonian patients before and during dopaminergic monotherapy: a suggested dopamine component in P300. Electroencephalogr Clin Neurophysiol 80:446–453 CrossRefPubMed
Zurück zum Zitat Velasco M, Velasco F, Olvera A (1985) Subcortical correlates of the somatic, auditory and visual vertex activities in man. I. bipolar EEG response and electrical stimulation. Electroencephalogr Clin Neurophysiol 61:519–529 CrossRefPubMed Velasco M, Velasco F, Olvera A (1985) Subcortical correlates of the somatic, auditory and visual vertex activities in man. I. bipolar EEG response and electrical stimulation. Electroencephalogr Clin Neurophysiol 61:519–529 CrossRefPubMed
Zurück zum Zitat Velasco M, Velasco F, Velasco ANAL et al (1986) Subcortical correlates of the P300 potential complex in man to auditory stimuli. Electroencephalogr Clin Neurophysiol 64:199–210 CrossRefPubMed Velasco M, Velasco F, Velasco ANAL et al (1986) Subcortical correlates of the P300 potential complex in man to auditory stimuli. Electroencephalogr Clin Neurophysiol 64:199–210 CrossRefPubMed
Zurück zum Zitat Wronka E, Kaiser J, Coenen AML (2012) Neural generators of the auditory evoked potential components P3a and P3b. Acta Neurobiol Exp (Wars) 72:51–64 (pii 7205) Wronka E, Kaiser J, Coenen AML (2012) Neural generators of the auditory evoked potential components P3a and P3b. Acta Neurobiol Exp (Wars) 72:51–64 (pii 7205)
Zurück zum Zitat Yamaguchi S, Knight RT (1991) Anterior and posterior association cortex contributions to the somatosensory P300. J Neurosci 11:2039–2054 PubMed Yamaguchi S, Knight RT (1991) Anterior and posterior association cortex contributions to the somatosensory P300. J Neurosci 11:2039–2054 PubMed
Zurück zum Zitat Zeng F-G (1994) Loudness growth in forward masking: relation to intensity discrimination. J Acoust Soc Am 96:2127–2132 CrossRefPubMed Zeng F-G (1994) Loudness growth in forward masking: relation to intensity discrimination. J Acoust Soc Am 96:2127–2132 CrossRefPubMed
Metadaten
Titel
Thalamic and basal ganglia regions are involved in attentional processing of behaviorally significant events: evidence from simultaneous depth and scalp EEG
verfasst von
Anne-Kathrin Beck
Götz Lütjens
Kerstin Schwabe
Reinhard Dengler
Joachim K. Krauss
Pascale Sandmann
Publikationsdatum
04.09.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 1/2018
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1506-z

Weitere Artikel der Ausgabe 1/2018

Brain Structure and Function 1/2018 Zur Ausgabe

Neu im Fachgebiet Neurologie

Newsletter

Bestellen Sie unseren kostenlosen Newsletter Update Neurologie und bleiben Sie gut informiert – ganz bequem per eMail.