The interrelationship between movement and cognition: Theta rhythm and the P300 event‐related potential

The relationship among brain electrophysiological activity, motor activity, and cognition has been a matter of great interest. For example, it has been discussed whether hippocampal theta rhythm reflects motor activity or cognitive activity, whereas it is widely accepted that the P300 event‐related potential (ERP) reflects cognitive processes such as updating working memory. Here, we investigated the interrelationships among motor activity, hippocampal theta rhythm, and hippocampal P300 ERP using electrophysiological and behavioral data recorded from rats performing an auditory discrimination task (i.e., the auditory oddball paradigm) in a chamber with and without a running‐wheel. We found that the hippocampal theta rhythm generated during locomotion codes information about self‐motion, and event‐related increases in hippocampal theta rhythm observed when rats performed the auditory discrimination cognitive task reflect a change in motor behavior after learning the cognitive task. Interestingly, the hippocampal P300 ERP occurred coincidently with increases in the power and frequency of hippocampal theta rhythm. In addition, we found that changes in theta rhythm observed during spontaneous wheel running without performing a cognitive task as well as when performing the cognitive task are associated with changes in delta‐ and gamma‐band EEG activities. These major findings are discussed with respect to current hypotheses regarding P300 ERP and theta‐, delta‐, and gamma‐band EEG activities in brain functions. © 2010 Wiley‐Liss, Inc.

[1]  F. Carver,et al.  Human Hippocampal and Parahippocampal Theta during Goal-Directed Spatial Navigation Predicts Performance on a Virtual Morris Water Maze , 2008, The Journal of Neuroscience.

[2]  Juliana Yordanova,et al.  On the relation of movement-related potentials to the go/no-go effect on P3 , 2006, Biological Psychology.

[3]  Apostolos P Georgopoulos,et al.  Neural aspects of cognitive motor control , 2000, Current Opinion in Neurobiology.

[4]  René Hen,et al.  Serotonin1A receptor acts during development to establish normal anxiety-like behaviour in the adult , 2002, Nature.

[5]  John Rohrbaugh,et al.  Delta and Theta Oscillations as Risk Markers in Adolescent Offspring of Alcoholics , 2006 .

[6]  André A Fenton,et al.  Is the hippocampal theta rhythm related to cognition in a non‐locomotor place recognition task? , 2005, Hippocampus.

[7]  M. Jeannerod.  Neural Simulation of Action: A Unifying Mechanism for Motor Cognition , 2001, NeuroImage.

[8]  D. Wolpert,et al.  Abnormalities in the awareness and control of action. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[9]  E. Basar,et al.  A compound P300-40 Hz response of the cat hippocampus. , 1991, The International journal of neuroscience.

[10]  T. Shinba,et al.  Event-related potentials in the dorsal hippocampus of rats during an auditory discrimination paradigm. , 1996, Electroencephalography and clinical neurophysiology.

[11]  A. Labarga,et al.  Gamma band activity in an auditory oddball paradigm studied with the wavelet transform , 2001, Clinical Neurophysiology.

[12]  J. Yordanova,et al.  Single-sweep analysis of the theta frequency band during an auditory oddball task. , 1998, Psychophysiology.

[13]  R. Passingham.  The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[14]  S. Kasicki,et al.  The frequency of rat's hippocampal theta rhythm is related to the speed of locomotion , 1998, Brain Research.

[15]  E. Donchin.  Presidential address, 1980. Surprise!...Surprise? , 1981, Psychophysiology.

[16]  Passive rotation‐induced theta rhythm and orientation homeostasis response , 2010, Synapse.

[17]  T. Sejnowski,et al.  Analysis and visualization of single‐trial event‐related potentials , 2001, Human brain mapping.

[18]  Christian G Bien,et al.  Two P300 generators in the hippocampal formation , 2009, Hippocampus.

[19]  L STAN LEUNG,et al.  Generation of Theta and Gamma Rhythms in the Hippocampus , 1998, Neuroscience & Biobehavioral Reviews.

[20]  R. Barry,et al.  Movement-related potentials in the Go/NoGo task: The P3 reflects both cognitive and motor inhibition , 2008, Clinical Neurophysiology.

[21]  E. Basar.  EEG-brain dynamics: Relation between EEG and Brain evoked potentials , 1980 .

[22]  J. O’Keefe,et al.  Grid cells and theta as oscillatory interference: Electrophysiological data from freely moving rats , 2008, Hippocampus.

[23]  R. Knight.  Contribution of human hippocampal region to novelty detection , 1996, Nature.

[24]  E. Basar,et al.  A compound P300-40 Hz response of the cat hippocampus. , 1991 .

[25]  P. Cooke.  Presidential address 1980. , 1980, The Hospital and health services review.

[26]  R. Hayashi,et al.  Relationship between cognitive impairments, event-related potentials, and motor disability scores in patients with Parkinson's disease: 2-year follow-up study , 1996, Journal of the Neurological Sciences.

[27]  O. Vinogradova.  Expression, control, and probable functional significance of the neuronal theta-rhythm , 1995, Progress in Neurobiology.

[28]  J. Polich.  Clinical application of the P300 event-related brain potential. , 2004, Physical medicine and rehabilitation clinics of North America.

[29]  J. Karhu,et al.  Theta oscillations index human hippocampal activation during a working memory task. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  M J Brammer,et al.  A functional study of auditory verbal imagery , 2001, Psychological Medicine.

[31]  Jonghan Shin,et al.  A single trial analysis of hippocampal theta frequency during nonsteady wheel running in rats , 2001, Brain Research.

[32]  E. Donchin,et al.  Is the P300 component a manifestation of context updating? , 1988, Behavioral and Brain Sciences.

[33]  B. H. Bland,et al.  Theta band oscillation and synchrony in the hippocampal formation and associated structures: the case for its role in sensorimotor integration , 2001, Behavioural Brain Research.

[34]  C. H. Vanderwolf,et al.  Hippocampal electrical activity and voluntary movement in the rat. , 1969, Electroencephalography and clinical neurophysiology.

[35]  N Aydin,et al.  The use of the wavelet transform to describe embolic signals. , 1999, Ultrasound in medicine & biology.

[36]  A. Kok.  Overlap between P300 and movement-related-potentials: A response to Verleger , 1988, Biological Psychology.

[37]  B. H. Bland.  The physiology and pharmacology of hippocampal formation theta rhythms , 1986, Progress in Neurobiology.

[38]  E. Basar,et al.  P300-response: possible psychophysiological correlates in delta and theta frequency channels. A review. , 1992, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[39]  Xue-li Sun,et al.  Findings of P300-like and CNV-like potentials in rat model of depression following repeatedly forced swim stress. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[40]  Jonghan Shin,et al.  A unifying theory on the relationship between spike trains, EEG, and ERP based on the noise shaping/predictive neural coding hypothesis. , 2002, Bio Systems.

[41]  G. Buzsáki.  Theta Oscillations in the Hippocampus , 2002, Neuron.

[42]  M. McCabe.  Presidential address. , 1970, Irish nurses' journal.

[43]  Hee-Sup Shin,et al.  Genetic dissection of theta rhythm heterogeneity in mice. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Dr. Robert Miller.  Cortico-Hippocampal Interplay and the Representation of Contexts in the Brain , 1991, Studies of Brain Function.

[45]  C. Ehlers,et al.  Long latency event-related potentials in mice: effects of stimulus characteristics and strain , 2002, Brain Research.

[46]  Hee-Sup Shin,et al.  Phospholipase C β4 in the Medial Septum Controls Cholinergic Theta Oscillations and Anxiety Behaviors , 2009, The Journal of Neuroscience.