Involvement of the subthalamic nucleus and globus pallidus internus in attention

We studied the appearance of cognitive event-related potentials (ERPs) and event-related de/synchronizations (ERD/S) in the subthalamic nucleus (STN) and globus pallidus internus (GPi). We particularly focused on the rare non-target (distractor) stimuli processing. ERPs and ERD/S in the alpha and beta frequency range were analyzed in seven Parkinson’s disease patients and one primary dystonia patient with implanted deep brain stimulation (DBS) electrodes. A visual three-stimulus protocol was used (frequent stimulus, target stimulus, and distractor). The non-target and distractor-related waveforms manifested similar shapes. A specific positive ERP peak around 200 ms and a low alpha frequency ERS were detected from the STN as a response to the distractor stimuli in six of the patients with Parkinson’s disease and also in the primary dystonia patient’s GPi. This positivity probably reflects an attentional orienting response to the distractor stimuli. The STN and GPi are probably involved in attentional cerebral networks.

[1]  H. Steinbusch,et al.  The functional role of the subthalamic nucleus in cognitive and limbic circuits , 2005, Progress in Neurobiology.

[2]  Paul Krack,et al.  Deep brain stimulation: Neuropsychological and neuropsychiatric issues , 2006, Movement disorders : official journal of the Movement Disorder Society.

[3]  T. Robbins,et al.  Lesions of the medial and lateral striatum in the rat produce differential deficits in attentional performance. , 2001, Behavioral neuroscience.

[4]  M. Mesulam,et al.  The central role of the prefrontal cortex in directing attention to novel events. , 2000, Brain : a journal of neurology.

[5]  Paavo Alku,et al.  Increased distractibility in closed head injury as revealed by event‐related potentials , 2000, Neuroreport.

[6]  R. Wennberg,et al.  Intracranial volume conduction of cortical spikes and sleep potentials recorded with deep brain stimulating electrodes , 2003, Clinical Neurophysiology.

[7]  D. Sholl The organization of the cerebral cortex , 1957 .

[8]  Christo Pantev,et al.  Conflict and inhibition differentially affect the N200/P300 complex in a combined go/nogo and stop-signal task , 2010, NeuroImage.

[9]  W. Klimesch EEG-alpha rhythms and memory processes. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[10]  N. Squires,et al.  Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. , 1975, Electroencephalography and clinical neurophysiology.

[11]  R. Knight Decreased response to novel stimuli after prefrontal lesions in man. , 1984, Electroencephalography and clinical neurophysiology.

[12]  L. Hazrati,et al.  Functional anatomy of the basal ganglia , 1995 .

[13]  J. Saint-Cyr,et al.  The subthalamic nucleus in the context of movement disorders. , 2004, Brain : a journal of neurology.

[14]  A. Medl,et al.  Time Frequency and Wavelets in Biomedical Signal Processing , 1998, IEEE Engineering in Medicine and Biology Magazine.

[15]  A. Benabid,et al.  Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. , 2003, The New England journal of medicine.

[16]  Bettina Schrader,et al.  Manic episode with psychotic symptoms induced by subthalamic nucleus stimulation in a patient with Parkinson's disease , 2003, Movement disorders : official journal of the Movement Disorder Society.

[17]  R. Knight Distributed Cortical Network for Visual Attention , 1997, Journal of Cognitive Neuroscience.

[18]  J. Polich Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[19]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. I. Superior temporal plane and parietal lobe. , 1995, Electroencephalography and clinical neurophysiology.

[20]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. II. Medial, lateral and posterior temporal lobe. , 1995, Electroencephalography and clinical neurophysiology.

[21]  J. Polich,et al.  P300 and alpha event-related desynchronization (ERD). , 2001, Psychophysiology.

[22]  J. Penney,et al.  The functional anatomy of basal ganglia disorders , 1989, Trends in Neurosciences.

[23]  Bettina Sorger,et al.  Novelty and target processing during an auditory novelty oddball: A simultaneous event-related potential and functional magnetic resonance imaging study , 2008, NeuroImage.

[24]  M. Brázdil,et al.  A SEEG study of ERP in motor and premotor cortices and in the basal ganglia , 2003, Clinical Neurophysiology.

[25]  S. Houle,et al.  Stimulation of the subthalamic nucleus and impulsivity: Release your horses , 2009, Annals of neurology.

[26]  G Pfurtscheller,et al.  Functional Topography During a Visuoverbal Judgment Task Studied with Event‐Related Desynchronization Mapping , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[27]  J. Intriligator,et al.  On the relationship between EEG and ERP variability. , 1995, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[28]  Adrian Danek,et al.  Neuropsychological and psychiatric changes after deep brain stimulation for Parkinson's disease: a randomised, multicentre study , 2008, The Lancet Neurology.

[29]  W. van Winsum,et al.  Event-related desynchronization and P300. , 1987, Psychophysiology.

[30]  T. Robbins,et al.  Effects of dopamine depletion of the dorsal striatum and further interaction with subthalamic nucleus lesions in an attentional task in the rat , 1999, Neuroscience.

[31]  A. Nambu,et al.  Functional significance of the cortico–subthalamo–pallidal ‘hyperdirect’ pathway , 2002, Neuroscience Research.

[32]  M. Amalric,et al.  The subthalamic nucleus exerts opposite control on cocaine and 'natural' rewards , 2005, Nature Neuroscience.

[33]  G. McCarthy,et al.  Augmenting mental chronometry: the P300 as a measure of stimulus evaluation time. , 1977, Science.

[34]  J. Saint-Cyr,et al.  Neuropsychological consequences of chronic bilateral stimulation of the subthalamic nucleus in Parkinson's disease. , 2000, Brain : a journal of neurology.

