publication . Article . 2017

An inhibitory gate for state transition in cortex

Dania Vecchia; Giuseppe Pica; Claudio Moretti; Stefano Varani; Michela Chiappalone; Tommaso Fellin; Serena Bovetti; Manuel Molano-Mazón; Stefano Zucca; Stefano Panzeri; ...
Open Access English
  • Published: 16 May 2017
  • Country: Italy
Abstract
Large scale transitions between active (up) and silent (down) states during quiet wakefulness or NREM sleep regulate fundamental cortical functions and are known to involve both excitatory and inhibitory cells. However, if and how inhibition regulates these activity transitions is unclear. Using fluorescence-targeted electrophysiological recording and cell-specific optogenetic manipulation in both anesthetized and non-anesthetized mice, we found that two major classes of interneurons, the parvalbumin and the somatostatin positive cells, tightly control both up-to-down and down-to-up state transitions. Inhibitory regulation of state transition was observed under ...
Persistent Identifiers
Subjects
free text keywords: Neocortex; mouse; neuroscience; parvalbumin positive interneuron; somatostatin positive interneuron; up and down states; Animals; Cerebral Cortex; Electroencephalography; Interneurons; Mice; Optogenetics; Neural Inhibition; Sleep; Wakefulness, Research Article, Neuroscience, Neocortex, parvalbumin positive interneuron, somatostatin positive interneuron, up and down states, Mouse, oscillations, medicine.anatomical_structure, medicine, Parvalbumin, biology.protein, biology, Anatomy, Neural Inhibition, Inhibitory postsynaptic potential, Excitatory postsynaptic potential, Wakefulness, Electrophysiology, Optogenetics
Funded by
EC| NEURO-PATTERNS
Project
NEURO-PATTERNS
How neuronal activity patterns drive behavior: novel all-optical control and monitoring of brain neuronal networks with high spatiotemporal resolution
  • Funder: European Commission (EC)
  • Project Code: 647725
  • Funding stream: H2020 | ERC | ERC-COG
,
NIH| The role of patterned activity in neuronal codes for behavior
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1U01NS090576-01
  • Funding stream: NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE
,
EC| ETIC
Project
ETIC
Encoding and Transmission of Information in the Mouse Somatosensory Cortex
  • Funder: European Commission (EC)
  • Project Code: 699829
  • Funding stream: H2020 | MSCA-IF-EF-ST
76 references, page 1 of 6

Adesnik, H, Scanziani, M. Lateral competition for cortical space by layer-specific horizontal circuits. Nature. 2010; 464: 1155-1160 [OpenAIRE] [PubMed] [DOI]

Adesnik, H, Bruns, W, Taniguchi, H, Huang, ZJ, Scanziani, M. A neural circuit for spatial summation in visual cortex. Nature. 2012; 490: 226-231 [OpenAIRE] [PubMed] [DOI]

Apicella, AJ, Wickersham, IR, Seung, HS, Shepherd, GM. Laminarly orthogonal excitation of fast-spiking and low-threshold-spiking interneurons in mouse motor cortex. Journal of Neuroscience. 2012; 32: 7021-7033 [OpenAIRE] [PubMed] [DOI]

Aravanis, AM, Wang, LP, Zhang, F, Meltzer, LA, Mogri, MZ, Schneider, MB, Deisseroth, K. An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. Journal of Neural Engineering. 2007; 4: S143-S156 [OpenAIRE] [PubMed] [DOI]

Bazhenov, M, Timofeev, I, Steriade, M, Sejnowski, TJ. Model of thalamocortical slow-wave sleep oscillations and transitions to activated States. Journal of Neuroscience. 2002; 22: 8691-8704 [OpenAIRE] [PubMed]

Beltramo, R, D'Urso, G, Dal Maschio, M, Farisello, P, Bovetti, S, Clovis, Y, Lassi, G, Tucci, V, De Pietri Tonelli, D, Fellin, T, Dal, MM, De Pietri, TD. Layer-specific excitatory circuits differentially control recurrent network dynamics in the neocortex. Nature Neuroscience. 2013; 16: 227-234 [OpenAIRE] [PubMed] [DOI]

