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Behavioral-state modulation of inhibition is context-dependent and cell type specific in mouse visual cortex
Open accessAbstract
Cortical responses to sensory stimuli are modulated by behavioral state. In the primary visual cortex (V1), visual responses of pyramidal neurons increase during locomotion. This response gain was suggested to be mediated through inhibitory neurons, resulting in the disinhibition of pyramidal neurons. Using in vivo two-photon calcium imaging in layers 2/3 and 4 in mouse V1, we reveal that locomotion increases the activity of vasoactive intestinal peptide (VIP), somatostatin (SST) and parvalbumin (PV)-positive interneurons during visual stimulation, challenging the disinhibition model. In darkness, while most VIP and PV neurons remained locomotion responsive, SST and excitatory neurons were largely non-responsive. Context-dependent locomotion responses were found in each cell type, with the highest proportion among SST neurons. These findings establish that modulation of neuronal activity by locomotion is context-dependent and contest the generality of a disinhibitory circuit for gain control of sensory responses by behavioral state.
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“In the visual cortex, the onset of arousal (as measured by pupil diameter) and locomotion increase neuronal gain32,33,36,37.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [36]
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MethodUltrasensitive fluorescent proteins for imaging neuronal activity
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BackgroundInfluentialCortical inhibitory interneurons control sensory processing
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The Cortical States of Wakefulness
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“Variable effects on the mean Vm and spike rates have been observed for PV and SOM interneurons in V1 (Polack et al., 2013; Fu et al., 2014; Vinck et al., 2015; Pakan et al., 2016; Dipoppa et al., 2018) and Au1 (Schneider et al.”
BackgroundReward Association Enhances Stimulus-Specific Representations in Primary Visual Cortex
Henschke, J. U., Dylda, E., Katsanevaki, D., Dupuy, N., Currie, S. P., Amvrosiadis, T., Pakan, J. M. P., & Rochefort, N. L. (2020) · Current Biology · doi:10.1016/j.cub.2020.03.018 · Cited by 117
“Impact of Locomotion on Experience-Dependent Changes of Stimulus Representation in V1 Because locomotion is known to modulate the gain of visual responses in V1 [21, 24, 27, 33], we assessed whether changes in the proportion of responsive neurons correlated with running behavior.”
BackgroundSelf-citationA disinhibitory circuit motif and flexible information routing in the brain
Wang, X.-J., & Yang, G. R. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.01.002 · Cited by 113
“[21 ,39] reported that, as mice made a transition from rest to movement, SST cells in L2/3 of V1 showed an increase of activity, instead of a previously reported decrease [38].”
Spontaneous behaviors drive multidimensional, brain-wide activityPreprint
Stringer, C., Pachitariu, M., Steinmetz, N. A., Reddy, C. B., Carandini, M., & Harris, K. D. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/306019 · Cited by 123
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“However, modulatory effects of arousal have been found to depend on the experimental context as well as on the sensory modality (Pakan et al., 2016; Shimaoka et al., 2018).”
