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      Four concurrent feedforward and feedback networks with different roles in the visual cortical hierarchy

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      Journal: PLoS Biology
      Publisher: Public Library of Science

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          Abstract

          Visual stimuli evoke fast-evolving activity patterns that are distributed across multiple cortical areas. These areas are hierarchically structured, as indicated by their anatomical projections, but how large-scale feedforward and feedback streams are functionally organized in this system remains an important missing clue to understanding cortical processing. By analyzing visual evoked responses in laminar recordings from 6 cortical areas in awake mice, we uncovered a dominant feedforward network with scale-free interactions in the time domain. In addition, we established the simultaneous presence of a gamma band feedforward and 2 low frequency feedback networks, each with a distinct laminar functional connectivity profile, frequency spectrum, temporal dynamics, and functional hierarchy. We could identify distinct roles for each of these 4 processing streams, by leveraging stimulus contrast effects, analyzing receptive field (RF) convergency along functional interactions, and determining relationships to spiking activity. Our results support a dynamic dual counterstream view of hierarchical processing and provide new insight into how separate functional streams can simultaneously and dynamically support visual processes.

          Abstract

          Visual stimuli evoke fast-evolving activity patterns that are distributed across multiple cortical areas, but how large-scale feedforward and feedback streams are functionally organized in this system remains unclear. Visual evoked responses in laminar recordings from six cortical areas in awake mice reveal how layers and rhythms dynamically orchestrate functional streams in vision.

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          Most cited references75

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          Investigating Causal Relations by Econometric Models and Cross-spectral Methods

          C. W. J. Granger (1969)
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            The origin of extracellular fields and currents--EEG, ECoG, LFP and spikes.

            György Buzsáki, Costas Anastassiou, Christof Koch (2012)
            Neuronal activity in the brain gives rise to transmembrane currents that can be measured in the extracellular medium. Although the major contributor of the extracellular signal is the synaptic transmembrane current, other sources--including Na(+) and Ca(2+) spikes, ionic fluxes through voltage- and ligand-gated channels, and intrinsic membrane oscillations--can substantially shape the extracellular field. High-density recordings of field activity in animals and subdural grid recordings in humans, combined with recently developed data processing tools and computational modelling, can provide insight into the cooperative behaviour of neurons, their average synaptic input and their spiking output, and can increase our understanding of how these processes contribute to the extracellular signal.
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              Fully integrated silicon probes for high-density recording of neural activity

