Spatial Representations in Local Field Potential Activity of Primate Anterior Intraparietal Cortex (AIP) - PubMed (original) (raw)
Spatial Representations in Local Field Potential Activity of Primate Anterior Intraparietal Cortex (AIP)
Sebastian J Lehmann et al. PLoS One. 2015.
Abstract
The execution of reach-to-grasp movements in order to interact with our environment is an important subset of the human movement repertoire. To coordinate such goal-directed movements, information about the relative spatial position of target and effector (in this case the hand) has to be continuously integrated and processed. Recently, we reported the existence of spatial representations in spiking-activity of the cortical fronto-parietal grasp network (Lehmann & Scherberger 2013), and in particular in the anterior intraparietal cortex (AIP). To further investigate the nature of these spatial representations, we explored in two rhesus monkeys (Macaca mulatta) how different frequency bands of the local field potential (LFP) in AIP are modulated by grip type, target position, and gaze position, during the planning and execution of reach-to-grasp movements. We systematically varied grasp type, spatial target, and gaze position and found that both spatial and grasp information were encoded in a variety of frequency bands (1-13Hz, 13-30Hz, 30-60Hz, and 60-100Hz, respectively). Whereas the representation of grasp type strongly increased towards and during movement execution, spatial information was represented throughout the task. Both spatial and grasp type representations could be readily decoded from all frequency bands. The fact that grasp type and spatial (reach) information was found not only in spiking activity, but also in various LFP frequency bands of AIP, might significantly contribute to the development of LFP-based neural interfaces for the control of upper limb prostheses.
Conflict of interest statement
Competing Interests: The authors have declared that no competing interests exist.
Figures
Fig 1. Behavioral task design.
A. Delayed reach-to-grasp task with the epochs fixation, cue, planning, and movement. Trials were initiated by placing both hands on hand rest sensors and fixating a red LED. After 500-700ms (fixation epoch), the instruction which grip type to use (precision or power grip, indicated by the color of a second LED) and the target position (by illumination) were revealed (cue epoch). After a planning epoch of 800-1200ms, a blink of the fixation LED instructed the monkey to grasp the target in the dark, while maintaining eye fixation. After successful termination, the animal got rewarded with a fixed amount of liquid. B. The target was grasped with either a precision grip (left) or a power grip (right photo). C. Schematic of the reach-to-grasp experimental setup. After placing both hands on the sensors in front of the body (circles), the monkeys had to grasp for the target positioned in front of them. D. Schematic view of the possible spatial variations. Target (T) and gaze positions (e for eye) were systematically varied, resulting in the subtasks CV (combined variation), with target and gaze presented in five joint positions, TV (target variation), with gaze position in the center, and GV (gaze variation), with target position in the center.
Fig 2. LFP spectrograms.
Averaged LFP spectrograms for animal P (A) and animal S (B), normalized to the baseline epoch (prior to fixation onset), and averaged across all recording sites (147 sites in animal P, 99 sites in animal S). Vertical solid lines indicate on- and offset of the fixation, cue, planning, and movement epochs; dashed line indicates movement onset (i.e., hand rest sensor release). Sharp transitions in the slow band are due to the applied multi-taper spectral analysis (time-frequency bandwidth 6.67Hz; see Methods).
Fig 3. Grip type and position tuning of LFP frequency bands.
Percentage of sites tuned (two-way ANOVA, p < 0.05) for the factors grip type (A,C) and position (B,D) for animal P (A,B) and animal S (C,D). Tuning percentages are shown for the slow frequency band (black bars), beta band (dark grey), low gamma band (light grey) and high gamma band (white). Horizontal lines inside bars in A,C indicate fraction of sites tuned for precision (bottom) and power grip (top). Asterisk in Fig 3A indicates preference of 100% for power grip for the beta band during the cue epoch in animal P.
Fig 4. Tuning Onset.
Sliding window analysis (window size 300ms, step size 50ms, two-way ANOVA, p < 0.05) in combined plots for both animals (N = 246 sites) revealed times with significant tuning in the slow frequency band (A), beta band (B), low gamma (C), and high gamma band (D). Horizontal lines indicate time periods with significant tuning for grip type (blue) and position (red), aligned to onset of the planning epoch. Sites are ordered by tuning onset (defined by the appearance of at least five consecutive significant steps). Vertical lines mark the border of the fixation, cue, planning, and movement epoch.
Fig 5. Linear model.
A. Percentage of all LFP sites (both animals, N = 246) that have a significant coefficient for grip type in the various frequency bands (slow, beta, low gamma, and high gamma band) and task epochs B. Percentage of sites with a significant spatial position coefficient. C. White bars indicate percentage of sites with significant spatial coefficients averaged across bands and animals for the different epochs fixation, cue, plan, and movement. Colored lines indicate fraction of sites with spatial coefficients for target (green), gaze (blue), and for both (red). D. Directional tuning of target modulated sites (all bands) for the task epochs fixation, cue, plan, and movement, as revealed by the linear fit. Tuning directions are derived from the target coefficient vectors (green: target modulated; red: target and gaze modulated). E. Directional tuning of gaze modulated sites (blue: gaze modulated; red: target and gaze modulated). F. Scatter plots of spatially tuned sites illustrating angular orientation difference (y-axis) between target (green) and gaze position vectors (blue) against the length contrast (LC) of these vectors (x-axis). Sites with significant target and gaze modulation (red) were considered retinotopic if the coefficient vectors were of comparable length (| LC | < 0.33) and oriented in nearly opposite direction (angular difference < 135deg), as indicated by the black rectangles.
Fig 6. Decoding simulation.
Simulated decoding performance of grip type and spatial factors for different frequency bands (slow: green, beta: red, low gamma: blue, high gamma: cyan, and all bands combined: black curves) and both animals (animal P: A-E, animal S: F-J). Individual panels show the decoding performance for grip type (A, F), the13 different spatial conditions (B,G), as well as for target (C,H), gaze (D,I), and retinotopic target position (E,J) separately for all task epochs. Dashed horizontal lines indicate chance level, and error bars the standard deviation after 100 simulated decoding repetitions.
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