Interference with Performance of a Response Selection Task that has no Working Memory Component: An rTMS Comparison of the Dorsolateral Prefrontal and Medial Frontal Cortex

It has been suggested that the dorsolateral prefrontal cortex (DLPFC) is involved in free selection (FS), the process by which subjects themselves decide what action to perform. Evidence for this proposal has been provided by imaging studies showing activation of the DLPFC when subjects randomly generate responses. However, these response selection tasks have a hidden working memory element and it has been widely reported that the DLPFC is activated when subjects perform tasks which involve working memory. The primary aim of this experiment was to establish if the DLPFC is genuinely involved in response selection. We used repetitive transcranial magnetic stimulation (rTMS) to investigate whether temporary interference of the DLPFC could disrupt performance of a response selection task that had no working memory component. Subjects performed tasks in which they made bimanual sequences of eight nonrepeating finger movements. In the FS task, subjects chose their movements at random while a computer monitor displayed these moves. This visual feedback obviated the need for subjects to maintain their previous moves on-line. No selection was required for the two control tasks as responses were cued by the visual display. The attentional demands of the control tasks varied. In the high load (HL) version, subjects had to maintain their attention throughout the sequence, but this requirement was absent in the low load (LL) task. rTMS over the DLPFC slowed response times on the FS task and at the end of the sequence on the HL task, but had no effect on the LL task. rTMS over the medial frontal cortex (MFC) slowed response times on the FS task but had no effect on the HL task. This suggests that a response selection task without a working memory load will depend on the DLPFC and the MFC. The difference appears to be that the DLPFC is important when selecting between competing responses or when concentrating if there is a high attentional demand, but that the MFC is only important during the response selection task.

[1]  S. Anand,et al.  Transcranial magnetic stimulation: Neurophysiological applications and safety , 2002, Brain and Cognition.

[2]  M. Jahanshahi,et al.  Willed action and its impairments. , 1998, Cognitive neuropsychology.

[3]  M C Ridding,et al.  The effects of transcranial magnetic stimulation over the dorsolateral prefrontal cortex on suppression of habitual counting during random number generation. , 1998, Brain : a journal of neurology.

[4]  Giuseppe Vallar,et al.  Short-Term Forgetting and the Articulatory Loop , 1982 .

[5]  Marjan Jahanshahi,et al.  Transcranial magnetic stimulation studies of cognition: an emerging field , 2000, Experimental Brain Research.

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

[7]  H. E. Rosvold,et al.  Localization of function within the dorsolateral prefrontal cortex of the rhesus monkey. , 1970, Experimental neurology.

[8]  Leslie G. Ungerleider,et al.  Object and spatial visual working memory activate separate neural systems in human cortex. , 1996, Cerebral cortex.

[9]  P. Goldman-Rakic,et al.  Activation of human prefrontal cortex during spatial and nonspatial working memory tasks measured by functional MRI. , 1996, Cerebral cortex.

[10]  Peter L. Strick,et al.  How do the basal ganglia and cerebellum gain access to the cortical motor areas? , 1985, Behavioural Brain Research.

[11]  M Hallett,et al.  Induction of errors in a delayed response task by repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex. , 1994, Neuroreport.

[12]  E. Wassermann.  Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. , 1998, Electroencephalography and clinical neurophysiology.

[13]  R. Dolan,et al.  Active representation of shape and spatial location in man. , 1996, Cerebral cortex.

[14]  Leslie G. Ungerleider,et al.  Discrete Cortical Regions Associated with Knowledge of Color and Knowledge of Action , 1995, Science.

[15]  M. D’Esposito,et al.  Human Prefrontal Cortex Is Not Specific for Working Memory: A Functional MRI Study , 1998, NeuroImage.

[16]  R. Buckner,et al.  Dissociation of human prefrontal cortical areas across different speech production tasks and gender groups. , 1995, Journal of neurophysiology.

[17]  E. Procyk,et al.  Anterior cingulate activity during routine and non-routine sequential behaviors in macaques , 2000, Nature Neuroscience.

[18]  R M Müri,et al.  Effects of single-pulse transcranial magnetic stimulation over the prefrontal and posterior parietal cortices during memory-guided saccades in humans. , 1996, Journal of neurophysiology.

[19]  R. Passingham,et al.  Self-initiated versus externally triggered movements. II. The effect of movement predictability on regional cerebral blood flow. , 2000, Brain : a journal of neurology.

[20]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. I. Frontal cortex and attention to action. , 1997, Journal of neurophysiology.

[21]  M. Jahanshahi,et al.  The left dorsolateral prefrontal cortex and random generation of responses: studies with transcranial magnetic stimulation , 1998, Neuropsychologia.

[22]  L. Goldstein.  The frontal lobes and voluntary action , 1996 .

[23]  M. Raichle,et al.  Localization of a human system for sustained attention by positron emission tomography , 1991, Nature.

[24]  A. Turken,et al.  Response selection in the human anterior cingulate cortex , 1999, Nature Neuroscience.

[25]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[26]  M Hallett,et al.  Stimulation over the human supplementary motor area interferes with the organization of future elements in complex motor sequences. , 1997, Brain : a journal of neurology.

[27]  M. Rushworth,et al.  A primer of magnetic stimulation as a tool for neuropsychology. , 1999, Neuropsychologia.

[28]  Albert Gjedde,et al.  Origin of Human Motor Readiness Field Linked to Left Middle Frontal Gyrus by MEG and PET , 1998, NeuroImage.

[29]  T. Robbins,et al.  Planning and spatial working memory following frontal lobe lesions in man , 1990, Neuropsychologia.

[30]  Iole Indovina,et al.  On Somatotopic Representation Centers for Finger Movements in Human Primary Motor Cortex and Supplementary Motor Area , 2001, NeuroImage.

[31]  R. Passingham,et al.  The prefrontal cortex: response selection or maintenance within working memory? , 2000, 5th IEEE EMBS International Summer School on Biomedical Imaging, 2002..

[32]  R.N.Dej.,et al.  Epilepsy and the Functional Anatomy of the Human Brain , 1954, Neurology.

[33]  S A Spence,et al.  Prefrontal cortex activity in people with schizophrenia and control subjects , 1998, British Journal of Psychiatry.

[34]  G. Rizzolatti,et al.  Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey , 1993, The Journal of comparative neurology.

[35]  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.

[36]  J. B. Preston,et al.  Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe , 1994, The Journal of comparative neurology.

[37]  J. Lewin,et al.  Cortical localization of human sustained attention: detection with functional MR using a visual vigilance paradigm. , 1996, Journal of computer assisted tomography.

[38]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[39]  J. Desmond,et al.  Dissociation of Frontal and Cerebellar Activity in a Cognitive Task: Evidence for a Distinction between Selection and Search , 1998, NeuroImage.