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
-
- 2,774
- views
-
- 453
- downloads
-
- 88
- 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
When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.
-
- Neuroscience
Cerebellar dysfunction leads to postural instability. Recent work in freely moving rodents has transformed investigations of cerebellar contributions to posture. However, the combined complexity of terrestrial locomotion and the rodent cerebellum motivate new approaches to perturb cerebellar function in simpler vertebrates. Here, we adapted a validated chemogenetic tool (TRPV1/capsaicin) to describe the role of Purkinje cells — the output neurons of the cerebellar cortex — as larval zebrafish swam freely in depth. We achieved both bidirectional control (activation and ablation) of Purkinje cells while performing quantitative high-throughput assessment of posture and locomotion. Activation modified postural control in the pitch (nose-up/nose-down) axis. Similarly, ablations disrupted pitch-axis posture and fin-body coordination responsible for climbs. Postural disruption was more widespread in older larvae, offering a window into emergent roles for the developing cerebellum in the control of posture. Finally, we found that activity in Purkinje cells could individually and collectively encode tilt direction, a key feature of postural control neurons. Our findings delineate an expected role for the cerebellum in postural control and vestibular sensation in larval zebrafish, establishing the validity of TRPV1/capsaicin-mediated perturbations in a simple, genetically tractable vertebrate. Moreover, by comparing the contributions of Purkinje cell ablations to posture in time, we uncover signatures of emerging cerebellar control of posture across early development. This work takes a major step towards understanding an ancestral role of the cerebellum in regulating postural maturation.
