The effects of transcranial magnetic stimulation over the dorsolateral prefrontal cortex on suppression of habitual counting during random number generation.

Random number generation is an attention-demanding task that engages working memory and executive processes. Random number generation requires holding information 'on line', suppression of habitual counting, internally driven response generation and monitoring of responses. Evidence from PET studies suggests that the dorsolateral prefrontal cortex (DLPFC) is involved in the generation of random responses. We examined the effects of short trains of transcranial magnetic stimulation (TMS) over the left or right DLPFC or medial frontal cortex on random number generation in healthy normal participants. As in previous evidence, in control trials without stimulation participants performed poorly on the random number generation task, showing repetition avoidance and a tendency to count. Brief disruption of processing with TMS over the left DLPFC changed the balance of the individuals' counting bias, increasing the most habitual counting in ones and reducing the lower probability response of counting in twos. This differential effect of TMS over the left DLPFC on the balance of the subject's counting bias was not obtained with TMS over the right DLPFC or the medial frontal cortex. The results suggest that, with disruption of the left DLPFC with TMS, habitual counting in ones that has previously been suppressed is released from inhibition. From these findings a network modulation model of random number generation is proposed, whereby suppression of habitual responses is achieved through the modulatory influence of the left DLPFC over a number-associative network in the superior temporal cortex. To allow emergence of appropriate random responses, the left DLPFC inhibits the superior temporal cortex to prevent spreading activation and habitual counting in ones.

[1]  Karl J. Friston,et al.  Willed action and the prefrontal cortex in man: a study with PET , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  V. Amassian,et al.  Suppression of visual perception by magnetic coil stimulation of human occipital cortex. , 1989, Electroencephalography and clinical neurophysiology.

[3]  Theodore P. Hill,et al.  Random-Number Guessing and the First Digit Phenomenon , 1988 .

[4]  M. Ridding,et al.  Rapid rate transcranial magnetic stimulation--a safety study. , 1997, Electroencephalography and clinical neurophysiology.

[5]  S. Wiegersma A control theory of sequential response production , 1982 .

[6]  M. Hallett,et al.  Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. , 1994, Brain : a journal of neurology.

[7]  Excitatory and inhibitory effects of magnetic coil stimulation of human cortex. , 1990, Electroencephalography and clinical neurophysiology. Supplement.

[8]  N. Ginsburg,et al.  Random Generation: Analysis of the Responses , 1994 .

[9]  D. Norman,et al.  Attention to Action: Willed and Automatic Control of Behavior Technical Report No. 8006. , 1980 .

[10]  F. J. Evans,et al.  Random number generation, psychopathology and therapeutic change. , 1982, Archives of general psychiatry.

[11]  R. G Brown,et al.  Executive processes in Parkinsons disease—random number generation and response suppression , 1998, Neuropsychologia.

[12]  Mark Hallett,et al.  Locating the Motor Cortex on the MRI with Transcranial Magnetic Stimulation and PET , 1996, NeuroImage.

[13]  F. J. Evans,et al.  Subjective random number generation and attention deployment during acquisition and overlearning of a motor skill , 1980 .

[14]  G. Goldenberg,et al.  Components of Random Generation by Normal Subjects and Patients with Dysexecutive Syndrome , 1993, Brain and Cognition.

[15]  S. Wiegersma,et al.  Can repetition avoidance in randomization be explained by randomness concepts? , 1982 .

[16]  P. Brugger,et al.  Random number generation in dementia of the Alzheimer type: A test of frontal executive functions , 1996, Neuropsychologia.

[17]  Julien Clinton Sprott Numerical Recipes Routines and Examples in BASIC , 1991 .

[18]  Alan C. Evans,et al.  Functional activation of the human frontal cortex during the performance of verbal working memory tasks. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Karl J. Friston,et al.  Patterns of Cerebral Blood Flow in Schizophrenia , 1992, British Journal of Psychiatry.

[20]  Allan Collins,et al.  A spreading-activation theory of semantic processing , 1975 .

[21]  Karl J. Friston,et al.  Regional cerebral blood flow in depression measured by positron emission tomography: the relationship with clinical dimensions , 1993, Psychological Medicine.

[22]  E. Perret The left frontal lobe of man and the suppression of habitual responses in verbal categorical behaviour. , 1974, Neuropsychologia.

[23]  G. Bower,et al.  Human Associative Memory , 1973 .

[24]  J. Stroop Studies of interference in serial verbal reactions. , 1992 .

[25]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[26]  S. Heywood The Popular Number Seven or Number Preference , 1972 .

[27]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[28]  E. D. Haan,et al.  Random generation deficit in alcoholic Korsakoff patients , 1995, Neuropsychologia.

[29]  F Duval,et al.  Random number generation by normal, alcoholic and schizophrenic subjects , 1990, Psychological Medicine.

[30]  Richard S. J. Frackowiak,et al.  Impaired mesial frontal and putamen activation in Parkinson's disease: A positron emission tomography study , 1992, Annals of neurology.

[31]  J Valls-Solé,et al.  Safety of rapid-rate transcranial magnetic stimulation in normal volunteers. , 1993, Electroencephalography and clinical neurophysiology.

[32]  V. Amassian,et al.  Matching focal and non-focal magnetic coil stimulation to properties of human nervous system: mapping motor unit fields in motor cortex contrasted with altering sequential digit movements by premotor-SMA stimulation. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

[33]  Karl J. Friston,et al.  Investigating a network model of word generation with positron emission tomography , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  H. S. Yavuz The Production of Random Letters Sequences in Schizophrenics , 1963 .

[35]  R. Hazlewood,et al.  The effects of Parkinson's disease on the capacity to generate information randomly , 1996, Neuropsychologia.

[36]  T. Shallice From Neuropsychology to Mental Structure: Converging Operations: Specific Syndromes and Evidence from Normal Subjects , 1988 .

[37]  B L Day,et al.  Delay in the execution of voluntary movement by electrical or magnetic brain stimulation in intact man. Evidence for the storage of motor programs in the brain. , 1989, Brain : a journal of neurology.