Distributed task-specific processing of somatosensory feedback for voluntary motor control

  1. Mohsen Omrani
  2. Chantelle D Murnaghan
  3. J Andrew Pruszynski
  4. Stephen H Scott  Is a corresponding author
  1. Queen's Univertsity, Canada
  2. Rutgers Biomedical and Health Sciences, United States
  3. University of Western Ontario, Canada
  4. Queen's University, Canada
  5. Queen’s University, Canada
5 figures and 2 tables

Figures

Figure 1 with 1 supplement
Behavioral tasks and perturbation responses across cortical areas.

Each task varied in how the monkeys were instructed to respond to perturbations applied to the limb: correct for the disturbance in the Posture Task (A), not required to respond in the Movie Task (B), move to a spatial target in the IN/OUT Task (C). (D) Perturbation response, in the cell’s preferred torque direction, in the Posture Task of a neuron in A5 and in M1. Tick marks denote action potentials, each row representing a separate trial. (E) Population responses in each cortical area (Mean±2SEM). Arrows depict when population signal surpassed threshold (baseline + 3SD) for >20 ms. Pre-perturbation baseline activity (-100:0 ms pre-perturbation, horizontal insets) in each area is stated below each corresponding population response. Scale bars denote 20 sp/s. Population activity between 60–250 ms (denoted by thick horizontal line) is compressed for visualization purposes. The 'American Pie' picture is reproduced with permission from Universal Studios.

© 1999, Universal Pictures, All Rights Reserved. Figure 1 part B photo (from the film American Pie) is reproduced with permission from Universal Studios.

https://doi.org/10.7554/eLife.13141.003
Figure 1—figure supplement 1
Locations of recorded neurons from each session in Monkey P.

(A5:cyan, S1:green, M1:navy blue, PMd:red) and the locations of the inserted pins (black dots). We applied up to 0.5 mm random jitter on each data point for visualization purposes to avoid multiple sessions obscuring each other.

https://doi.org/10.7554/eLife.13141.004
Response onset across tasks.

(A) Different areas were ranked based on their activity/task onset times across 10000 random iterations of data in each area. Proportion of times each area assumed a rank is plotted for each task. (B) Absolute and (C) cumulative distributions of change in activity across targets (in the IN/OUT task) in each area.

https://doi.org/10.7554/eLife.13141.007
Perturbation responses compared across the Posture and Movie Tasks.

(A) Perturbation response across the Posture (green) and Movie (red) tasks (same neurons as in Figure 1D). (B) Population signal and (C) differential signal across tasks (Posture - Movie) in each cortical area. Each scale bar represents 20 sp/s.

https://doi.org/10.7554/eLife.13141.008
Perturbation responses compared across different target positions.

(A) Perturbation response for the OUT (navy blue) versus IN (cyan) targets (same neurons as in Figure 1D). (B) Population signal and (C) average differential signal across tasks (OUT-IN) in each cortical area. Each scale bar represents 20 sp/s.

https://doi.org/10.7554/eLife.13141.009
Context-dependent patterns across sensorimotor cortex -

Default response (top panel), is represented by activity patterns in the Movie Task. Task engagement (middle panel), is represented by the differential signal between the Movie and Posture Tasks. Target selection (bottom panel), is represented by differential signal between the OUT and IN targets. Activity is plotted using a color map. In the default response, population response is capped at 70 sp/s. Differential signals are normalized to their maximum response in the Posture Task (au).

https://doi.org/10.7554/eLife.13141.010

Tables

Table 1

Number of neurons in each area recorded in each monkey and neurons with significant change in activity (two-sample t-test, p<0.05) in response to perturbation or across tasks.

https://doi.org/10.7554/eLife.13141.005
A5A2S1M1PMd
#cells in Monkey P7004014750
#cells in Monkey X000900
#cells in Monkey A555503569
#cells with significant perturbation response (/recorded neurons) in the Posture Task87/12547/5533/40213/27264/119
#cells with significant perturbation response recorded in both the Posture & Movie Tasks65/8736/4321/26129/16054/100
#cells with significant change in activity between Posture & Movie Tasks (/significant perturbation response)22/654/366/2174/12917/54
#cells with significant reduction in activity in Movie Task (/significant task effect)20/223/45/665/7415/17
#cells with significant perturbation response (/recorded neurons) in the IN-OUT Task35/4121/2518/1883/9258/87
#cells with significant change in activity in the IN/OUT task (/significant perturbation response)9/350/212/1831/8316/58
#cells with significant increase in activity in OUT target (/significant task effect)4/9NA1/224/317/16
Table 2

Neural activity [mean ± SD] in each area, 50-100 ms post perturbation minus baseline, in response to the perturbation and across tasks. sp/s: spikes per second.

https://doi.org/10.7554/eLife.13141.006
A5A2S1M1PMd
Perturbation response30.3 ± 27.4 sp/s38.7 ± 26.1 sp/s68.5 ± 50.1 sp/s43.3 ± 27 sp/s26.9 ± 31.6 sp/s
Differential activity across areas (Movie)11.2 ± 12.8 sp/s5.6 ± 16.9 sp/s8.2 ± 20.8 sp/s14.4 ± 19 sp/s8.3 ± 18.3 sp/s
Change ratio across areas (Movie)36%15%9%36%40%
Differential activity across areas (IN/OUT)-0.3 ± 6.3 sp/s-2.2 ± 10.2 sp/s-1.1 ± 6 sp/s7.4 ± 16.5 sp/s3.2 ± 14.2 sp/s

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  1. Mohsen Omrani
  2. Chantelle D Murnaghan
  3. J Andrew Pruszynski
  4. Stephen H Scott
(2016)
Distributed task-specific processing of somatosensory feedback for voluntary motor control
eLife 5:e13141.
https://doi.org/10.7554/eLife.13141