Visuomotor Coordination and Motor Representation by Human Temporal Lobe Neurons

Abstract

The division of cortical visual processing into distinct dorsal and ventral streams is a key concept in primate neuroscience [Goodale, M. A., & Milner, A. D. Separate visual pathways for perception and action. Trends in Neurosciences, 15, 20-25, 1992; Steele, G., Weller, R., & Cusick, C. Cortical connections of the caudal subdivision of the dorsolateral area (V4) in monkeys. Journal of Comparative Neurology, 306, 495-520, 1991]. The ventral stream is usually characterized as a "What" pathway, whereas the dorsal stream is implied in mediating spatial perception ("Where") and visually guided actions ("How"). A subpathway emerging from the dorsal stream and projecting to the medial-temporal lobe has been identified [Kravitz, D. J., Saleem, K. S., Baker, C. I., & Mishkin, M. A new neural framework for visuospatial processing. Nature Reviews Neuroscience, 12, 217-230, 2011; Cavada, C., & Goldman-Raiuc, P. S. Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory cortico-cortical connections. Journal of Comparative Neurology, 287, 393-421, 1989]. The current article studies the coordination of visual information typically associated with the dorsal stream ("Where"), with planned movements, focusing on the temporal lobe. We recorded extracellular activity from 565 cells in the human medial-temporal and frontal lobes while 13 patients performed cued hand movements with visual feedback (visuomotor task), without feedback (motor task), or observed visual feedback without motor movement (visual-only task). We discovered two different neural populations in the human medial-temporal lobe. One consists of motor-like neurons representing hand position, speed or acceleration during the motor task but not during the visuomotor or visual tasks. The other is specific to the parahippocampal gyrus (an area known to process visual motion [Gur, M., & Snodderly, D. M. Direction selectivity in V1 of alert monkeys: Evidence for parallel pathways for motion processing. Journal of Physiology, 585, 383-400, 2007; Sato, N., & Nakamura, K. Visual response properties of neurons in the parahippocampal cortex of monkeys. Journal of Neurophysiology, 90, 876-886, 2003]) and encodes speed, acceleration, or direction of hand movements, but only during the visuomotor task: neither during visual-only nor during motor tasks. These findings suggest a functional basis for the anatomical subpathway between the dorsal stream and the medial-temporal lobe. Similar to the recent expansion of the motor control process into the sensory cortex [Matyas, F., Sreenivasan, V., Marbach, F., Wacongne, C., Barsy, B., Mateo, C., et al. Motor control by sensory cortex. Science, 330, 1240-1243, 2010], our findings render the human medial-temporal lobe an important junction in the process of planning and execution of motor acts whether internally or externally (visually) driven. Thus, the medial-temporal lobe might serve as an integration node between the two processing streams. Our findings thus shed new light on the br...

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