Distinct mechanisms mediate speed-accuracy adjustments in cortico-subthalamic networks
- University of Oxford, United Kingdom
- Kings College London, United Kingdom
- University College London Institute of Neurology, United Kingdom
Abstract
Optimal decision-making requires balancing fast but error-prone and more accurate but slower decisions through adjustments of decision thresholds. Here, we demonstrate two distinct correlates of such speed-accuracy adjustments by recording subthalamic nucleus (STN) activity and electroencephalography in eleven Parkinson’s disease patients during a perceptual decision-making task; STN low-frequency oscillatory (LFO) activity (2-8 Hz), coupled to activity at prefrontal electrode Fz, and STN beta activity (13-30 Hz) coupled to electrodes C3/C4 close to motor cortex. These two correlates not only differed in their cortical topography and spectral characteristics, but also in the relative timing of recruitment and in their precise relationship with decision thresholds. Increases of STN LFO power preceding the response predicted increased thresholds only after accuracy instructions, while cue-induced reductions of STN beta power decreased thresholds irrespective of instructions. These findings indicate that distinct neural mechanisms determine whether a decision will be made in haste or with caution.
Data availability
-
Neural correlates of speed-accuracy adjustments in the subthalamic nucleusPublicly available at Oxford University Research Archive (uuid: 09bef38c-999f-4fb7-aa46-14eda3123571).
Article and author information
Author details
Funding
Medical Research Council (MC_UU_12024/1)
- Peter Brown
Horizon 2020 Framework Programme (655605)
- Damian M Herz
Parkinson Appeal UK
- Thomas Foltynie
- Patricia Limousin
- Ludvic Zrinzo
Monument Trust
- Thomas Foltynie
- Patricia Limousin
- Ludvic Zrinzo
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: In accordance with the declaration of Helsinki, participants gave written informed consent to participate in the study, which was approved by the local ethics committee (Oxfordshire REC A).
Reviewing Editor
- Peter Lakatos, NYU, United States
Publication history
- Received: September 13, 2016
- Accepted: January 15, 2017
- Accepted Manuscript published: January 31, 2017 (version 1)
- Version of Record published: February 1, 2017 (version 2)
Copyright
© 2017, Herz 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.
Metrics
-
- 2,640
- Page views
-
- 632
- Downloads
-
- 47
- Citations
Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Distinct mechanisms mediate speed-accuracy adjustments in cortico-subthalamic networks
eLife 6:e21481.
https://doi.org/10.7554/eLife.21481
Further reading
-
- Computational and Systems Biology
- Neuroscience
The locus coeruleus (LC) houses the vast majority of noradrenergic neurons in the brain and regulates many fundamental functions including fight and flight response, attention control, and sleep/wake cycles. While efferent projections of the LC have been extensively investigated, little is known about its local circuit organization. Here, we performed large-scale multi-patch recordings of noradrenergic neurons in adult mouse LC to profile their morpho-electric properties while simultaneously examining their interactions. LC noradrenergic neurons are diverse and could be classified into two major morpho-electric types. While fast excitatory synaptic transmission among LC noradrenergic neurons was not observed in our preparation, these mature LC neurons connected via gap junction at a rate similar to their early developmental stage and comparable to other brain regions. Most electrical connections form between dendrites and are restricted to narrowly spaced pairs or small clusters of neurons of the same type. In addition, more than two electrically coupled cell pairs were often identified across a cohort of neurons from individual multi-cell recording sets that followed a chain-like organizational pattern. The assembly of LC noradrenergic neurons thus follows a spatial and cell type-specific wiring principle that may be imposed by a unique chain-like rule.
-
- Neuroscience
Every decision that we make involves a conflict between exploiting our current knowledge of an action's value or exploring alternative courses of action that might lead to a better, or worse outcome. The sub-cortical nuclei that make up the basal ganglia have been proposed as a neural circuit that may contribute to resolving this explore-exploit 'dilemma'. To test this hypothesis, we examined the effects of neuromodulating the basal ganglia's output nucleus, the globus pallidus interna, in patients who had undergone deep brain stimulation (DBS) for isolated dystonia. Neuromodulation enhanced the number of exploratory choices to the lower value option in a 2-armed bandit probabilistic reversal-learning task. Enhanced exploration was explained by a reduction in the rate of evidence accumulation (drift rate) in a reinforcement learning drift diffusion model. We estimated the functional connectivity profile between the stimulating DBS electrode and the rest of the brain using a normative functional connectome derived from heathy controls. Variation in the extent of neuromodulation induced exploration between patients was associated with functional connectivity from the stimulation electrode site to a distributed brain functional network. We conclude that the basal ganglia's output nucleus, the globus pallidus interna, can adaptively modify decision choice when faced with the dilemma to explore or exploit.
