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.
Reviewing Editor
- Laura Colgin, The University of Texas at Austin, United States
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.
Version history
- Received: September 18, 2018
- Accepted: January 30, 2019
- Accepted Manuscript published: February 4, 2019 (version 1)
- Version of Record published: February 26, 2019 (version 2)
- Version of Record updated: March 21, 2019 (version 3)
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
-
- 2,646
- views
-
- 443
- downloads
-
- 66
- 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
Cholecystokinin (CCK) is an essential modulator for neuroplasticity in sensory and emotional domains. Here, we investigated the role of CCK in motor learning using a single pellet reaching task in mice. Mice with a knockout of Cck gene (Cck−/−) or blockade of CCK-B receptor (CCKBR) showed defective motor learning ability; the success rate of retrieving reward remained at the baseline level compared to the wildtype mice with significantly increased success rate. We observed no long-term potentiation upon high-frequency stimulation in the motor cortex of Cck−/− mice, indicating a possible association between motor learning deficiency and neuroplasticity in the motor cortex. In vivo calcium imaging demonstrated that the deficiency of CCK signaling disrupted the refinement of population neuronal activity in the motor cortex during motor skill training. Anatomical tracing revealed direct projections from CCK-expressing neurons in the rhinal cortex to the motor cortex. Inactivation of the CCK neurons in the rhinal cortex that project to the motor cortex bilaterally using chemogenetic methods significantly suppressed motor learning, and intraperitoneal application of CCK4, a tetrapeptide CCK agonist, rescued the motor learning deficits of Cck−/− mice. In summary, our results suggest that CCK, which could be provided from the rhinal cortex, may surpport motor skill learning by modulating neuroplasticity in the motor cortex.
-
- Neuroscience
Probing memory of a complex visual image within a few hundred milliseconds after its disappearance reveals significantly greater fidelity of recall than if the probe is delayed by as little as a second. Classically interpreted, the former taps into a detailed but rapidly decaying visual sensory or ‘iconic’ memory (IM), while the latter relies on capacity-limited but comparatively stable visual working memory (VWM). While iconic decay and VWM capacity have been extensively studied independently, currently no single framework quantitatively accounts for the dynamics of memory fidelity over these time scales. Here, we extend a stationary neural population model of VWM with a temporal dimension, incorporating rapid sensory-driven accumulation of activity encoding each visual feature in memory, and a slower accumulation of internal error that causes memorized features to randomly drift over time. Instead of facilitating read-out from an independent sensory store, an early cue benefits recall by lifting the effective limit on VWM signal strength imposed when multiple items compete for representation, allowing memory for the cued item to be supplemented with information from the decaying sensory trace. Empirical measurements of human recall dynamics validate these predictions while excluding alternative model architectures. A key conclusion is that differences in capacity classically thought to distinguish IM and VWM are in fact contingent upon a single resource-limited WM store.
