Section: Neuroscience
Topic:
Neuroscience,
Genetics/Genomics
Functional correlates of immediate early gene expression in mouse visual cortex
Corresponding author(s): Keller, Georg B. (georg.keller@fmi.ch)
10.24072/pcjournal.156 - Peer Community Journal, Volume 2 (2022), article no. e45.
Get full text PDF Peer reviewed and recommended by PCIDuring visual development, response properties of layer 2/3 neurons in visual cortex are shaped by experience. Both visual and visuomotor experience are necessary to coordinate the integration of bottom-up visual input and top-down motor-related input. Whether visual and visuomotor experience engage different plasticity mechanisms, possibly associated with the two separate input pathways, is still unclear. To begin addressing this, we measured the expression level of three different immediate early genes (IEG) (c-fos, egr1 or Arc) and neuronal activity in layer 2/3 neurons of visual cortex before and after a mouse’s first visual exposure in life, and subsequent visuomotor learning. We found that expression levels of all three IEGs correlated positively with neuronal activity, but that first visual and first visuomotor exposure resulted in differential changes in IEG expression patterns. In addition, IEG expression levels differed depending on whether neurons exhibited primarily visually driven or motor-related activity. Neurons with strong motor-related activity preferentially expressed EGR1, while neurons that developed strong visually driven activity preferentially expressed Arc. Our findings are consistent with the interpretation that bottom-up visual input and top-down motor-related input are associated with different IEG expression patterns and hence possibly also with different plasticity pathways.
Type: Research article
Mahringer, David 1, 2; Zmarz, Pawel 1, 2, 3; Okuno, Hiroyuki 4; Bito, Haruhiko 5; Keller, Georg B. 1, 2
@article{10_24072_pcjournal_156, author = {Mahringer, David and Zmarz, Pawel and Okuno, Hiroyuki and Bito, Haruhiko and Keller, Georg B.}, title = {Functional correlates of immediate early gene expression in mouse visual cortex}, journal = {Peer Community Journal}, eid = {e45}, publisher = {Peer Community In}, volume = {2}, year = {2022}, doi = {10.24072/pcjournal.156}, url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.156/} }
TY - JOUR AU - Mahringer, David AU - Zmarz, Pawel AU - Okuno, Hiroyuki AU - Bito, Haruhiko AU - Keller, Georg B. TI - Functional correlates of immediate early gene expression in mouse visual cortex JO - Peer Community Journal PY - 2022 VL - 2 PB - Peer Community In UR - https://peercommunityjournal.org/articles/10.24072/pcjournal.156/ DO - 10.24072/pcjournal.156 ID - 10_24072_pcjournal_156 ER -
%0 Journal Article %A Mahringer, David %A Zmarz, Pawel %A Okuno, Hiroyuki %A Bito, Haruhiko %A Keller, Georg B. %T Functional correlates of immediate early gene expression in mouse visual cortex %J Peer Community Journal %D 2022 %V 2 %I Peer Community In %U https://peercommunityjournal.org/articles/10.24072/pcjournal.156/ %R 10.24072/pcjournal.156 %F 10_24072_pcjournal_156
Mahringer, David; Zmarz, Pawel; Okuno, Hiroyuki; Bito, Haruhiko; Keller, Georg B. Functional correlates of immediate early gene expression in mouse visual cortex. Peer Community Journal, Volume 2 (2022), article no. e45. doi : 10.24072/pcjournal.156. https://peercommunityjournal.org/articles/10.24072/pcjournal.156/
PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.neuro.100005
Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
[1] Visuomotor Coupling Shapes the Functional Development of Mouse Visual Cortex, Cell, Volume 169 (2017) no. 7 | DOI
[2] Differential expression of the immediate early genes FOS and ZENK following auditory stimulation in the juvenile male and female zebra finch, Molecular Brain Research, Volume 116 (2003) no. 1-2, pp. 147-154 | DOI
[3] Alteration of Neuronal Firing Properties after In Vivo Experience in a FosGFP Transgenic Mouse, Journal of Neuroscience, Volume 24 (2004) no. 29, pp. 6466-6475 | DOI