Berndt, A, Yizhar, O, Gunaydin, LA, Hegemann, P, Deisseroth, K. Bi-stable neural state switches. Nature Neuroscience. 2009; 12: 229-234 [OpenAIRE] [PubMed] [DOI]

Chen, JY, Chauvette, S, Skorheim, S, Timofeev, I, Bazhenov, M. Interneuron-mediated inhibition synchronizes neuronal activity during slow oscillation. The Journal of Physiology. 2012; 590: 3987-4010 [OpenAIRE] [PubMed] [DOI]

Chen, N, Sugihara, H, Sur, M. An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity. Nature Neuroscience. 2015; 18: 892-902 [OpenAIRE] [PubMed] [DOI]

Chow, BY, Han, X, Dobry, AS, Qian, X, Chuong, AS, Li, M, Henninger, MA, Belfort, GM, Lin, Y, Monahan, PE, Boyden, ES. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature. 2010; 463: 98-102 [OpenAIRE] [PubMed] [DOI]

Civillico, EF, Contreras, D. Spatiotemporal properties of sensory responses in vivo are strongly dependent on network context. Frontiers in Systems Neuroscience. 2012; 6 [OpenAIRE] [PubMed] [DOI]

Compte, A, Sanchez-Vives, MV, McCormick, DA, Wang, XJ. Cellular and network mechanisms of slow oscillatory activity (<1 hz) and wave propagations in a cortical network model. Journal of Neurophysiology. 2003; 89: 2707-2725 [OpenAIRE] [PubMed] [DOI]

Contreras, D, Steriade, M. Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. Journal of Neuroscience. 1995; 15: 604-622 [OpenAIRE] [PubMed]

Crochet, S, Chauvette, S, Boucetta, S, Timofeev, I. Modulation of synaptic transmission in neocortex by network activities. The European Journal of Neuroscience. 2005; 21: 1030-1044 [OpenAIRE] [PubMed] [DOI]

Crochet, S, Petersen, CC. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nature Neuroscience. 2006; 9: 608-610 [OpenAIRE] [PubMed] [DOI]

76 references, page 1 of 6
Related research
Abstract
Large scale transitions between active (up) and silent (down) states during quiet wakefulness or NREM sleep regulate fundamental cortical functions and are known to involve both excitatory and inhibitory cells. However, if and how inhibition regulates these activity transitions is unclear. Using fluorescence-targeted electrophysiological recording and cell-specific optogenetic manipulation in both anesthetized and non-anesthetized mice, we found that two major classes of interneurons, the parvalbumin and the somatostatin positive cells, tightly control both up-to-down and down-to-up state transitions. Inhibitory regulation of state transition was observed under ...
Persistent Identifiers
Subjects
free text keywords: Neocortex; mouse; neuroscience; parvalbumin positive interneuron; somatostatin positive interneuron; up and down states; Animals; Cerebral Cortex; Electroencephalography; Interneurons; Mice; Optogenetics; Neural Inhibition; Sleep; Wakefulness, Research Article, Neuroscience, Neocortex, parvalbumin positive interneuron, somatostatin positive interneuron, up and down states, Mouse, oscillations, medicine.anatomical_structure, medicine, Parvalbumin, biology.protein, biology, Anatomy, Neural Inhibition, Inhibitory postsynaptic potential, Excitatory postsynaptic potential, Wakefulness, Electrophysiology, Optogenetics
Funded by
EC| NEURO-PATTERNS
Project
NEURO-PATTERNS
How neuronal activity patterns drive behavior: novel all-optical control and monitoring of brain neuronal networks with high spatiotemporal resolution
  • Funder: European Commission (EC)
  • Project Code: 647725
  • Funding stream: H2020 | ERC | ERC-COG
,
NIH| The role of patterned activity in neuronal codes for behavior
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1U01NS090576-01
  • Funding stream: NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE
,
EC| ETIC
Project
ETIC
Encoding and Transmission of Information in the Mouse Somatosensory Cortex
  • Funder: European Commission (EC)
  • Project Code: 699829
  • Funding stream: H2020 | MSCA-IF-EF-ST
76 references, page 1 of 6

