An electrophysiological link between the cerebellum, cognition and emotion: Frontal theta EEG activity to single-pulse cerebellar TMS

Early intracranial electrical stimulation studies in animals demonstrated cerebellar connectivity to brain structures involved in cognitive and emotive functions. Human electrophysiological data to support cerebellum involvement in the latter functions are however lacking. In the present study, electrophysiological responses were recorded to single-pulse transcranial magnetic stimulation (TMS) over the vermis in healthy human volunteers. Increased theta activity was observed after single-pulse vermis TMS as compared to sham and occipital TMS. Both animal and human research relate theta activity with the septo-hippocampal complex, an important brain structure involved in cognition and emotion. The present electrophysiological study supports the earlier intracranial electrical stimulation findings by demonstrating cerebellar involvement in the modulation of the core frequencies related to cognitive and emotive aspects of human behavior.

[1]  Yasushi Mizuki,et al.  Appearance of Frontal Midline Theta Activity in Patients with Generalized Anxiety Disorder , 2000, Neuropsychobiology.

[2]  M. Molliver,et al.  Organizational principles and microcircuitry of the cerebellum , 2001 .

[3]  J. Panksepp.  Affective Neuroscience: The Foundations of Human and Animal Emotions , 1998 .

[4]  Alan C. Evans,et al.  Three-Dimensional MRI Atlas of the Human Cerebellum in Proportional Stereotaxic Space , 1999, NeuroImage.

[5]  Eric A. Zilli,et al.  Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior , 2005, Hippocampus.

[6]  R. Heath,et al.  Ascending projections of the cerebellar fastigial nucleus to the hippocampus, amygdala, and other temporal lobe sites: evoked potential and histological studies in monkeys and cats. , 1974, Experimental neurology.

[7]  Marjolein P. M. Kammers,et al.  A case of illusory own-body perceptions after transcranial magnetic stimulation of the cerebellum , 2008, The Cerebellum.

[8]  J. Schmahmann.  The role of the cerebellum in affect and psychosis , 2000, Journal of Neurolinguistics.

[9]  J. W. Papez.  A PROPOSED MECHANISM OF EMOTION , 1937 .

[10]  G. V. Prisco,et al.  Theta-rhythmically firing neurons in the anterior thalamus: implications for mnemonic functions of Papez’s circuit , 2001, Neuroscience.

[11]  D. Schutter,et al.  Increased positive emotional memory after repetitive transcranial magnetic stimulation over the orbitofrontal cortex. , 2006, Journal of psychiatry & neuroscience : JPN.

[12]  E H de Haan,et al.  Effects of slow rTMS at the right dorsolateral prefrontal cortex on EEG asymmetry and mood , 2001, Neuroreport.

[13]  John Rothwell,et al.  Effects of low frequency and low intensity repetitive paired pulse stimulation of the primary motor cortex , 2004, Clinical Neurophysiology.

[14]  C. Caltagirone,et al.  Interference of Left and Right Cerebellar rTMS with Procedural Learning , 2004, Journal of Cognitive Neuroscience.

[15]  Mary-Frances O'Connor,et al.  Functional neuroanatomy of grief: an FMRI study. , 2003, The American journal of psychiatry.

[16]  J. Gotman,et al.  The EEG in deep midline lesions , 1981, Neurology.

[17]  E. Basar.  Memory as the "whole brain work": a large-scale model based on "oscillations in super-synergy". , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[18]  Jaak Panksepp,et al.  High frequency repetitive transcranial magnetic over the medial cerebellum induces a shift in the prefrontal electroencephalography gamma spectrum: a pilot study in humans , 2003, Neuroscience Letters.

[19]  N. McNaughton,et al.  Comparison between the behavioural effects of septal and hippocampal lesions: A review , 1983, Neuroscience & Biobehavioral Reviews.

[20]  Y. Mizuki,et al.  Differential effects of noradrenergic drugs on anxiety and arousal in healthy volunteers with high and low anxiety , 1996, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[21]  R. J. Ilmoniemi,et al.  Prefrontal transcranial magnetic stimulation produces intensity-dependent EEG responses in humans , 2005, NeuroImage.

[22]  J. Leon Kenemans,et al.  Electrophysiological correlates of cortico-subcortical interaction: A cross-frequency spectral EEG analysis , 2006, Clinical Neurophysiology.

