Cortico‐cortical connectivity of the human mid‐dorsolateral frontal cortex and its modulation by repetitive transcranial magnetic stimulation

Modulation of cortico‐cortical connectivity in specific neural circuits might underlie some of the behavioural effects observed following repetitive transcranial magnetic stimulation (rTMS) of the human frontal cortex. This possibility was tested by applying rTMS to the left mid‐dorsolateral frontal cortex (MDL‐FC) and subsequently measuring functional connectivity of this region with positron emission tomography (PET) and TMS. The results showed a strong rTMS‐related modulation of brain activity in the fronto‐cingulate circuit. These results were confirmed in a parallel experiment in the rat using electrical stimulation and field‐potential recordings. Future studies are needed to provide a direct link between the rTMS‐induced modulation of cortical connectivity and its effects on specific behaviours.

[1]  L. Swanson.  The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[2]  J. Mazziotta,et al.  Reduction of prefrontal cortex glucose metabolism common to three types of depression. , 1989, Archives of general psychiatry.

[3]  P. Goldman-Rakic,et al.  Connections of the ventral granular frontal cortex of macaques with perisylvian premotor and somatosensory areas: Anatomical evidence for somatic representation in primate frontal association cortex , 1989, The Journal of comparative neurology.

[4]  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 .

[5]  Karl J. Friston,et al.  The anatomy of melancholia – focal abnormalities of cerebral blood flow in major depression , 1992, Psychological Medicine.

[6]  H. Barbas,et al.  Architecture and cortical connections of the prefrontal cortex in the rhesus monkey. , 1992, Advances in neurology.

[7]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[8]  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.

[9]  J. Mazziotta,et al.  MRI‐PET Registration with Automated Algorithm , 1993, Journal of computer assisted tomography.

[10]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[11]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[12]  R. Nicoll,et al.  Contrasting properties of two forms of long-term potentiation in the hippocampus , 1995, Nature.

[13]  M Hallett,et al.  Changes in mood and hormone levels after rapid-rate transcranial magnetic stimulation (rTMS) of the prefrontal cortex. , 1996, The Journal of neuropsychiatry and clinical neurosciences.

[14]  Á. Pascual-Leone,et al.  Lateralized effect of rapid-rate transcranial magnetic stimulation of the prefrontal cortex on mood , 1996, Neurology.

[15]  Á. Pascual-Leone,et al.  Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression , 1996, The Lancet.

[16]  M Hallett,et al.  Mood improvement following daily left prefrontal repetitive transcranial magnetic stimulation in patients with depression: a placebo-controlled crossover trial. , 1997, The American journal of psychiatry.

[17]  P. Fox,et al.  Cingulate function in depression: a potential predictor of treatment response , 1997, Neuroreport.

[18]  Peter T. Fox,et al.  Imaging human intra‐cerebral connectivity by PET during TMS , 1997, Neuroreport.

[19]  Alan C. Evans,et al.  Transcranial Magnetic Stimulation during Positron Emission Tomography: A New Method for Studying Connectivity of the Human Cerebral Cortex , 1997, The Journal of Neuroscience.

[20]  M. Raichle,et al.  Subgenual prefrontal cortex abnormalities in mood disorders , 1997, Nature.

[21]  T. Paus.  Imaging the brain before, during, and after transcranial magnetic stimulation , 1998, Neuropsychologia.

[22]  T Paus,et al.  Transcranial magnetic stimulation during PET: Reaching and verifying the target site , 1998, Human brain mapping.

[23]  C. Mathiesen,et al.  Modification of activity‐dependent increases of cerebral blood flow by excitatory synaptic activity and spikes in rat cerebellar cortex , 1998, The Journal of physiology.

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

[25]  B. Jacobs,et al.  Electrical Stimulation of Rat Medial Prefrontal Cortex Enhances Forebrain Serotonin Output: Implications for Electroconvulsive Therapy and Transcranial Magnetic Stimulation in Depression , 1999, Neuropsychopharmacology.

[26]  S. Kosslyn,et al.  The role of area 17 in visual imagery: convergent evidence from PET and rTMS. , 1999, Science.

[27]  E. Klein,et al.  Chronic repetitive transcranial magnetic stimulation alters β-adrenergic and 5-HT2 receptor characteristics in rat brain , 1999, Brain Research.

[28]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[29]  F. Ebner,et al.  Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia. , 1999, Journal of neurophysiology.

[30]  J C Rothwell,et al.  Paired-pulse investigations of short-latency intracortical facilitation using TMS in humans. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[31]  Á. Pascual-Leone,et al.  Applications of transcranial magnetic stimulation in studies on motor learning. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[32]  M. Segal,et al.  Long-Term Effects of Transcranial Magnetic Stimulation on Hippocampal Reactivity to Afferent Stimulation , 1999, The Journal of Neuroscience.

[33]  T. Paus,et al.  Functional connectivity of the anterior cingulate cortex within the human frontal lobe: a brain-mapping meta-analysis , 2000, Experimental Brain Research.

[34]  P. Dannon,et al.  Repetitive transcranial magnetic stimulation is as effective as electroconvulsive therapy in the treatment of nondelusional major depressive disorder: an open study , 2000, Biological Psychiatry.

[35]  T. Paus,et al.  Repetitive Transcranial Magnetic Stimulation of the Human Prefrontal Cortex Induces Dopamine Release in the Caudate Nucleus , 2001, The Journal of Neuroscience.

[36]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[37]  T. Paus.  Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.