[4] MAPK, CREB and<i>zif268</i>are all required for the consolidation of recognition memory, Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Volume 358 (2003) no. 1432, pp. 805-814 | DOI
[5] Expression ofC-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat, The Journal of Comparative Neurology, Volume 296 (1990) no. 4, pp. 517-530 | DOI
[6] Narp regulates homeostatic scaling of excitatory synapses on parvalbumin-expressing interneurons, Nature Neuroscience, Volume 13 (2010) no. 9, pp. 1090-1097 | DOI
[7] Arc/Arg3.1 Interacts with the Endocytic Machinery to Regulate AMPA Receptor Trafficking, Neuron, Volume 52 (2006) no. 3, pp. 445-459 | DOI
[8] Sensitive red protein calcium indicators for imaging neural activity, eLife, Volume 5 (2016) | DOI
[9] Hippocampal Memory Traces Are Differentially Modulated by Experience, Time, and Adult Neurogenesis, Neuron, Volume 83 (2014) no. 1, pp. 189-201 | DOI
[10] Functional imaging of hippocampal place cells at cellular resolution during virtual navigation, Nature Neuroscience, Volume 13 (2010) no. 11, pp. 1433-1440 | DOI
[11] Imaging Large-Scale Neural Activity with Cellular Resolution in Awake, Mobile Mice, Neuron, Volume 56 (2007) no. 1, pp. 43-57 | DOI
[12] Transcriptional Regulation by Neuronal Activity, Springer US, Boston, MA, 2008 | DOI
[13] Differential expression of immediate early genes Zif268 and c-Fos in the hippocampus and prefrontal cortex following spatial learning and glutamate receptor antagonism, Behavioural Brain Research, Volume 307 (2016), pp. 194-198 | DOI
[14] Small modulation of ongoing cortical dynamics by sensory input during natural vision, Nature, Volume 431 (2004) no. 7008, pp. 573-578 | DOI
[15] Impaired Long-Term Memory and NR2A-Type NMDA Receptor-Dependent Synaptic Plasticity in Mice Lacking c-Fos in the CNS, The Journal of Neuroscience, Volume 23 (2003) no. 27, pp. 9116-9122 | DOI
[16] Activation of the CREB/c-Fos Pathway during Long-Term Synaptic Plasticity in the Cerebellum Granular Layer, Frontiers in Cellular Neuroscience, Volume 11 (2017) | DOI
[17] A Specific Requirement of Arc/Arg3.1 for Visual Experience-Induced Homeostatic Synaptic Plasticity in Mouse Primary Visual Cortex, Journal of Neuroscience, Volume 30 (2010) no. 21, pp. 7168-7178 | DOI
[18] Generation of a Synthetic Memory Trace, Science, Volume 335 (2012) no. 6075, pp. 1513-1516 | DOI
[19] Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene, Nature, Volume 311 (1984) no. 5985, pp. 433-438 | DOI
[20] Obligatory Role for the Immediate Early Gene NARP in Critical Period Plasticity, Neuron, Volume 79 (2013) no. 2, pp. 335-346 | DOI
[21] Insights into immediate-early gene function in hippocampal memory consolidation using antisense oligonucleotide and fluorescent imaging approaches, Hippocampus, Volume 12 (2002) no. 1, pp. 86-104 | DOI
[22] Inhibition of Activity-Dependent Arc Protein Expression in the Rat Hippocampus Impairs the Maintenance of Long-Term Potentiation and the Consolidation of Long-Term Memory, The Journal of Neuroscience, Volume 20 (2000) no. 11, pp. 3993-4001 | DOI
[23] Antisense oligodeoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training, Proceedings of the National Academy of Sciences, Volume 94 (1997) no. 6, pp. 2693-2698 | DOI
[24] Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles, Nature Neuroscience, Volume 2 (1999) no. 12, pp. 1120-1124 | DOI
[25] Recent behavioral history modifies coupling between cell activity and <i>Arc</i> gene transcription in hippocampal CA1 neurons, Proceedings of the National Academy of Sciences, Volume 103 (2006) no. 4, pp. 1077-1082 | DOI
[26] Neuronal Firing Rate Homeostasis Is Inhibited by Sleep and Promoted by Wake, Cell, Volume 165 (2016) no. 1, pp. 180-191 | DOI
[27] Critical period plasticity in local cortical circuits, Nature Reviews Neuroscience, Volume 6 (2005) no. 11, pp. 877-888 | DOI