              Matteo Carandini, James Jun, Nicholas Steinmetz … (2017)
              Sensory, motor and cognitive operations involve the coordinated action of large neuronal populations across multiple brain regions in both superficial and deep structures. Existing extracellular probes record neural activity with excellent spatial and temporal (sub-millisecond) resolution, but from only a few dozen neurons per shank. Optical Ca2+ imaging offers more coverage but lacks the temporal resolution needed to distinguish individual spikes reliably and does not measure local field potentials. Until now, no technology compatible with use in unrestrained animals has combined high spatiotemporal resolution with large volume coverage. Here we design, fabricate and test a new silicon probe known as Neuropixels to meet this need. Each probe has 384 recording channels that can programmably address 960 complementary metal–oxide–semiconductor (CMOS) processing-compatible low-impedance TiN sites that tile a single 10-mm long, 70 × 20-μm cross-section shank. The 6 × 9-mm probe base is fabricated with the shank on a single chip. Voltage signals are filtered, amplified, multiplexed and digitized on the base, allowing the direct transmission of noise-free digital data from the probe. The combination of dense recording sites and high channel count yielded well-isolated spiking activity from hundreds of neurons per probe implanted in mice and rats. Using two probes, more than 700 well-isolated single neurons were recorded simultaneously from five brain structures in an awake mouse. The fully integrated functionality and small size of Neuropixels probes allowed large populations of neurons from several brain structures to be recorded in freely moving animals. This combination of high-performance electrode technology and scalable chip fabrication methods opens a path towards recording of brain-wide neural activity during behaviour.
              Article 0 comments Cited 638 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Elham Barzegaran:
                ORCID: https://orcid.org/0000-0001-9337-2134
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – original draft
                Gijs Plomp: Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Christopher Pack: Role: Academic Editor
                Journal
                Journal ID (nlm-ta): PLoS Biol
                Journal ID (iso-abbrev): PLoS Biol
                Journal ID (publisher-id): plos
                Title: PLoS Biology
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Print): 1544-9173
                ISSN (Electronic): 1545-7885
                Publication date (Electronic): 10 February 2022
                Publication date Collection: February 2022
                Publication date PMC-release: 10 February 2022
                Volume: 20
                Issue: 2
                Electronic Location Identifier: e3001534
                Affiliations
                [001] Perceptual Networks Group, Department of Psychology, University of Fribourg, Fribourg, Switzerland
                McGill University, CANADA
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0001-9337-2134
                Article
                Publisher ID: PBIOLOGY-D-21-00633
                DOI: 10.1371/journal.pbio.3001534
                PMC ID: 8865670
                PubMed ID: 35143472
                SO-VID: 7c4adcf5-8bd3-4d9e-8a49-4f5a73241d31
                Copyright © © 2022 Barzegaran, Plomp
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 5 March 2021
                Date accepted : 10 January 2022
                Page count
                Figures: 6, Tables: 1, Pages: 22
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001711, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung;
                Award ID: PP00P1_157420
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001711, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung;
                Award ID: PP00P1_183714
                Award Recipient :
                This research was supported by the Swiss National Science Foundation (grants PP00P1_157420, GP and PP00P1_183714, GP). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Computer and Information Sciences
                Subject: Network Analysis
                Subject: Scale-Free Networks
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Cognitive Science
                Subject: Cognitive Psychology
                Subject: Perception
                Subject: Sensory Perception
                Subject: Vision
                Subject: Biology and Life Sciences
                Subject: Psychology
                Subject: Cognitive Psychology
                Subject: Perception
                Subject: Sensory Perception
                Subject: Vision
                Subject: Social Sciences
                Subject: Psychology
                Subject: Cognitive Psychology
                Subject: Perception
                Subject: Sensory Perception
                Subject: Vision
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Sensory Perception
                Subject: Vision
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Brain
                Subject: Visual Cortex
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Brain
                Subject: Visual Cortex
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Mammals
                Subject: Primates
                Subject: Biology and Life Sciences
                Subject: Zoology
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Mammals
                Subject: Primates
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Mammals
                Subject: Rodents
                Subject: Mice
                Subject: Biology and Life Sciences
                Subject: Zoology
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Mammals
                Subject: Rodents
                Subject: Mice
                Subject: Computer and Information Sciences
                Subject: Neural Networks
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Neural Networks
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Cognitive Science
                Subject: Cognitive Psychology
                Subject: Perception
                Subject: Sensory Perception
                Subject: Biology and Life Sciences
                Subject: Psychology
                Subject: Cognitive Psychology
                Subject: Perception
                Subject: Sensory Perception
                Subject: Social Sciences
                Subject: Psychology
                Subject: Cognitive Psychology
                Subject: Perception
                Subject: Sensory Perception
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Sensory Perception
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Cognitive Science
                Custom metadata
                PLOS Publication Stage vor-update-to-uncorrected-proof
                Publication Update 2022-02-23
                Data Availability The data used in this work are publicly available recordings from the Visual Coding - Neuropixels dataset, provided by the Allen Institute for Brain Science. The LFPs, Spike-sorted data and metadata can be accessed via: https://allensdk.readthedocs.io/en/latest/visual_coding_neuropixels.html. The underlying data for figures are available at https://osf.io/pqf7z/.

                ScienceOpen disciplines: Life sciences
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                ScienceOpen disciplines: Life sciences

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