Adesnik, H, Scanziani, M. Lateral competition for cortical space by layer-specific horizontal circuits. Nature. 2010; 464: 1155-1160 [OpenAIRE] [PubMed] [DOI]

Adesnik, H, Bruns, W, Taniguchi, H, Huang, ZJ, Scanziani, M. A neural circuit for spatial summation in visual cortex. Nature. 2012; 490: 226-231 [OpenAIRE] [PubMed] [DOI]

Apicella, AJ, Wickersham, IR, Seung, HS, Shepherd, GM. Laminarly orthogonal excitation of fast-spiking and low-threshold-spiking interneurons in mouse motor cortex. Journal of Neuroscience. 2012; 32: 7021-7033 [OpenAIRE] [PubMed] [DOI]

Aravanis, AM, Wang, LP, Zhang, F, Meltzer, LA, Mogri, MZ, Schneider, MB, Deisseroth, K. An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. Journal of Neural Engineering. 2007; 4: S143-S156 [OpenAIRE] [PubMed] [DOI]

Bazhenov, M, Timofeev, I, Steriade, M, Sejnowski, TJ. Model of thalamocortical slow-wave sleep oscillations and transitions to activated States. Journal of Neuroscience. 2002; 22: 8691-8704 [OpenAIRE] [PubMed]

Beltramo, R, D'Urso, G, Dal Maschio, M, Farisello, P, Bovetti, S, Clovis, Y, Lassi, G, Tucci, V, De Pietri Tonelli, D, Fellin, T, Dal, MM, De Pietri, TD. Layer-specific excitatory circuits differentially control recurrent network dynamics in the neocortex. Nature Neuroscience. 2013; 16: 227-234 [OpenAIRE] [PubMed] [DOI]

Berndt, A, Yizhar, O, Gunaydin, LA, Hegemann, P, Deisseroth, K. Bi-stable neural state switches. Nature Neuroscience. 2009; 12: 229-234 [OpenAIRE] [PubMed] [DOI]

Chen, JY, Chauvette, S, Skorheim, S, Timofeev, I, Bazhenov, M. Interneuron-mediated inhibition synchronizes neuronal activity during slow oscillation. The Journal of Physiology. 2012; 590: 3987-4010 [OpenAIRE] [PubMed] [DOI]

Chen, N, Sugihara, H, Sur, M. An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity. Nature Neuroscience. 2015; 18: 892-902 [OpenAIRE] [PubMed] [DOI]

Chow, BY, Han, X, Dobry, AS, Qian, X, Chuong, AS, Li, M, Henninger, MA, Belfort, GM, Lin, Y, Monahan, PE, Boyden, ES. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature. 2010; 463: 98-102 [OpenAIRE] [PubMed] [DOI]

Civillico, EF, Contreras, D. Spatiotemporal properties of sensory responses in vivo are strongly dependent on network context. Frontiers in Systems Neuroscience. 2012; 6 [OpenAIRE] [PubMed] [DOI]

Compte, A, Sanchez-Vives, MV, McCormick, DA, Wang, XJ. Cellular and network mechanisms of slow oscillatory activity (<1 hz) and wave propagations in a cortical network model. Journal of Neurophysiology. 2003; 89: 2707-2725 [OpenAIRE] [PubMed] [DOI]

Contreras, D, Steriade, M. Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. Journal of Neuroscience. 1995; 15: 604-622 [OpenAIRE] [PubMed]

Crochet, S, Chauvette, S, Boucetta, S, Timofeev, I. Modulation of synaptic transmission in neocortex by network activities. The European Journal of Neuroscience. 2005; 21: 1030-1044 [OpenAIRE] [PubMed] [DOI]

Crochet, S, Petersen, CC. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nature Neuroscience. 2006; 9: 608-610 [OpenAIRE] [PubMed] [DOI]

76 references, page 1 of 6
Related research
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