Neuronal representation of saccadic error in macaque posterior parietal cortex
- Beijing Normal University, China
- The First Affiliated Hospital of Zhengzhou University, China
Abstract
Motor control, motor learning, self-recognition, and spatial perception all critically depend on the comparison of motor intention to the actually executed movement. Despite our knowledge that the brainstem-cerebellum plays an important role in motor error detection and motor learning, the involvement of neocortex remains largely unclear. Here, we report the neuronal computation and representation of saccadic error in macaque posterior parietal cortex (PPC). Neurons with persistent pre- and post-saccadic response (PPS) represent the intended end-position of saccade; neurons with late post-saccadic response (LPS) represent the actual end-position of saccade. Remarkably, after the arrival of the LPS signal, the PPS neurons' activity becomes highly correlated with the discrepancy between intended and actual end-position, and with the probability of making secondary (corrective) saccades. Thus, this neuronal computation might underlie the formation of saccadic error signals in PPC for speeding up saccadic learning and leading the occurrence of secondary saccade.
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Author details
Reviewing Editor
- Wolfram Schultz, University of Cambridge, United Kingdom
Ethics
Animal experimentation: Two male rhesus monkeys (6-8 kg, 6-7 years old) were involved in the present study. They were housed in separate cages in a large room with 12 hours light/dark cycle. The horizontal and vertical eye positions signals were recorded using the scleral eye coil technique (Crist Instrument Sclera), and data were sampled at 1 kHz. Before training, each monkey was surgically implanted with a head post and two eye coils. After training in three oculomotor tasks, a recording chamber was implanted above the posterior parietal cortex of the right hemisphere for chronic electrophysiological recording. All experimental and surgical procedures were standard and approved by the Animal Care Committee of Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences (Project number ER-SIBS-221112P); Animal Care and Ethics Committee of Beijing Normal University. (Project number IACUC (BNU) - NKLCNL 2013-09)
Version history
- Received: August 16, 2015
- Accepted: April 18, 2016
- Accepted Manuscript published: April 20, 2016 (version 1)
- Version of Record published: May 12, 2016 (version 2)
Copyright
© 2016, Zhou et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Neuronal representation of saccadic error in macaque posterior parietal cortex
eLife 5:e10912.
https://doi.org/10.7554/eLife.10912
Further reading
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- Medicine
- Neuroscience
Background:
Ketamine has emerged as one of the most promising therapies for treatment-resistant depression. However, inter-individual variability in response to ketamine is still not well understood and it is unclear how ketamine’s molecular mechanisms connect to its neural and behavioral effects.
Methods:
We conducted a single-blind placebo-controlled study, with participants blinded to their treatment condition. 40 healthy participants received acute ketamine (initial bolus 0.23 mg/kg, continuous infusion 0.58 mg/kg/hr). We quantified resting-state functional connectivity via data-driven global brain connectivity and related it to individual ketamine-induced symptom variation and cortical gene expression targets.
Results:
We found that: (i) both the neural and behavioral effects of acute ketamine are multi-dimensional, reflecting robust inter-individual variability; (ii) ketamine’s data-driven principal neural gradient effect matched somatostatin (SST) and parvalbumin (PVALB) cortical gene expression patterns in humans, while the mean effect did not; and (iii) behavioral data-driven individual symptom variation mapped onto distinct neural gradients of ketamine, which were resolvable at the single-subject level.
Conclusions:
These results highlight the importance of considering individual behavioral and neural variation in response to ketamine. They also have implications for the development of individually precise pharmacological biomarkers for treatment selection in psychiatry.
Funding:
This study was supported by NIH grants DP5OD012109-01 (A.A.), 1U01MH121766 (A.A.), R01MH112746 (J.D.M.), 5R01MH112189 (A.A.), 5R01MH108590 (A.A.), NIAAA grant 2P50AA012870-11 (A.A.); NSF NeuroNex grant 2015276 (J.D.M.); Brain and Behavior Research Foundation Young Investigator Award (A.A.); SFARI Pilot Award (J.D.M., A.A.); Heffter Research Institute (Grant No. 1–190420) (FXV, KHP); Swiss Neuromatrix Foundation (Grant No. 2016–0111) (FXV, KHP); Swiss National Science Foundation under the framework of Neuron Cofund (Grant No. 01EW1908) (KHP); Usona Institute (2015 – 2056) (FXV).
Clinical trial number:
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- Neuroscience
Storing and accessing memories is required to successfully perform day-to-day tasks, for example for engaging in a meaningful conversation. Previous studies in both rodents and primates have correlated hippocampal cellular activity with behavioral expression of memory. A key role has been attributed to awake hippocampal replay – a sequential reactivation of neurons representing a trajectory through space. However, it is unclear if awake replay impacts immediate future behavior, gradually creates and stabilizes long-term memories over a long period of time (hours and longer), or enables the temporary memorization of relevant events at an intermediate time scale (seconds to minutes). In this study, we aimed to address the uncertainty around the timeframe of impact of awake replay by collecting causal evidence from behaving rats. We detected and disrupted sharp wave ripples (SWRs) - signatures of putative replay events - using electrical stimulation of the ventral hippocampal commissure in rats that were trained on three different spatial memory tasks. In each task, rats were required to memorize a new set of locations in each trial or each daily session. Interestingly, the rats performed equally well with or without SWR disruptions. These data suggest that awake SWRs - and potentially replay - does not affect the immediate behavior nor the temporary memorization of relevant events at a short timescale that are required to successfully perform the spatial tasks. Based on these results, we hypothesize that the impact of awake replay on memory and behavior is long-term and cumulative over time.