[23]  Alvaro Pascual-Leone,et al.  Increased variability of paced finger tapping accuracy following repetitive magnetic stimulation of the cerebellum in humans , 2001, Neuroscience Letters.

[24]  L. Aftanas,et al.  Human anterior and frontal midline theta and lower alpha reflect emotionally positive state and internalized attention: high-resolution EEG investigation of meditation , 2001, Neuroscience Letters.

[25]  Risto J. Ilmoniemi,et al.  Prefrontal TMS produces smaller EEG responses than motor-cortex TMS: implications for rTMS treatment in depression , 2005, Psychopharmacology.

[26]  Arnaud Delorme,et al.  Frontal midline EEG dynamics during working memory , 2005, NeuroImage.

[27]  Nick F. Ramsey,et al.  A stereotactic method for image-guided transcranial magnetic stimulation validated with fMRI and motor-evoked potentials , 2004, NeuroImage.

[28]  B. Christensen,et al.  Reduced cerebellar inhibition in schizophrenia: a preliminary study. , 2005, The American journal of psychiatry.

[29]  Robert F. Simons,et al.  Anxiety and error-related brain activity , 2003, Biological Psychology.

[30]  J. Schmahmann,et al.  Rediscovery of an early concept. , 1997, International review of neurobiology.

[31]  R. Snider,et al.  Cerebellar contributions to the papez circuit , 1976, Journal of neuroscience research.

[32]  J. Gray,et al.  Anxiolytic action on the behavioural inhibition system implies multiple types of arousal contribute to anxiety. , 2000, Journal of affective disorders.

[33]  Charles M Epstein,et al.  Iron-Core Coils for Transcranial Magnetic Stimulation , 2002, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[34]  Robert Chen,et al.  Suppression of the motor cortex by magnetic stimulation of the cerebellum , 2001, Experimental Brain Research.

[35]  Jan Smid,et al.  Theta activity in neurons and networks of the amygdala related to long‐term fear memory , 2005, Hippocampus.

[36]  R. Ilmoniemi,et al.  Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity , 1997, Neuroreport.

[37]  Dennis J. L. G. Schutter,et al.  The cerebellum on the rise in human emotion , 2008, The Cerebellum.

[38]  L. Aftanas,et al.  Trait anxiety impact on posterior activation asymmetries at rest and during evoked negative emotions: EEG investigation. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[39]  R. Heath,et al.  Cerebellar stimulation: effects on septal region, hippocampus, and amygdala of cats and rats. , 1978, Biological psychiatry.

[40]  Hans-Christian Pape,et al.  Amygdalar and Hippocampal Theta Rhythm Synchronization During Fear Memory Retrieval , 2003, Science.

[41]  K. Inanaga,et al.  Frontal midline theta rhythm and mental activity , 1998, Psychiatry and Clinical Neurosciences.

[42]  P. Strick,et al.  Cerebellar Projections to the Prefrontal Cortex of the Primate , 2001, The Journal of Neuroscience.

[43]  Robert Chen,et al.  Exploring the connectivity between the cerebellum and motor cortex in humans , 2004, The Journal of physiology.

[44]  Heath Rg.  Fastigial nucleus connections to the septal region in monkey and cat: a demonstration with evoked potentials of a bilateral pathway. , 1973 .

[45]  Seppo Kähkönen,et al.  The effect of stimulus intensity on brain responses evoked by transcranial magnetic stimulation , 2004, Human brain mapping.

[46]  James L. McGaugh,et al.  Mechanisms of emotional arousal and lasting declarative memory , 1998, Trends in Neurosciences.

[47]  R. Borisyuk,et al.  A model of theta rhythm production in the septal‐hippocampal system and its modulation by ascending brain stem pathways , 2000, Hippocampus.

[48]  D. Tucker,et al.  Electrophysiological Responses to Errors and Feedback in the Process of Action Regulation , 2003, Psychological science.

[49]  Risto J. Ilmoniemi,et al.  Distinct differences in cortical reactivity of motor and prefrontal cortices to magnetic stimulation , 2004, Clinical Neurophysiology.

[50]  R. Heath.  Modulation of emotion with a brain pacemamer. Treatment for intractable psychiatric illness. , 1977, The Journal of nervous and mental disease.