Statistics from Altmetric.com
Studies on primates, and increasing evidences in humans, support the notion that the anterior cingulate cortex, which subserves various executive functions, is involved in the preparation and execution of motor operations.1 Recently, the specific role of the caudal part of the anterior cingulate cortex in manual control has been demonstrated in a patient with a focal anterior cingulate cortex lesion,2 thus providing additional arguments for the functional specialisation of cingulate motor areas in the human brain. Interestingly, the damaged area widely overlapped a more anterior part of Brodmann's area 24 from where complex coordinated movements adapted to environmental constraints have been electrically induced in epileptic patients (figure A).3Both areas encompass dorsally the ventral bank of the cingulate sulcus, at a level that seems to correspond to the simian rostral cingulate motor area (CMAr),1 but whether this region is specifically involved in voluntary movements in humans is not known. We report a finding which shows for the first time that compulsive goal directed motor behaviour can be electrically induced in humans by stimulating the anterior cingulate sulcus.
The patient, a 30 year old right handed woman, had medically intractable epileptic seizures which proved to arise from the right parietal cortex. Before surgery, she underwent intracerebral EEG recordings and stimulation to locate the epileptogenic zone, using 13 stereotactically implanted multilead intracerebral electrodes, three of which investigated the right cingulate cortex. Electrical stimulation at low intensity of the anterior and posterior cingulate gyrus (figure B, electrodes H and V) did not result in any motor reaction. Conversely, using the same parameters, stimulation of the ventral bank of the anterior cingulate sulcus (figure A red dot, and B electrode F) incited the patient to act. It consisted in an irresistible urge to grasp something, resulting in exploratory eye movements scanning both sides of the visual field, and accompanied by a wandering arm movement contralateral to the stimulation side. Then, after the patient had visually localised a potential target, her left hand moved towards the object to grasp it, as if mimicking a spontaneous movement. This irrepressible need started and ended with stimulation, and the patient was unable to control it. Yet, the patient was aware of both her inability to resist and of the movement she thus performed and could describe very precisely. Interestingly, the arm movement seemed visually guided, as when the patient was asked to keep her eyes closed while stimulated, her arm executed a wandering movement which did not result in grasping an object. This was not true if the object location had been memorised before closing her eyes; in that case, the arm moved blindly towards the place where the object was set.
Our finding demonstrates that a cingulate motor area buried in the ventral bank of the cingulate sulcus, just below the presupplementary motor area, is engaged in motor intention in humans, involving the contralateral upper limb. We can assume that the stimulated zone was restricted to the cingulate sulcus, as the stimulation was performed here with a highly localising technique using low intensity in bipolar mode through adjacent contacts distant only by 3.5 mm. This area could be homologous to the simian CMAr, which contains many neurons firing in relation to the intention to move,4 and has essentially an arm representation. In addition, the CMAr lies within the cingulate sulcus anterior to the VCA plane, and then seems embedded in foci of activation seen in humans during relatively simple movements, as well as during more complex manual tasks. It remains that the behavioural response we found involved a high level of motor integration, as previously reported in epileptic patients when stimulating the anterior cingulate gyrus proper,3 but it was preceded in the present case by an “urge to grasp”, which gave rise to a compulsive and adapted manual reaction only when there was visual guidance. The anterior cingulate sulcus has been recently proved in humans to be responsive to visual stimuli,5 and together with our finding, this may suggest that this area plays a part in integrating visual information in execution for movement.