Salient Experiences Are Represented by Unique Transcriptional Signatures in the Mouse Brain

Overview

Journal Elife

Specialty Biology

Date 2018 Feb 8

PMID 29412137

Citations 24

Authors

Diptendu Mukherjee

Bogna Marta Ignatowska-Jankowska

Eyal Itskovits

Ben Jerry Gonzales

Hagit Turm

Liz Izakson

Doron Haritan

Noa Bleistein

Chen Cohen

Ido Amit

Tal Shay

Brad Grueter

Alon Zaslaver

Ami Citri

Affiliations

Soon will be listed here.

Abstract

It is well established that inducible transcription is essential for the consolidation of salient experiences into long-term memory. However, whether inducible transcription relays information about the identity and affective attributes of the experience being encoded, has not been explored. To this end, we analyzed transcription induced by a variety of rewarding and aversive experiences, across multiple brain regions. Our results describe the existence of robust transcriptional signatures uniquely representing distinct experiences, enabling near-perfect decoding of recent experiences. Furthermore, experiences with shared attributes display commonalities in their transcriptional signatures, exemplified in the representation of valence, habituation and reinforcement. This study introduces the concept of a neural transcriptional code, which represents the encoding of experiences in the mouse brain. This code is comprised of distinct transcriptional signatures that correlate to attributes of the experiences that are being committed to long-term memory.

Citing Articles

Stimulation of Locus Ceruleus Inputs to the Prelimbic Cortex in Mice Induces Cell Type-Specific Expression of the Gene.

Craig G, Ramos L, Essig S, Eagles N, Jaffe A, Martinowich K eNeuro. 2024; 11(12).

PMID: 39632090 PMC: 11675532. DOI: 10.1523/ENEURO.0328-24.2024.

Stimulation of locus coeruleus inputs to the frontal cortex in mice induces cell type-specific expression of the gene.

Craig G, Ramos L, Essig S, Eagles N, Jaffe A, Martinowich K bioRxiv. 2024; .

PMID: 39091890 PMC: 11291023. DOI: 10.1101/2024.07.22.604695.

Projection-TAGs enable multiplex projection tracing and multi-modal profiling of projection neurons.

Yang L, Liu F, Hahm H, Okuda T, Li X, Zhang Y bioRxiv. 2024; .

PMID: 38712231 PMC: 11071495. DOI: 10.1101/2024.04.24.590975.

Moral considerability of brain organoids from the perspective of computational architecture.

Boyd J Oxf Open Neurosci. 2024; 3:kvae004.

PMID: 38595940 PMC: 10995847. DOI: 10.1093/oons/kvae004.

Biphasic Npas4 expression promotes inhibitory plasticity and suppression of fear memory consolidation in mice.

Brito D, Kupke J, Sokolov R, Cambridge S, Both M, Bengtson C Mol Psychiatry. 2024; 29(7):1929-1940.

PMID: 38347124 PMC: 11408256. DOI: 10.1038/s41380-024-02454-3.

References

Bialek W, Rieke F, de Ruyter van Steveninck R, Warland D . Reading a neural code. Science. 1991; 252(5014):1854-7. DOI: 10.1126/science.2063199. View

Collins F, Varmus H . A new initiative on precision medicine. N Engl J Med. 2015; 372(9):793-5. PMC: 5101938. DOI: 10.1056/NEJMp1500523. View

Lamb J . The Connectivity Map: a new tool for biomedical research. Nat Rev Cancer. 2006; 7(1):54-60. DOI: 10.1038/nrc2044. View

Sylwestrak E, Rajasethupathy P, Wright M, Jaffe A, Deisseroth K . Multiplexed Intact-Tissue Transcriptional Analysis at Cellular Resolution. Cell. 2016; 164(4):792-804. PMC: 4775740. DOI: 10.1016/j.cell.2016.01.038. View

Hyman S, Malenka R, Nestler E . Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci. 2006; 29:565-98. DOI: 10.1146/annurev.neuro.29.051605.113009. View

Okuno H . Regulation and function of immediate-early genes in the brain: beyond neuronal activity markers. Neurosci Res. 2010; 69(3):175-86. DOI: 10.1016/j.neures.2010.12.007. View

Lacar B, Linker S, Jaeger B, Krishnaswami S, Barron J, Kelder M . Nuclear RNA-seq of single neurons reveals molecular signatures of activation. Nat Commun. 2016; 7:11022. PMC: 4838832. DOI: 10.1038/ncomms11022. View

Robison A, Nestler E . Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurosci. 2011; 12(11):623-37. PMC: 3272277. DOI: 10.1038/nrn3111. View

Li S, Harner E, Adjeroh D . Random KNN feature selection - a fast and stable alternative to Random Forests. BMC Bioinformatics. 2011; 12:450. PMC: 3281073. DOI: 10.1186/1471-2105-12-450. View

10.

Clayton D . The genomic action potential. Neurobiol Learn Mem. 2000; 74(3):185-216. DOI: 10.1006/nlme.2000.3967. View

11.

Renier N, Adams E, Kirst C, Wu Z, Azevedo R, Kohl J . Mapping of Brain Activity by Automated Volume Analysis of Immediate Early Genes. Cell. 2016; 165(7):1789-1802. PMC: 4912438. DOI: 10.1016/j.cell.2016.05.007. View

12.

Haber S, Knutson B . The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology. 2009; 35(1):4-26. PMC: 3055449. DOI: 10.1038/npp.2009.129. View

13.

Kragel P, Knodt A, Hariri A, LaBar K . Decoding Spontaneous Emotional States in the Human Brain. PLoS Biol. 2016; 14(9):e2000106. PMC: 5023171. DOI: 10.1371/journal.pbio.2000106. View

14.

Robinson T, Berridge K . Review. The incentive sensitization theory of addiction: some current issues. Philos Trans R Soc Lond B Biol Sci. 2008; 363(1507):3137-46. PMC: 2607325. DOI: 10.1098/rstb.2008.0093. View

15.

Schultz W . Dopamine signals for reward value and risk: basic and recent data. Behav Brain Funct. 2010; 6:24. PMC: 2876988. DOI: 10.1186/1744-9081-6-24. View

16.

Stanley G . Reading and writing the neural code. Nat Neurosci. 2013; 16(3):259-63. DOI: 10.1038/nn.3330. View

17.

Fortin S, Chartoff E, Roitman M . The Aversive Agent Lithium Chloride Suppresses Phasic Dopamine Release Through Central GLP-1 Receptors. Neuropsychopharmacology. 2015; 41(3):906-15. PMC: 4707837. DOI: 10.1038/npp.2015.220. View

18.

Posner J, Russell J, Peterson B . The circumplex model of affect: an integrative approach to affective neuroscience, cognitive development, and psychopathology. Dev Psychopathol. 2005; 17(3):715-34. PMC: 2367156. DOI: 10.1017/S0954579405050340. View

19.

Turm H, Mukherjee D, Haritan D, Tahor M, Citri A . Comprehensive analysis of transcription dynamics from brain samples following behavioral experience. J Vis Exp. 2014; (90). PMC: 4828017. DOI: 10.3791/51642. View

20.

Alberini C . Transcription factors in long-term memory and synaptic plasticity. Physiol Rev. 2009; 89(1):121-45. PMC: 3883056. DOI: 10.1152/physrev.00017.2008. View