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Nelly Amador and Itzhak Fried

Object

The supplementary motor area (SMA) is considered critical in the planning, initiation, and execution of motor acts. Despite decades of research, including electrical stimulation mapping in patients undergoing neurosurgery, the contribution of this region to the generation of motor behavior has remained enigmatic. This is a study of single-neuron responses at various stages of a motor task during depth electrode recording in the SMA, pre-SMA, and medial temporal lobe of humans, with the goal of elucidating the disparate roles of neurons in these regions during movements.

Methods

The patients were undergoing evaluation for epilepsy surgery requiring implantation of intracranial depth electrodes. Single-unit recordings were made during both the execution and mental imagery of finger apposition sequences.

Only medial frontal neurons responded selectively to specific features of the motor plan, such as which hand performed the motor activity or the complexity of the sequence. Neuron activity progressively increased before the patient was given a “go” cue for the execution of movements; this activity peaked earlier in the pre-SMA than in the SMA proper. We observed similar patterns of activation during motor imagery and actual movement, but only neurons in the SMA differentiated between imagined and real movements.

Conclusions

These results provide support at the single-neuron level for the role of the medial frontal cortex in the temporal organization and planning of movements in humans.

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Itzhak Fried, Jung H. Kim, and Dennis D. Spencer

✓ The authors examined hippocampal tissue removed during surgical procedures in 17 patients with intractable epilepsy who were found by preoperative magnetic resonance imaging or computerized tomography to have intra-axial masses in the temporal lobe. Neuronal densities in the cornu ammonis (CA) fields of the hippocampus and in the dentate granule cell layer were measured in hematoxylin and eosin-stained sections and were found to be lower compared to a group of 18 autopsy controls. The neuronal densities in all hippocampal fields except CA2 were related to the patient's age at seizure onset. Patients with an earlier onset of seizures had lower neuronal densities. With the exception of CA4, neuronal densities were not significantly related to the duration of the seizure disorder. Cell counts in all fields except CA2 were also related to the location of the lesion in the temporal lobe. Patients with mesial temporal lesions had lower neuronal counts. These results suggest increased vulnerability of hippocampal cytoarchitecture to proximal lesions with early ictal manifestation.

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Itzhak Fried, Dennis D. Spencer, and Susan S. Spencer

✓ An aura is generally understood to be the beginning of a seizure. Yet, following successful surgery for intractable epilepsy, patients may have persistent auras even though they are otherwise seizure free. Ninety patients with intractable seizures and auras underwent resective surgery. Forty-three patients had hippocampal sclerosis and 47 had temporal or extratemporal lesions such as glial tumors or vascular malformations. The semiology of the auras was found to have value in localization but not lateralization of the pathology. Epigastric auras as well as gustatory and olfactory auras were significantly more frequent in patients with hippocampal sclerosis than in those with temporal or extratemporal lesions. Auras of vertigo or dizziness were most frequent in patients with extratemporal pathology.

There was a significant difference between the pathology groups in the efficacy of resection in eliminating the auras. Of the patients with hippocampal sclerosis who were rendered seizure free, 18.9% had persistent auras, whereas only one (2.6%) of the patients with temporal or extratemporal lesions who were rendered seizure free had persistent auras. These findings suggest that for patients with hippocampal sclerosis an anatomical dissociation between seizure and aura may occur, whereas this dissociation is not present in patients with lesions. Patients suspected of having hippocampal sclerosis should be counseled preoperatively as to the significant likelihood of persistent auras even if seizures are successfully abolished.

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Fani Andelman, Svetlana Kipervasser, Miri Y. Neufeld, Uri Kramer, and Itzhak Fried

Object

Surgery for refractory epilepsy often bestows significant relief but may cause memory impairment. The risk of postoperative memory loss can be determined by the intracarotid amobarbital procedure, or the Wada test. Chemical inactivation of the hemisphere on the side of the lesion is usually performed first, followed by inactivation of the contralateral hemisphere. Patients who demonstrate adequate memory capacity of the contralateral hemisphere following deactivation of the ipsilateral hemisphere are considered good candidates for anterior temporal lobectomy. Evidence for the contribution of deactivating the contralateral healthy hemisphere remains inconclusive.

Methods

The authors analyzed results in 32 patients with intractable epilepsy who had undergone a bilateral Wada test followed by an anterior temporal lobectomy and in whom the findings of both pre- and postsurgical neuropsychological evaluations were available. The Wada memory scores were correlated with the difference in scores between pre- and postsurgical standardized memory test scores.

