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New Research, Sensory and Motor Systems

Narrow and broad gamma bands process complementary visual information in mouse primary visual cortex

Nicolò Meneghetti, Chiara Cerri, Elena Tantillo, Eleonora Vannini, Matteo Caleo and Alberto Mazzoni
eNeuro 18 October 2021, ENEURO.0106-21.2021; https://doi.org/10.1523/ENEURO.0106-21.2021
Nicolò Meneghetti
1The Biorobotics Institute, Scuola Superiore Sant’Anna, 56025 Pisa, Italy
2Department of Excellence for Robotics and AI, Scuola Superiore Sant’Anna, 56025 Pisa, Italy
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Chiara Cerri
3Neuroscience Institute, National Research Council (CNR), via G. Moruzzi 1, 56124 Pisa, Italy
4Fondazione Umberto Veronesi, Piazza Velasca 5, 20122 Milan, Italy
5Department of Pharmacy, University of Pisa, Via Bonanno Pisano 6, 56126 Pisa, Italy
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Elena Tantillo
3Neuroscience Institute, National Research Council (CNR), via G. Moruzzi 1, 56124 Pisa, Italy
6Fondazione Pisana per la Scienza Onlus (FPS), via Ferruccio Giovannini 13, San Giuliano Terme, 56017 Pisa, Italy
7Scuola Normale Superiore, Piazza dei Cavalieri 7, 56100 Pisa, Italy
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Eleonora Vannini
3Neuroscience Institute, National Research Council (CNR), via G. Moruzzi 1, 56124 Pisa, Italy
4Fondazione Umberto Veronesi, Piazza Velasca 5, 20122 Milan, Italy
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Matteo Caleo
3Neuroscience Institute, National Research Council (CNR), via G. Moruzzi 1, 56124 Pisa, Italy
8Department of Biomedical Sciences, University of Padua, viale G. Colombo 3, 35131 Padua, Italy
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Alberto Mazzoni
1The Biorobotics Institute, Scuola Superiore Sant’Anna, 56025 Pisa, Italy
2Department of Excellence for Robotics and AI, Scuola Superiore Sant’Anna, 56025 Pisa, Italy
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Abstract

Gamma band plays a key role in the encoding of visual features in the primary visual cortex (V1). In rodents V1 two ranges within the gamma band are sensitive to contrast: a broad gamma band (BB) increasing with contrast, and a narrow gamma band (NB), peaking at ⁓60 Hz, decreasing with contrast. The functional roles of the two bands and the neural circuits originating them are not completely clear yet. Here we show, combining experimental and simulated data, that in mice V1 i) BB carries information about high contrast and NB about low contrast; ii) BB modulation depends on excitatory-inhibitory interplay in the cortex, while NB modulation is due to entrainment to the thalamic drive. In awake mice presented with alternating gratings, NB power progressively decreased from low to intermediate levels of contrast where it reached a plateau. Conversely, BB power was constant across low levels of contrast, but it progressively increased from intermediate to high levels of contrast. Furthermore, BB response was stronger immediately after contrast reversal, while the opposite held for NB. These complementary modulations were reproduced by a recurrent excitatory-inhibitory leaky integrate-and-fire network provided that the thalamic inputs were composed of a sustained and a periodic component having complementary sensitivity ranges. These results show that in rodents the thalamic-driven NB plays a specific key role in encoding visual contrast. Moreover, we propose a simple and effective network model of response to visual stimuli in rodents that might help in investigating network dysfunctions of pathological visual information processing.

Significance statement

Gamma oscillations are known to play a relevant and functional role in visual information processing. In the visual cortex of the mice two different frequency bands within this range have been found to display different sensitivity to visual stimuli. Here we help understanding this peculiar phenomenon with two advancements. First, we characterize the response to visual contrast of the two bands, finding them to be complementary both in their temporal activation and in their sensitivity to contrasts. Second, we developed a spiking neurons network model showing that two complementary neural mechanisms originate the two bands. This suggests that these gamma oscillations can be considered as two separate, yet complementary, information channels processing different aspects of the external world.

  • broad gamma band
  • local field potential
  • narrow gamma band
  • spiking neuronal network
  • visual contrast
  • visual cortex

Footnotes

  • Authors report no conflict of interest.

  • This work was supported by the Italian Ministry of Research (MIUR, PRIN2017, PROTECTION, project 20178L7WRS).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Narrow and broad gamma bands process complementary visual information in mouse primary visual cortex
Nicolò Meneghetti, Chiara Cerri, Elena Tantillo, Eleonora Vannini, Matteo Caleo, Alberto Mazzoni
eNeuro 18 October 2021, ENEURO.0106-21.2021; DOI: 10.1523/ENEURO.0106-21.2021

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Narrow and broad gamma bands process complementary visual information in mouse primary visual cortex
Nicolò Meneghetti, Chiara Cerri, Elena Tantillo, Eleonora Vannini, Matteo Caleo, Alberto Mazzoni
eNeuro 18 October 2021, ENEURO.0106-21.2021; DOI: 10.1523/ENEURO.0106-21.2021
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Keywords

  • broad gamma band
  • local field potential
  • narrow gamma band
  • spiking neuronal network
  • visual contrast
  • visual cortex

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