Surface color and predictability determine contextual modulation of V1 firing and gamma oscillations
- Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany
- Max Planck Institute for Brain Research, Germany
Abstract
The integration of direct bottom-up inputs with contextual information is a core feature of neocortical circuits. In area V1, neurons may reduce their firing rates when their receptive field input can be predicted by spatial context. Gamma-synchronized (30-80Hz) firing may provide a complementary signal to rates, reflecting stronger synchronization between neuronal populations receiving mutually predictable inputs. We show that large uniform surfaces, which have high spatial predictability, strongly suppressed firing yet induced prominent gamma-synchronization in macaque V1, particularly when they were colored. Yet, chromatic mismatches between center and surround, breaking predictability, strongly reduced gamma-synchronization while increasing firing rates. Differences between responses to different colors, including strong gamma-responses to red, arose from stimulus adaptation to a full-screen background, suggesting prominent differences in adaptation between M- and L-cone signaling pathways. Thus, synchrony signaled whether RF inputs were predicted from spatial context, while firing rates increased when stimuli were unpredicted from context.
Data availability
As described in the Methods section, several datasets were acquired in this study. Datasets have been uploaded onto Dryad (https://doi.org/10.5061/dryad.4809qj4). Thse include individual sessions with each session preprocessed (downsampled, see Methods), epoched into trials with time, channel and condition information.
-
Data from: Surface color and predictability determine contextual modulation of macaque V1 firing and gamma oscillationsDryad Digital Repository, doi:10.5061/dryad.4809qj4.
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft (SPP 1665)
- Pascal Fries
European Commission (FP7-604102-HBP)
- Pascal Fries
Deutsche Forschungsgemeinschaft (FOR 1847)
- Pascal Fries
Deutsche Forschungsgemeinschaft (FR2557/5-1-CORNET)
- Pascal Fries
Deutsche Forschungsgemeinschaft (FR2557/6-1-NeuroTMR)
- Pascal Fries
Deutsche Forschungsgemeinschaft (Reinhart Kosselleck grant)
- Wolf Singer
National Institutes of Health (1U54MH091657-WU-Minn- Consortium-HCP)
- Pascal Fries
European Science Foundation (European Young Investigator Award)
- Pascal Fries
LOEWE (NeFF)
- Pascal Fries
European Commission (HEALTH-F2-2008-200728-BrainSynch)
- Pascal Fries
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All procedures complied with the German and European regulations for the protection of animals and were approved by the regional authority (Regierungspräsidium Darmstadt, F-149-1000/1005). All surgeries were performed under anesthesia and were followed by analgesic treatment post-operatively.
Copyright
© 2019, Peter 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
-
- 2,757
- views
-
- 453
- downloads
-
- 87
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
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)
Surface color and predictability determine contextual modulation of V1 firing and gamma oscillations
eLife 8:e42101.
https://doi.org/10.7554/eLife.42101
Further reading
-
- Neuroscience
Active inference integrates perception, decision-making, and learning into a united theoretical framework, providing an efficient way to trade off exploration and exploitation by minimizing (expected) free energy. In this study, we asked how the brain represents values and uncertainties (novelty and variability), and resolves these uncertainties under the active inference framework in the exploration-exploitation trade-off. Twenty-five participants performed a contextual two-armed bandit task, with electroencephalogram (EEG) recordings. By comparing the model evidence for active inference and reinforcement learning models of choice behavior, we show that active inference better explains human decision-making under novelty and variability, which entails exploration or information seeking. The EEG sensor-level results show that the activity in the frontal, central, and parietal regions is associated with novelty, while the activity in the frontal and central brain regions is associated with variability. The EEG source-level results indicate that the expected free energy is encoded in the frontal pole and middle frontal gyrus and uncertainties are encoded in different brain regions but with overlap. Our study dissociates the expected free energy and uncertainties in active inference theory and their neural correlates, speaking to the construct validity of active inference in characterizing cognitive processes of human decisions. It provides behavioral and neural evidence of active inference in decision processes and insights into the neural mechanism of human decisions under uncertainties.
-
- Genetics and Genomics
- Neuroscience
The mammalian suprachiasmatic nucleus (SCN), situated in the ventral hypothalamus, directs daily cellular and physiological rhythms across the body. The SCN clockwork is a self-sustaining transcriptional-translational feedback loop (TTFL) that in turn coordinates the expression of clock-controlled genes (CCGs) directing circadian programmes of SCN cellular activity. In the mouse, the transcription factor, ZFHX3 (zinc finger homeobox-3), is necessary for the development of the SCN and influences circadian behaviour in the adult. The molecular mechanisms by which ZFHX3 affects the SCN at transcriptomic and genomic levels are, however, poorly defined. Here, we used chromatin immunoprecipitation sequencing to map the genomic localization of ZFHX3-binding sites in SCN chromatin. To test for function, we then conducted comprehensive RNA sequencing at six distinct times-of-day to compare the SCN transcriptional profiles of control and ZFHX3-conditional null mutants. We show that the genome-wide occupancy of ZFHX3 occurs predominantly around gene transcription start sites, co-localizing with known histone modifications, and preferentially partnering with clock transcription factors (CLOCK, BMAL1) to regulate clock gene(s) transcription. Correspondingly, we show that the conditional loss of ZFHX3 in the adult has a dramatic effect on the SCN transcriptome, including changes in the levels of transcripts encoding elements of numerous neuropeptide neurotransmitter systems while attenuating the daily oscillation of the clock TF Bmal1. Furthermore, various TTFL genes and CCGs exhibited altered circadian expression profiles, consistent with an advanced in daily behavioural rhythms under 12 h light–12 h dark conditions. Together, these findings reveal the extensive genome-wide regulation mediated by ZFHX3 in the central clock that orchestrates daily timekeeping in mammals.
