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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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
Awh E, Vogel EK (2008) The bouncer in the brain. Nat Neurosci 11:5–6. doi:10.1038/nn0108-5
Baláz M, Rektor I, Pulkrábek J (2008) Participation of the subthalamic nucleus in executive functions: an intracerebral recording study. Mov Disord 23:553–557. doi:10.1002/mds.21873
Bell AJ, Sejnowski TJ (1995) An information-maximisation approach to blind separation and blind deconvolution. Neural Comput 7:1004–1034
Bledowski C, Prvulovic D, Goebel R et al (2004) Attentional systems in target and distractor processing: a combined ERP and fMRI study. Neuroimage 22:530–540. doi:10.1016/j.neuroimage.2003.12.034
Chen LC, Sandmann P, Thorne JD et al (2015) Association of concurrent fNIRS and EEG signatures in response to auditory and visual stimuli. Brain Topogr 28:710–725. doi:10.1007/s10548-015-0424-8
Coizet V, Graham JH, Moss J et al (2009) Short-latency visual input to the subthalamic nucleus is provided by the midbrain superior colliculus. J Neurosci 29:5701–5709. doi:10.1523/JNEUROSCI.0247-09.2009
Coull JT (1998) Neural correlates of attention and arousal: insights from electrophysiology, functional neuroimaging and psychopharmacology. Prog Neurobiol 55:343–361. doi:10.1016/S0301-0082(98)00011-2
De Bourbon-Teles J, Bentley P, Koshino S et al (2014) Thalamic control of human attention driven by memory and learning. Curr Biol 24:993–999. doi:10.1016/j.cub.2014.03.024
De Vos M, Gandras K, Debener S (2014) Towards a truly mobile auditory brain–computer interface: exploring the P300 to take away. Int J Psychophysiol 91:46–53. doi:10.1016/j.ijpsycho.2013.08.010
DeLong MR, Wichmann T (2007) Circuits and circuit disorders of the basal ganglia. Arch Neurol 64:20–24. doi:10.1177/155005941004100204
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
Delorme A, Sejnowski TJ, Makeig S (2007) Enhanced detection of artifacts in EEG data using higher-order statistics and independent component analysis. Neuroimaging 34:1443–1449. doi:10.1016/j.neuroimage.2006.11.004.Enhanced
Donchin E, Coles MGH (1988) Is the P300 component a manifestation of context updating? Behav Brain Sci 11:357–427
Donchin E, Coles MGH (1998) Context updating and the P300. Behav Brain Sci 21:152–154. doi:10.1017/S0140525X98230950
Downar J, Crawley AP, Mikulis DJ, Davis KD (2001) The effect of task relevance on the cortical response to changes in visual and auditory stimuli: an event-related fMRI study. Neuroimage 14:1256–1267. doi:10.1006/nimg.2001.0946
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
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
Geiser E, Kaelin-Lang A (2011) The function of dopaminergic neural signal transmission in auditory pulse perception: evidence from dopaminergic treatment in Parkinson’s patients. Behav Brain Res 225:270–275. doi:10.1016/j.bbr.2011.07.019
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
Groh A, Bokor H, Mease RA et al (2014) Convergence of cortical and sensory driver inputs on single thalamocortical cells. Cereb Cortex 24:3167–3179. doi:10.1093/cercor/bht173
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
Kajikawa Y, Schoeder E (2012) How local is the local field potential? Neuron 72:847–858. doi:10.1016/j.neuron.2011.09.029.How
Kinomura S, Larsson J, Gulyás B, Roland PE (1996) Activation by attention of the human reticular formation and thalamic intralaminar nuclei. Science 271:512–515. doi:10.1126/science.271.5248.512
Klostermann F, Wahl M, Marzinzik F et al (2006) Mental chronometry of target detection: human thalamus leads cortex. Brain 129:923–931. doi:10.1093/brain/awl014
Knight RT (1984) Decreased response to novel stimuli after prefrontal lesions in man. Electroencephalogr Clin Neurophysiol 59:9–20
Knight RT, Scabini D, Woods DL, Clayworth CC (1989) Contributions of temporal-parietal junction to the human auditory P3. Brain Res 502:109–116
Kok A (2001) On the utility of P3 amplitude as a measure of processing capacity. Psychophysiology 38:557–577. doi:10.1017/S0048577201990559
Krauss JK, Jankovic J, Grossman RG (2001) Surgery for Parkinson’s disease and movement disorders. Lippincott Williams & Wilkins, Philadelphia
Kropotov JD, Ponomarev VA (1991) Subcortical neuronal correlates of component P300 in man. Electroencephalogr Clin Neurophysiol 78:40–49
Lee T, Sejnowski TJ (1999) Independent component analysis using an extended infomax algorithm for mixed subgaussian and supergaussian sources. Neural Comput 441:417–441
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
McCarthy G, Donchin E (1981) A metric for thought: a comparison of P300 latency and reaction time. Science 211:77–80
McHaffie J, Stanford T, Stein B et al (2005) Subcortical loops through the basal ganglia. Trends Neurosci 28:401–407. doi:10.1016/j.tins.2005.06.006
Miller WC, DeLong MR (1988) Parkinsonian symptomatology. An anatomical and physiological analysis. Ann N Y Acad Sci 515:287–302. doi:10.1111/j.1749-6632.1988.tb32998.x
Näätänen R, Picton T (1987) The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiology 24:375–425. doi:10.1111/j.1469-8986.1987.tb00311.x
Nicola SM, Surmeier DJ, Malenka RC (2000) Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23:185–215
Paus T, Zatorre RJ, Hofle N et al (1997) Time-related changes in neural systems underlying attention and arousal during the performance of an auditory vigilance task. J Cogn Neurosci 9:392–408. doi:10.1162/jocn.1997.9.3.392