BackgroundExperience shapes activity dynamics and stimulus coding of VIP inhibitory cells
Garrett, M., Manavi, S., Roll, K., Ollerenshaw, D. R., Groblewski, P. A., Ponvert, N. D., Kiggins, J. T., Casal, L., Mace, K. D., Williford, A., et al. (2020) · eLife · doi:10.7554/elife.50340 · Cited by 103
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BackgroundMethodInhibitory control of correlated intrinsic variability in cortical networks
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Dual-polarity voltage imaging of the concurrent dynamics of multiple neuron types
Kannan, M., Vasan, G., Haziza, S., Huang, C., Chrapkiewicz, R., Luo, J., Cardin, J. A., Schnitzer, M. J., & Pieribone, V. A. (2022) · Science · doi:10.1126/science.abm8797 · Cited by 97
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BackgroundMethodOptimization of interneuron function by direct coupling of cell migration and axonal targeting
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Self-citationBehavioral state modulates the ON visual motion pathway of Drosophila
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MethodMalina, K. C.-K., Tsivourakis, E., Kushinsky, D., Apelblat, D., Shtiglitz, S., Zohar, E., Sokoletsky, M., Tasaka, G., Mizrahi, A., Lampl, I., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.05.001 · Cited by 95
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Self-citationFISSA: A neuropil decontamination toolbox for calcium imaging signals
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Self-citationStructure and function of axo-axonic inhibition
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“The encoding of behaviorally important spatial locations could either occur in the aforementioned cortical and subcortical areas and be transmitted to V1, or encoding could occur in V1 itself since previous studies have shown neuronal responses to running speed (Erisken et al., 2014; Keller et al., 2012; Pakan et al.,…”
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“Subsequent studies have shown that GABAergic neuron modulation depends on the context and magnitude of the visual stimulus and that this disinhibitory circuit model may not be the only way that locomotion can engage interneurons in V1 (Pakan et al., 2016; Dipoppa et al., 2018).”
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“This is in line with the findings that the activity of SST interneurons is 422 modulated by locomotion only in the presence of visual input (Pakan et al., 2016), and that in 423 excitatory neurons, inputs from both excitatory neurons and SST interneurons, but not PV or VIP 424 expressing…”
ResultActivity in primate visual cortex is minimally driven by spontaneous movements
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“Moreover, the activity of both excitatory and inhibitory neurons is modulated by behavioral states, and highly context-dependent (45).”
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“…and examined the underlying cortical and subcortical circuits (Ayaz et al., 2013; Bennett et al., 2013; Polack et al., 2013; Saleem et al., 2013; Fu et al., 2014; Lee et al., 2014; Vinck et al., 2015; Mineault et al., 2016; Pakan et al., 2016; Dadarlat and Stryker, 2017; Dipoppa et al., 2018).”
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“However, the disinhibitory motif failed to explain all neuronal computations when studied under refined behavioral conditions (Pakan et al. 2016).”
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Cell-specific gain modulation by synaptically released zinc in cortical circuits of audition
Anderson, C. T., Kumar, M., Xiong, S., & Tzounopoulos, T. (2017) · eLife · doi:10.7554/elife.29893 · Cited by 50
“…responses from populations of principal excitatory neurons, by utilizing an AAV driven by the calcium/calmodulin-dependent protein kinase 2 (CaMKII) promoter to express GCaMP6f in principal neurons (Figure 2a–c and Figure 2— figure supplement 1a; AAV-CaMKII-GCaMP6f, [Pakan et al., 2016]).”
Reflections of action in sensory cortex
Schneider, D. M. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.02.004 · Cited by 50
Francioni, V., & Harnett, M. T. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.05.038 · Cited by 50
Hayden, D. J., Montgomery, D. P., Cooke, S. F., & Bear, M. F. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0391-21.2021 · Cited by 43
Cortex-wide response mode of VIP-expressing inhibitory neurons by reward and punishment
Szadai, Z., Pi, H.-J., Chevy, Q., Ócsai, K., Albeanu, D. F., Chiovini, B., Szalay, G., Katona, G., Kepecs, Á., & Rózsa, B. J. (2022) · eLife · doi:10.7554/elife.78815 · Cited by 47
Spatial navigation signals in rodent visual cortex
Floßmann, T., & Rochefort, N. L. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.11.004 · Cited by 54
Self-citationHenschke, J. U., & Pakan, J. M. P. (2023) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2023.1165307 · Cited by 58
Self-citationCortical microcircuits as gated-recurrent neural networksPreprint
Costa, R. P., Assael, Y., Shillingford, B., de Freitas, N., & Vogels, T. P. (2017) · arXiv (Cornell University) · doi:10.48550/arxiv.1711.02448 · Cited by 45
“…serve as a platform to discuss and develop ideas of cortical function and to establish links to relevant experimental work on the role of excitatory and inhibitory neurons in contextual learning (Froemke et al., 2007; Froemke, 2015; Poort et al., 2015; Pakan et al., 2016; Kuchibhotla et al., 2017).”