[28] Functional and structural underpinnings of neuronal assembly formation in learning, Nature Neuroscience, Volume 19 (2016) no. 12, pp. 1553-1562 | DOI
[29] Behaviourally driven gene expression reveals song nuclei in hummingbird brain, Nature, Volume 406 (2000) no. 6796, pp. 628-632 | DOI
[30] Arc restores juvenile plasticity in adult mouse visual cortex, Proceedings of the National Academy of Sciences, Volume 114 (2017) no. 34, pp. 9182-9187 | DOI
[31] A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories, Nature Neuroscience, Volume 4 (2001) no. 3, pp. 289-296 | DOI
[32] Opposing Influence of Top-down and Bottom-up Input on Excitatory Layer 2/3 Neurons in Mouse Primary Visual Cortex, Neuron, Volume 108 (2020) no. 6 | DOI
[33] Finding the engram, Nature Reviews Neuroscience, Volume 16 (2015) no. 9, pp. 521-534 | DOI
[34] Visual Stimulation Regulates the Expression of Transcription Factors and Modulates the Composition of AP-1 in Visual Cortex<sup>a</sup>, The Journal of Neuroscience, Volume 16 (1996) no. 12, pp. 3968-3978 | DOI
[35] Immediate early gene expression in cat visual cortex during and after the critical period: differences between EGR-1 and Fos proteins, Molecular Brain Research, Volume 36 (1996) no. 1, pp. 12-22 | DOI
[36] Functional labeling of neurons and their projections using the synthetic activity–dependent promoter E-SARE, Nature Methods, Volume 10 (2013) no. 9, pp. 889-895 | DOI
[37] Synaptic Scaling and Homeostatic Plasticity in the Mouse Visual Cortex In Vivo, Neuron, Volume 80 (2013) no. 2, pp. 327-334 | DOI
[38] Sensorimotor Mismatch Signals in Primary Visual Cortex of the Behaving Mouse, Neuron, Volume 74 (2012) no. 5, pp. 809-815 | DOI
[39] Predictive Processing: A Canonical Cortical Computation, Neuron, Volume 100 (2018) no. 2, pp. 424-435 | DOI
[40] A gene for neuronal plasticity in the mammalian brain: Zif268/Egr-1/NGFI-A/Krox-24/TIS8/ZENK?, Progress in Neurobiology, Volume 74 (2004) no. 4, pp. 183-211 | DOI
[41] Two-photon Calcium Imaging in Mice Navigating a Virtual Reality Environment, Journal of Visualized Experiments (2014) no. 84 | DOI
[42] A Sensorimotor Circuit in Mouse Cortex for Visual Flow Predictions, Neuron, Volume 95 (2017) no. 6 | DOI
[43] Optogenetic stimulation of a hippocampal engram activates fear memory recall, Nature, Volume 484 (2012) no. 7394, pp. 381-385 | DOI
[44] Expression of c-Fos and Arc in hippocampal region CA1 marks neurons that exhibit learning-related activity changes, bioRxiv, 644526 (2019) | DOI
[45] Learning enhances the relative impact of top-down processing in the visual cortex, Nature Neuroscience, Volume 18 (2015) no. 8, pp. 1116-1122 | DOI
[46] Experience-Dependent Plasticity of Mouse Visual Cortex in the Absence of the Neuronal Activity-Dependent Marker<i>egr1/zif268</i>, The Journal of Neuroscience, Volume 21 (2001) no. 24, pp. 9724-9732 | DOI
[47] Loss of Arc renders the visual cortex impervious to the effects of sensory experience or deprivation, Nature Neuroscience, Volume 13 (2010) no. 4, pp. 450-457 | DOI
[48] Sustained Arc/Arg3.1 Synthesis Controls Long-Term Potentiation Consolidation through Regulation of Local Actin Polymerization in the Dentate Gyrus In Vivo, Journal of Neuroscience, Volume 27 (2007) no. 39, pp. 10445-10455 | DOI
[49] Role of Immediate-Early Genes in Synaptic Plasticity and Neuronal Ensembles Underlying the Memory Trace, Frontiers in Molecular Neuroscience, Volume 8 (2016) | DOI
[50] Early growth response 1 (Egr-1) directly regulates GABA<sub>A</sub>receptor α2, α4, and θ subunits in the hippocampus, Journal of Neurochemistry, Volume 133 (2015) no. 4, pp. 489-500 | DOI
[51] Mapping Patterns of c- <i>fos</i> Expression in the Central Nervous System After Seizure, Science, Volume 237 (1987) no. 4811, pp. 192-197 | DOI
[52] Inverse Synaptic Tagging of Inactive Synapses via Dynamic Interaction of Arc/Arg3.1 with CaMKIIβ, Cell, Volume 149 (2012) no. 4, pp. 886-898 | DOI
[53] Paxinos, G. , and Franklin, K.B.J. (2013). Paxinos and Franklin’s the mouse brain in stereotaxic coordinates (Academic Press).
