Inhibition of protein synthesis in M1 of monkeys disrupts performance of sequential movements guided by memory

  1. Machiko Ohbayashi  Is a corresponding author
  1. University of Pittsburgh School of Medicine, United States
  2. University of Pittsburgh, United States
4 figures and 1 additional file

Figures

Task and cortical maps for monkey N.

(a, b) Sequences in the Repeating task. (c) Lateral view of cebus brain. Dashed lines indicate the M1-PMd border and the pre-PMd-PMd border. PS: principal sulcus; ArS: arcuate sulcus; CS: central sulcus; IPS: intra parietal sulcus; LS: lateral sulcus; pre-PMd: pre-dorsal premotor cortex; PMd: dorsal premotor cortex; M1: primary motor cortex. R: rostral; L: lateral. (d) MRI image after the chamber implantation for monkey N. The dotted circle indicates the chamber outline. (e) Intracortical stimulation map from monkey N. Letter indicate the movements evoked at each site. S:Shoulder; E: Elbow; W: Wrist; D: Digit. f. Anisomycin solution was injected in the area indicated by a gray oval.

Reaching end points before and after anisomycin injection.

Left: pre-injection; right: post-injection. EA: Accuracy errors; ED: Direction errors; gray dots: correct response; black dots: error response. The anisomycin injection was placed at sites shown in Figure 1f in monkey N. (a) Reaching end points for movement from target 1 to target 5. The monkey was performing sequence 5-3-1 during the Repeating task. (b) Reaching end points for movement from target 2 to target 4. The monkey was performing sequence 1-2-4 during the Repeating task. Percentage of trials ending in each target are given below the targets. Touches between targets were counted as touches to the closest target. *p<0.05.

Effect of anisomycin injection on performance of the task.

(a-c) The performance data for an injection session #2 in monkey N (Figure 1f, Figure 2). (a) Error rate in the Random task. Anisomycin injection did not have any effect on number of errors during the Random task (χ2 test, p=0.385 for move 3–1, df = 1; p=0.639 for move 5–3, df = 1; p=0.624 for move 1–5, df = 1; not significant for move 4–1, df = 1; p=0.957 for move 1–2, df = 1; p=0.371 for move 2–4, df = 1). (b) Error rate in the Repeating task. After the anisomycin injection, the number of errors increased dramatically in 5 of 6 movements in the Repeating task (χ2 test, p<0.001 for moves 5–3, 1–5, 4–1 and 2–4, df = 1; p=0.689 for move 3–1, df = 1; p=0.004 for move 1–2, df = 1). (c) Predictive responses. The percentage of predictive responses decreased significantly after the anisomycin injection (χ2 test, p<0.001 for all movements, df = 1).

Figure 4 with 2 supplements
Population data for anisomycin injections.

(a) Average error rate in the Random task. Anisomycin injections did not have an effect on the number of error responses in the Random task (paired t-test, six injection experiments, p=0.901 for strongest effect, df = 5; p=0.274 for weakest effect, df = 5). (b) Average error rate in the Repeating task. The error rate in the Repeating task increased significantly after the anisomycin injections (paired t-test, six injection experiments, p=0.002 for strongest effect, df = 5; p=0.497 for weakest effect, df = 5). (c) Average predictive responses in the Repeating task. The percentage of predictive responses decreased after anisomycin injections in M1 (paired t-test, p<0.001 for strongest effect, df = 5; p=0.419 for weakest effect, df = 5). *p<0.05.

Figure 4—figure supplement 1
Effect of anisomycin injections for each monkey.

(a, b, c) data from monkey N, a, Average error rate in the Random task. Anisomycin injections did not have a significant effect on performance of the Random task (paired t-test, four injection experiments, p=0.784 for strongest effect, df = 3; p=0.296 for weakest effect, df = 3). (b) Average error rate in the Repeating task. The number of error responses during the Repeating task significantly increased after the anisomycin injections (paired t-test, four injection experiments, p<0.001 for strongest effect, df = 3; p=0.422 for weakest effect, df = 3). (c) Average predictive responses in the Repeating task. The number of predictive responses decreased after anisomycin injections in M1 (paired t-test, p=0.002 for strongest effect, df = 3; p=0.074 for weakest effect, df = 3). *p<0.05. (d, e, f) data from monkey R, d, Error rate in the Random task. Anisomycin injections did not have a significant effect on the performance of the Random task (χ2 test, a movement with ‘strongest effect’: p=0.51; others: 100% correct). (e) Error rate in the Repeating task. The number of error responses during the Repeating task significantly increased after the injections (χ2 test, movements with ‘strongest effect’: p<0.01, p<0.01; movements with ‘weakest effect’: p=0.066, p=0.057). (f) Predictive responses during the Repeating task. (χ2 test, p<0.001 for all movements). *p<0.05.

Figure 4—figure supplement 2
Performance of the Repeating task from 3 days before the injection to 6 days after the injection for monkey N (a–d), monkey R (e, f) and both monkeys (g, h).

Anisomycin was injected at the time points indicated by the arrows. Panels a, c, e, g show percentage of successful trials during the Repeating task for movements on which anisomycin had the strongest effect (mean ± se). Panels b, d, f, h show percentage of predictive trials during the Repeating task for movements on which anisomycin had the strongest effect (mean ± se). In panels c-h, the data after the injection were normalized to the mean of data during 1–3 days before the injections. Anisomycin injection in M1 impaired performance of the Repeating task for 1–2 days after the injection even after the extensive training. The task performance returned to the base line after 1–2 days of training. Asterisks indicate significant differences from baseline (a-b, χ2 test, day 1 and 2: p<0.001; c, paired t-test, day 1, p=0.02; d, paired t-test, day 1, p=0.002; e-f, χ2 test for each injection, day 1, p<0.001; g, paired t-test, day 1, p=0.002; h, paired t-test, day 1, p<0.001). The results were consistent between monkeys.

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  1. Machiko Ohbayashi
(2020)
Inhibition of protein synthesis in M1 of monkeys disrupts performance of sequential movements guided by memory
eLife 9:e53038.
https://doi.org/10.7554/eLife.53038