BackgroundThalamus Controls Development and Expression of Arousal States in Visual Cortex
Murata, Y., & Colonnese, M. T. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1519-18.2018 · Cited by 44
“Our results are not consist with a simple model of cortical disinhibition causing movement-associated firing (Fu et al., 2014), but rather a more complex, and stimulusdependent (Pakan et al., 2016; Dipoppa et al., 2018) rebalancing of recurrent and thalamic inputs within the cortical network.”
ResultDadarlat, M. C., Sun, Y. J., & Stryker, M. P. (2023) · Neuron · doi:10.1016/j.neuron.2023.11.022 · Cited by 46
Vasilevskaya, A., Widmer, F. C., Keller, G. B., & Jordan, R. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112096 · Cited by 47
VIP interneurons regulate cortical size tuning and visual perception
Ferguson, K., Salameh, J., Alba, C., Selwyn, H., Barnes, C., Lohani, S., & Cardin, J. A. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113088 · Cited by 40
“7”
Serotonergic modulation across sensory modalities
Sizemore, T. R., Hurley, L. M., & Dacks, A. M. (2020) · Journal of Neurophysiology · doi:10.1152/jn.00034.2020 · Cited by 44
McBride, E. G., Lee, S.-Y. J., & Callaway, E. M. (2019) · Current Biology · doi:10.1016/j.cub.2019.03.065 · Cited by 39
“Perhaps locomotion is simply a more reliable driver of synchronization; locomotion causes increased firing rates in all interneuron subtypes [40, 41], which are thought to be major drivers of oscillatory activity in cortex [42].”
BackgroundProenneke, A., Witte, M., Möck, M., & Staiger, J. F. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz102 · Cited by 50
Hearing in Complex Environments: Auditory Gain Control, Attention, and Hearing Loss
Auerbach, B. D., & Gritton, H. J. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.799787 · Cited by 42
Corticofugal regulation of predictive coding
Lesicko, A. M. H., Angeloni, C. F., Blackwell, J. M., Biasi, M. D., & Geffen, M. N. (2022) · eLife · doi:10.7554/elife.73289 · Cited by 46
Pennartz, C. M. A., Oude Lohuis, M. N., & Olcese, U. (2023) · Philosophical Transactions of the Royal Society B · doi:10.1098/rstb.2022.0336 · Cited by 38
Ramos-Prats, A., Paradiso, E., Castaldi, F., Sadeghi, M., Mir, M. Y., Hörtnagl, H., Göbel, G., & Ferraguti, F. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110893 · Cited by 39
Population activity structure of excitatory and inhibitory neurons
Bittner, S. R., Williamson, R. C., Snyder, A. C., Litwin-Kumar, A., Doiron, B., Chase, S. M., Smith, M. A., & Yu, B. M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0181773 · Cited by 37
Functional flexibility in cortical circuits
Cardin, J. A. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.09.008 · Cited by 37
Antipsychotic drugs selectively decorrelate long-range interactions in deep cortical layers
Heindorf, M., & Keller, G. B. (2023) · eLife · doi:10.1101/2022.01.31.478462 · Cited by 61
Response nonlinearities in networks of spiking neurons
Sanzeni, A., Histed, M. H., & Brunel, N. (2020) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1008165 · Cited by 31
Shaping the Cortical Landscape: Functions and Mechanisms of Top-Down Cortical Feedback Pathways
Zagha, E. (2020) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2020.00033 · Cited by 40
Kumar, M., Xiong, S., Tzounopoulos, T., & Anderson, C. T. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1339-18.2018 · Cited by 33
“The pipette contained ACSF including 100 M ZX1 (Pan et al., 2011; Anderson et al., 2015; an extracellular, high-affinity, fast, zinc-specific chelator) and 50 M Alexa Fluor 594.”