Conclusions

Analyses revealed no significant relationship between the Wada memory scores in the contralateral hemisphere and postsurgical changes in memory abilities. There was, however, a significant negative correlation between the Wada memory score in the ipsilateral hemisphere and postsurgical memory changes, particularly in patients with right hemisphere epileptogenic lesions (p = 0.0007). The results of this study are discussed vis-à-vis two theories of hippocampal function, and the authors stress the importance of the functional status of the surgical hemisphere in the prediction of postsurgical memory changes.

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Itzhak Fried, Valeriy I. Nenov, Steven G. Ojemann, and Roger P. Woods

✓ Magnetic resonance (MR) imaging has recently been used to demonstrate physiological activation of the human brain. This development is of considerable interest to the neurosurgeon planning procedures near brain regions involving specific functions. In the present study, rolandic and visual cortices were imaged with a conventional 1.5-tesla clinical MR imager using a spoiled gradient-recalled acquisition in the steady state sequence. Two patients, one with a right frontal astrocytoma and the other with a left parietal meningioma, underwent MR imaging of rolandic cortex while performing a repetitive finger apposition task. Two patients with complex partial seizures referable to the temporal and occipital regions underwent MR imaging of visual cortex while exposed to repetitive photic stimulation (8.3 Hz). Significant signal intensity changes up to 15% between the activation and rest conditions were observed near the surgical targets at the expected anatomical location of the rolandic and visual cortices. In two of these cases activation measured by MR was compared and found similar to the activation measured at the same plane by H2 15O positron emission tomography (PET). These results suggest that functional MR and PET techniques can be used to obtain preoperative brain mapping in individual patients considered for neurosurgical procedures.

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Ariel Tankus, Yehezkel Yeshurun, Tamar Flash, and Itzhak Fried

Object

The supplementary motor area (SMA) plays an important role in planning, initiation, and execution of motor acts. Patients with SMA lesions are impaired in various kinematic parameters, such as velocity and duration of movement. However, the relationships between neuronal activity and these parameters in the human brain have not been fully characterized. This is a study of single-neuron activity during a continuous volitional motor task, with the goal of clarifying these relationships for SMA neurons and other frontal lobe regions in humans.

Methods

The participants were 7 patients undergoing evaluation for epilepsy surgery requiring implantation of intracranial depth electrodes. Single-unit recordings were conducted while the patients played a computer game involving movement of a cursor in a simple maze.

Results

In the SMA proper, most of the recorded units exhibited a monotonic relationship between the unit firing rate and hand motion speed. The vast majority of SMA proper units with this property showed an inverse relation, that is, firing rate decrease with speed increase. In addition, most of the SMA proper units were selective to the direction of hand motion. These relationships were far less frequent in the pre-SMA, anterior cingulate gyrus, and orbitofrontal cortex.

Conclusions

The findings suggest that the SMA proper takes part in the control of kinematic parameters of endeffector motion, and thus lend support to the idea of connecting neuroprosthetic devices to the human SMA.

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Ariel Tankus, Anat Mirelman, Nir Giladi, Itzhak Fried, and Jeffrey M. Hausdorff

OBJECTIVE

The ability to modulate the pace of movement is a critical factor in the smooth operation of the motor system. The authors recently described distinct and overlapping representations of movement kinematics in the subthalamic nucleus (STN), but it is still unclear how movement pace is modulated according to the demands of the task at the neuronal level in this area. The goal of this study was to clarify how different movement paces are being controlled by neurons in the STN.

METHODS

The authors performed direct recording of the electrical activity of single neurons in the STN of neurosurgical patients with Parkinson’s disease undergoing implantation of a deep brain stimulator under local anesthesia while the patients performed repetitive foot and hand movements intraoperatively at multiple paces.

RESULTS

A change was observed in the neuronal population controlling the movement for each pace. The mechanism for switching between these controlling populations differs for hand and foot movements.

CONCLUSIONS

These findings suggest that disparate schemes are utilized in the STN for neuronal recruitment for motor control of the upper and lower extremities. The results indicate a distributed model of motor control within the STN, where the active neuronal population changes when modifying the task condition and pace.

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Arne Ekstrom, Nanthia Suthana, Eric Behnke, B.S.E., Noriko Salamon, Susan Bookheimer, and Itzhak Fried

✓Localization and targeting of depth electrodes in specific regions of the human brain is critical for accurate clinical diagnoses and treatment as well as for neuroscientific electrophysiological research. By using high-resolution magnetic resonance imaging combined with 2D computational unfolding, the authors present a method that improves electrode localization in the medial temporal lobe. This method permits visualization of electrode placements in subregions of the hippocampus and parahippocampal gyrus, allowing for greater specificity in relating electrophysiological and anatomical features in the human medial temporal lobe. Such methods may be extended to therapeutic procedures targeting specific neuronal circuitry in subfields of structures deep in the human brain.