Intrinsically regulated learning is modulated by synaptic dopamine signaling
- New York University, United States
- L'Institut d'Investigació Biomèdica de Bellvitge (IDIBELL), Spain
- McGill University, Canada
- Universitat Autònoma de Barcelona, Spain
- Otto-von-Guericke University, Germany
- Sant Pau Institute of Biomedical Research, Spain
Abstract
We recently provided evidence that an intrinsic reward-related signal-triggered by successful learning in absence of any external feedback-modulated the entrance of new information into long-term memory via the activation of the dopaminergic midbrain, hippocampus, and ventral striatum (the SN/VTA-Hippocampal loop; Ripollés et al., 2016). Here, we used a double-blind, within-subject randomized pharmacological intervention to test whether this learning process is indeed dopamine-dependent. A group of healthy individuals completed three behavioural sessions of a language-learning task after the intake of different pharmacological treatments: a dopaminergic precursor, a dopamine receptor antagonist or a placebo. Results show that the pharmacological intervention modulated behavioral measures of both learning and pleasantness, inducing memory benefits after 24 hours only for those participants with a high sensitivity to reward. These results provide causal evidence for a dopamine-dependent mechanism instrumental in intrinsically regulated learning and further suggest that subject-specific reward sensitivity drastically alters learning success.
Data availability
Data is available via Dryad (https://dx.doi.org/10.5061/dryad.g5f7v1j)
-
Data from: Intrinsically regulated learning is modulated by synaptic dopamine signalingAvailable at Dryad Digital Repository under a CC0 Public Domain Dedication.
Article and author information
Author details
Funding
Ministerio de Industria, Economía y Competitividad (PSI2011-29219)
- Antoni Rodriguez-Fornells
Ministerio de Industria, Economía y Competitividad (AP2010-4179)
- Pablo Ripollés
Morelly-Rotary Postdoctoral Fellowship
- Laura Ferreri
Ministerio de Sanidad, Servicios Sociales e Igualdad (CP04/00 121)
- Marta Valle
Deutsche Forschungsgemeinschaft (DFG-SFB-779/A15)
- Toemme Noesselt
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: This study was performed according to local ethics and to the Declaration of Helsinki. It was approved by the Ethics Committee of Hospital Sant Pau and by the Spanish Medicines and Medical Devices Agency (EudraCT 2016-000801-35). All participants gave informed written consent and received compensation for their participation in the study according to Spanish legislation.
Reviewing Editor
- Vishnu Murty, Temple University, United States
Publication history
- Received: May 9, 2018
- Accepted: August 29, 2018
- Accepted Manuscript published: August 30, 2018 (version 1)
- Version of Record published: September 11, 2018 (version 2)
Copyright
© 2018, Ripollés 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
-
- 2,139
- Page views
-
- 288
- Downloads
-
- 16
- 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)
Further reading
-
- Neuroscience
Strong gamma-band oscillations in primate early visual cortex can be induced by homogeneous color surfaces (Peter et al., 2019; Shirhatti and Ray, 2018). Compared to other hues, particularly strong gamma oscillations have been reported for red stimuli. However, precortical color processing and the resultant strength of input to V1 have often not been fully controlled for. Therefore, stronger responses to red might be due to differences in V1 input strength. We presented stimuli that had equal luminance and cone contrast levels in a color coordinate system based on responses of the lateral geniculate nucleus, the main input source for area V1. With these stimuli, we recorded magnetoencephalography in 30 human participants. We found gamma oscillations in early visual cortex which, contrary to previous reports, did not differ between red and green stimuli of equal L-M cone contrast. Notably, blue stimuli with contrast exclusively on the S-cone axis induced very weak gamma responses, as well as smaller event-related fields and poorer change-detection performance. The strength of human color gamma responses for stimuli on the L-M axis could be well explained by L-M cone contrast and did not show a clear red bias when L-M cone contrast was properly equalized.
-
- Neuroscience
Resolving trajectories of axonal pathways in the primate prefrontal cortex remains crucial to gain insights into higher-order processes of cognition and emotion, which requires a comprehensive map of axonal projections linking demarcated subdivisions of prefrontal cortex and the rest of brain. Here, we report a mesoscale excitatory projectome issued from the ventrolateral prefrontal cortex (vlPFC) to the entire macaque brain by using viral-based genetic axonal tracing in tandem with high-throughput serial two-photon tomography, which demonstrated prominent monosynaptic projections to other prefrontal areas, temporal, limbic, and subcortical areas, relatively weak projections to parietal and insular regions but no projections directly to the occipital lobe. In a common 3D space, we quantitatively validated an atlas of diffusion tractography-derived vlPFC connections with correlative green fluorescent protein-labeled axonal tracing, and observed generally good agreement except a major difference in the posterior projections of inferior fronto-occipital fasciculus. These findings raise an intriguing question as to how neural information passes along long-range association fiber bundles in macaque brains, and call for the caution of using diffusion tractography to map the wiring diagram of brain circuits.