BackgroundLack of Evidence for Stereotypical Direction Columns in the Mouse Superior Colliculus
Chen, H., Savier, E. L., DePiero, V. J., & Cang, J. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1155-20.2020 · Cited by 33
Emerging Mechanisms Underlying Dynamics of GABAergic Synapses
Maffei, A., Charrier, C., Caiati, M. D., Barberis, A., Mahadevan, V., Woodin, M. A., & Tyagarajan, S. K. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1824-17.2017 · Cited by 35
“These patterns of activation also change with context (Pakan et al., 2016), highlighting the flexibility of inhibitory neuron recruitment.”
BackgroundMyers-Joseph, D., Wilmes, K. A., Fernández-Otero, M., Clopath, C., & Khan, A. G. (2023) · Neuron · doi:10.1016/j.neuron.2023.11.006 · Cited by 33
Horrocks, E. A. B., Rodrigues, F. R., & Saleem, A. B. (2024) · Nature Communications · doi:10.1038/s41467-024-50563-y · Cited by 35
Sensory- and Motor-Related Responses of Layer 1 Neurons in the Mouse Visual Cortex
Mesik, L., Huang, J., Zhang, L. I., & Tao, H. W. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1722-19.2019 · Cited by 29
“Locomotion as the primary driver of L1 activity Locomotion has been repeatedly shown to modulate visual responses in V1 and to directly activate multiple types of inhibitory neurons (Niell and Stryker, 2010; Polack et al., 2013; Fu et al., 2014; Mineault et al., 2016; Pakan et al., 2016).”
BackgroundContext value updating and multidimensional neuronal encoding in the retrosplenial cortex
Sun, W., Choi, I., Stoyanov, S., Senkov, O., Ponimaskin, E. G., Winter, Y., Pakan, J. M. P., & Dityatev, A. E. (2021) · Nature Communications · doi:10.1038/s41467-021-26301-z · Cited by 31
Self-citation
Metadata
- Authors
- Pakan, J. M., Lowe, S. C., Dylda, E., Keemink, S. W., Currie, S. P., Coutts, C. A., & Rochefort, N. L.
- Affiliations
- University of Edinburgh (GB)
- University of Freiburg (DE)
- Corresponding author
- Rochefort, Nathalie L
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2016-08-23
- Volume
- 5
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC5030095
- OpenAlex
- W2515318112
- Cited by
- 282
- References
- 43
- Citations by year
- 2026: 12 · 2025: 25 · 2024: 34 · 2023: 47 · 2022: 31 · 2021: 17 · 2020: 29 · 2019: 29 · 2018: 30 · 2017: 26 · 2016: 2
- FWCI
- 18.46
- Type
- journal article
- Language
- en
- Update notices
- correction (2017-09-06)
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
- Funders
- European Commission (Marie Curie Actions (FP7), IEF 624461, EuroSpin Erasmus Mundus Program, Marie Curie Actions (FP7), MC-CIG 631770)
- University Of Edinburgh (Doctoral Training Centre in Neuroinformatics, Graduate School of Life Sciences, Chancellor's fellow starting grant)
- Engineering and Physical Sciences Research Council (Doctoral Training Centre in Neuroinformatics, EP/F500385/1, Doctoral Training Centre in Neuroinformatics, BB/F529254/1)
- Patrick Wild Centre
- The Shirley Foundation
- RS MacDonald Charitable Trust (Seedcorn Grant 21)
- Wellcome Trust (Sir Henry Dale fellowship, 102857/Z/13/Z)
- Royal Society (Sir Henry Dale fellowship, 102857/Z/13/Z)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- primary visual cortex, locomotion, behavioral state, disinhibition, gain control, vasoactive intestinal peptide interneurons, somatostatin interneurons, parvalbumin interneurons, pyramidal neurons, inhibitory interneurons, context-dependent responses
- MeSH terms
- Animals, Behavior, Animal, Interneurons, Locomotion, Models, Neurological, Visual Cortex, Pyramidal Cells, Mice
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