Polich J (2007) Updating P300: an integrative theory of P3a and P3b. Clin Neurophysiol 118:2128–2148. doi:10.1016/j.clinph.2007.04.019.Updating
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
Redgrave P, Prescott TJ, Gurney K (1999a) The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89:1009–1023. doi:10.1016/S0306-4522(98)00319-4
Redgrave P, Prescott TJ, Gurney K (1999b) Is the short latency dopamine burst too short to signal reinforcement error? Trends Neurosci 22:146–151
Redgrave P, Gurney K, Reynolds J (2008) What is reinforced by phasic dopamine signals? Brain Res Rev 58:322–339. doi:10.1016/j.brainresrev.2007.10.007
Redgrave P, Coizet V, Comoli E et al (2010) Interactions between the midbrain superior colliculus and the basal ganglia. Front Neuroanat. doi:10.3389/fnana.2010.00132
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
Rektor I, Kaňovský P, Bareš M et al (2003) A SEEG study of ERP in motor and premotor cortices and in the basal ganglia. Clin Neurophysiol 114:463–471. doi:10.1016/S1388-2457(02)00388-7
Rektor I, Bares M, Kanovský P et al (2004) Cognitive potentials in the basal ganglia-frontocortical circuits. An intracerebral recording study. Exp Brain Res 158:289–301. doi:10.1007/s00221-004-1901-6
Rektor I, Bares M, Brázdil M et al (2005) Cognitive- and movement-related potentials recorded in the human basal ganglia. Mov Disord 20:562–568. doi:10.1002/mds.20368
Sandmann P, Eichele T, Buechler M et al (2009) Evaluation of evoked potentials to dyadic tones after cochlear implantation. Brain 132:1967–1979. doi:10.1093/brain/awp034
Sandmann P, Kegel A, Eichele T et al (2010) Neurophysiological evidence of impaired musical sound perception in cochlear-implant users. Clin Neurophysiol 121:2070–2082. doi:10.1016/j.clinph.2010.04.032
Sandmann P, Plotz K, Hauthal N et al (2015) Rapid bilateral improvement in auditory cortex activity in postlingually deafened adults following cochlear implantation. Clin Neurophysiol 126:594–607. doi:10.1016/j.clinph.2014.06.029
Sauleau P, Eusebio A, Thevathasan W et al (2009) Involvement of the subthalamic nucleus in engagement with behaviourally relevant stimuli. Eur J Neurosci 29:931–942. doi:10.1111/j.1460-9568.2009.06635.x
Schepers IM, Beck A-K, Bräuer S et al (2017) Human centromedian-parafascicular complex signals sensory cues for goal-oriented behavior selection. Neuroimage 152:390–399. doi:10.1016/j.neuroimage.2017.03.019
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
Schiff ND (2008) Central thalamic contributions to arousal regulation and neurological disorders of consciousness. Ann N Y Acad Sci 1129:105–118. doi:10.1196/annals.1417.029
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
Steriade M (1996) Arousal: revisiting the reticular activating system. Science 272:225–226. doi:10.1126/science.272.5259.225
Trenado C, Haab L, Strauss DJ (2009) Corticothalamic feedback dynamics for neural correlates of auditory selective attention. IEEE Trans Neural Syst Rehabil Eng 17:46–52. doi:10.1109/TNSRE.2008.2010469
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
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
Verleger R (1997) On the utility of P3 latency as an index of mental chronometry. Psychophysiology 34:131–156. doi:10.1111/j.1469-8986.1997.tb02125.x
Verleger R (2008) P3b: towards some decision about memory. Clin Neurophysiol 119:968–970. doi:10.1016/j.clinph.2007.11.175
Vogel EK, Luck SJ, Shapiro KL (1998) Electrophysiological evidence for a postperceptual locus of suppression during the attentional blink. J Exp Psychol Hum Percept Perform 24:1656–1674. doi:10.1037/0096-1523.24.6.1656
Wichmann T, Delong MR (1996) Functional and pathophysiological models of the basal ganglia. Curr Opin Neurobiol 6:751–758. doi:10.1016/S0959-4388(96)80024-9
Widmann A, Schröger E (2012) Filter effects and filter artifacts in the analysis of electrophysiological data. Front Psychol 3:1–5. doi:10.3389/fpsyg.2012.00233
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)
Yamaguchi S, Knight RT (1991) Anterior and posterior association cortex contributions to the somatosensory P300. J Neurosci 11:2039–2054
Yingling CD, Hosobuchi Y (1984) A subcortical correlate of P300 in man. Electroencephalogr Clin Neurophysiol 59:72–76. doi:10.1016/0168-5597(84)90022-4
Zaehle T, Bauch EM, Hinrichs H et al (2013) Nucleus accumbens activity dissociates different forms of salience: evidence from human intracranial recordings. J Neurosci 33:8764–8771. doi:10.1523/JNEUROSCI.5276-12.2013
Zeng F-G (1994) Loudness growth in forward masking: relation to intensity discrimination. J Acoust Soc Am 96:2127–2132
Acknowledgements
This research was supported by the Deutsche Forschungsgemeinschaft Cluster of Excellence EXC 1077 “Hearing4All”. The authors would like to thank Hans Heissler for the technical support.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
All procedures performed in the study were in accordance with the local ethics committee (Medical School of Hanover, Germany) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Rights and permissions
About this article
Cite this article
Beck, AK., Lütjens, G., Schwabe, K. et al. Thalamic and basal ganglia regions are involved in attentional processing of behaviorally significant events: evidence from simultaneous depth and scalp EEG. Brain Struct Funct 223, 461–474 (2018). https://doi.org/10.1007/s00429-017-1506-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-017-1506-z