[35]  K Lehnertz,et al.  Verbal novelty detection within the human hippocampus proper. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[36]  D. Bowers,et al.  Cognition and mood in Parkinson's disease in subthalamic nucleus versus globus pallidus interna deep brain stimulation: The COMPARE Trial , 2009, Annals of neurology.

[37]  I. Rektor,et al.  Participation of the subthalamic nucleus in executive functions: An intracerebral recording study , 2008, Movement disorders : official journal of the Movement Disorder Society.

[38]  W. Byblow,et al.  Intracortical inhibition during volitional inhibition of prepared action. , 2006, Journal of neurophysiology.

[39]  T. Robbins,et al.  Bilateral high‐frequency stimulation of the subthalamic nucleus on attentional performance: transient deleterious effects and enhanced motivation in both intact and parkinsonian rats , 2007, The European journal of neuroscience.

[40]  G Pfurtscheller,et al.  Event-related desynchronization during motor behavior and visual information processing. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

[41]  E. Donchin,et al.  On the dependence of P300 latency on stimulus evaluation processes. , 1984, Psychophysiology.

[42]  P. Hogarth,et al.  Pallidal vs subthalamic nucleus deep brain stimulation in Parkinson disease. , 2005, Archives of neurology.

[43]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. III. Frontal cortex. , 1995, Electroencephalography and clinical neurophysiology.

[44]  D. Friedman,et al.  The novelty P3: an event-related brain potential (ERP) sign of the brain's evaluation of novelty , 2001, Neuroscience & Biobehavioral Reviews.

[45]  R. Knight,et al.  Mechanisms of human attention: event-related potentials and oscillations , 2001, Neuroscience & Biobehavioral Reviews.

[46]  M. Ann The Basal Ganglia and Cognitive Pattern Generators , 2005 .

[47]  J. Mink THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[48]  Timothy Edward John Behrens,et al.  Triangulating a Cognitive Control Network Using Diffusion-Weighted Magnetic Resonance Imaging (MRI) and Functional MRI , 2007, The Journal of Neuroscience.

[49]  V. Mark,et al.  SUBTHALAMIC NUCLEUS AND ITS CONNECTIONS: ANATOMIC SUBSTRATE FOR THE NETWORK EFFECTS OF DEEP BRAIN STIMULATION , 2009, Neurology.

[50]  I. Rektor,et al.  The effect of cortical repetitive transcranial magnetic stimulation on cognitive event-related potentials recorded in the subthalamic nucleus , 2010, Experimental Brain Research.

[51]  J. Polich,et al.  On the relationship between EEG and P300: individual differences, aging, and ultradian rhythms. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[52]  M. Scherg,et al.  Localizing P300 Generators in Visual Target and Distractor Processing: A Combined Event-Related Potential and Functional Magnetic Resonance Imaging Study , 2004, The Journal of Neuroscience.

[53]  J. Polich,et al.  Normative Variation of P3a and P3b from a Large Sample , 2007 .

[54]  Functional disconnection of a prefrontal cortical-dorsal striatal system disrupts choice reaction time performance: implications for attentional function. , 2001 .

[55]  G. Pfurtscheller,et al.  Event-related cortical desynchronization detected by power measurements of scalp EEG. , 1977, Electroencephalography and clinical neurophysiology.

[56]  F. Boiten,et al.  Event-related desynchronization: the effects of energetic and computational demands. , 1992, Electroencephalography and clinical neurophysiology.

[57]  J. Yelnik Functional anatomy of the basal ganglia , 2002, Movement disorders : official journal of the Movement Disorder Society.

[58]  T. Robbins,et al.  Bilateral Lesions of the Subthalamic Nucleus Induce Multiple Deficits in an Attentional Task in Rats , 1997, The European journal of neuroscience.

[59]  R. Poldrack,et al.  Cortical and Subcortical Contributions to Stop Signal Response Inhibition: Role of the Subthalamic Nucleus , 2006, The Journal of Neuroscience.

[60]  Pavel Daniel,et al.  Cognitive‐ and movement‐related potentials recorded in the human basal ganglia , 2005, Movement disorders : official journal of the Movement Disorder Society.

[61]  T. Robbins,et al.  Effects of transient inactivation of the subthalamic nucleus by local muscimol and APV infusions on performance on the five-choice serial reaction time task in rats , 1999, Psychopharmacology.

[62]  E. Courchesne,et al.  Stimulus novelty, task relevance and the visual evoked potential in man. , 1975, Electroencephalography and clinical neurophysiology.

[63]  E. Schröger,et al.  Behavioral and electrophysiological effects of task-irrelevant sound change: a new distraction paradigm. , 1998, Brain research. Cognitive brain research.

[64]  Godfrey Pearlson,et al.  An adaptive reflexive processing model of neurocognitive function: supporting evidence from a large scale (n = 100) fMRI study of an auditory oddball task , 2005, NeuroImage.

[65]  G. Pfurtscheller,et al.  Functional brain imaging based on ERD/ERS , 2001, Vision Research.

[66]  Yasin Temel,et al.  Behavioural changes after bilateral subthalamic stimulation in advanced Parkinson disease: a systematic review. , 2006, Parkinsonism & related disorders.

[67]  T. Robbins,et al.  Enhanced Food-Related Motivation after Bilateral Lesions of the Subthalamic Nucleus , 2002, The Journal of Neuroscience.

[68]  Peter Brown,et al.  Basal ganglia local field potential activity: Character and functional significance in the human , 2005, Clinical Neurophysiology.

[69]  M. Brázdil,et al.  Modifications of cognitive and motor tasks affect the occurrence of event‐related potentials in the human cortex , 2007, The European journal of neuroscience.