[54] The subcellular organization of neocortical excitatory connections, Nature, Volume 457 (2009) no. 7233, pp. 1142-1145 | DOI
[55] The Activity-Regulated Cytoskeletal-Associated Protein (Arc/Arg3.1) Is Required for Memory Consolidation of Pavlovian Fear Conditioning in the Lateral Amygdala, Journal of Neuroscience, Volume 28 (2008) no. 47, pp. 12383-12395 | DOI
[56] Creating a False Memory in the Hippocampus, Science, Volume 341 (2013) no. 6144, pp. 387-391 | DOI
[57] Spatial Exploration-Induced Arc mRNA and Protein Expression: Evidence for Selective, Network-Specific Reactivation, Journal of Neuroscience, Volume 25 (2005) no. 7, pp. 1761-1768 | DOI
[58] Localization of a Stable Neural Correlate of Associative Memory, Science, Volume 317 (2007) no. 5842, pp. 1230-1233 | DOI
[59] Increased Expression of the Immediate-Early Gene Arc/Arg3.1 Reduces AMPA Receptor-Mediated Synaptic Transmission, Neuron, Volume 52 (2006) no. 3, pp. 461-474 | DOI
[60] Brief visual experience induces immediate early gene expression in the cat visual cortex., Proceedings of the National Academy of Sciences, Volume 89 (1992) no. 12, pp. 5437-5441 | DOI
[61] Integration of visual motion and locomotion in mouse visual cortex, Nature Neuroscience, Volume 16 (2013) no. 12, pp. 1864-1869 | DOI
[62] New views of Arc, a master regulator of synaptic plasticity, Nature Neuroscience, Volume 14 (2011) no. 3, pp. 279-284 | DOI
[63] Arc/Arg3.1 Mediates Homeostatic Synaptic Scaling of AMPA Receptors, Neuron, Volume 52 (2006) no. 3, pp. 475-484 | DOI
[64] Organization of visual pathways in normal and visually deprived cats., Physiological Reviews, Volume 62 (1982) no. 2, pp. 738-855 | DOI
[65] Delayed Degradation and Impaired Dendritic Delivery of Intron-Lacking EGFP-Arc/Arg3.1 mRNA in EGFP-Arc Transgenic Mice, Frontiers in Molecular Neuroscience, Volume 10 (2018) | DOI
[66] Multiple periods of functional ocular dominance plasticity in mouse visual cortex, Nature Neuroscience, Volume 8 (2005) no. 3, pp. 380-388 | DOI
[67] Rapid and active stabilization of visual cortical firing rates across light–dark transitions, Proceedings of the National Academy of Sciences, Volume 116 (2019) no. 36, pp. 18068-18077 | DOI
[68] Arc/Arg3.1: Linking Gene Expression to Synaptic Plasticity and Memory, Neuron, Volume 52 (2006) no. 3, pp. 403-407 | DOI
[69] Spatial exploration inducesARC, a plasticity-related immediate-early gene, only in calcium/calmodulin-dependent protein kinase II-positive principal excitatory and inhibitory neurons of the rat forebrain, The Journal of Comparative Neurology, Volume 498 (2006) no. 3, pp. 317-329 | DOI
[70] The Transcription Factor Zif268/Egr1, Brain Plasticity, and Memory, Progress in Molecular Biology and Translational Science, Elsevier, 2014, pp. 89-129 | DOI
[71] Egr1-EGFP transgenic mouse allows in vivo recording of Egr1 expression and neural activity, Journal of Neuroscience Methods, Volume 363 (2021) | DOI
[72] In Vivo Two-Photon Imaging Reveals a Role of Arc in Enhancing Orientation Specificity in Visual Cortex, Cell, Volume 126 (2006) no. 2, pp. 389-402 | DOI
[73] Rapid Translation of Arc/Arg3.1 Selectively Mediates mGluR-Dependent LTD through Persistent Increases in AMPAR Endocytosis Rate, Neuron, Volume 59 (2008) no. 1, pp. 84-97 | DOI
[74] Npas4 Is a Critical Regulator of Learning-Induced Plasticity at Mossy Fiber-CA3 Synapses during Contextual Memory Formation, Neuron, Volume 97 (2018) no. 5 | DOI
[75] NMDA receptors in visual cortex are necessary for normal visuomotor integration and skill learning, eLife, Volume 11 (2022) | DOI
[76] In vivo imaging of immediate early gene expression reveals layer-specific memory traces in the mammalian brain, Proceedings of the National Academy of Sciences, Volume 111 (2014) no. 7, pp. 2788-2793 | DOI
[77] Differential expression of immediate-early genes, c-fos and zif268, in the visual cortex of young rats: effects of a noradrenergic neurotoxin on their expression, Neuroscience, Volume 92 (1999) no. 2, pp. 473-484 | DOI
[78] Activity-Regulated Transcription: Bridging the Gap between Neural Activity and Behavior, Neuron, Volume 100 (2018) no. 2, pp. 330-348 | DOI
[79] Acute suppression, but not chronic genetic deficiency, of c- ifos/i gene expression impairs long-term memory in aversive taste learning, Proceedings of the National Academy of Sciences, Volume 103 (2006) no. 18, pp. 7106-7111 | DOI
[80] An Embedded Subnetwork of Highly Active Neurons in the Neocortex, Neuron, Volume 68 (2010) no. 6, pp. 1043-1050 | DOI
[81] Mismatch Receptive Fields in Mouse Visual Cortex, Neuron, Volume 92 (2016) no. 4, pp. 766-772 | DOI
Cited by Sources: