We used two-photon calcium imaging with single-cell and cell-type resolution. Fear conditioning induced heterogeneous tuning shifts at single-cell level in the auditory cortex, with shifts both to CS+ frequency and to the control CS- stimulus frequency. We thus extend the view of simple expansion of CS+ tuned regions. Instead of conventional freezing reactions only, we observe selective orienting responses towards the conditioned stimuli. The orienting responses were often followed by escape behavior.

Department of Physiology 2nd Faculty of Medicine Charles University Prague Prague Czech Republic

Zobrazit více v PubMed

ANTUNES R, MOITA MA. Discriminative auditory fear learning requires both tuned and nontuned auditory pathways to the amygdala. J Neurosci. 2010;30:9782–9787. doi: 10.1523/JNEUROSCI.1037-10.2010. PubMed DOI PMC

ATALLAH BV, BRUNS W, CARANDINI M, SCANZIANI M. Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron. 2012;73:159–170. doi: 10.1016/j.neuron.2011.12.013. PubMed DOI PMC

BAKIN JS, WEINBERGER NM. Classical-conditioning induces CS-specific receptive-field plasticity in the auditory-cortex of the guinea-pig. Brain Res. 1990;536:271–286. doi: 10.1016/0006-8993(90)90035-A. PubMed DOI

BANDYOPADHYAY S, SHAMMA SA, KANOLD PO. Dichotomy of functional organization in the mouse auditory cortex. Nat Neurosci. 2010;13:361–368. doi: 10.1038/nn.2490. PubMed DOI PMC

BAO SW, CHAN WT, MERZENICH MM. Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature. 2001;412:79–83. doi: 10.1038/35083586. PubMed DOI

BATHELLIER B, USHAKOVA L, RUMPEL S. Discrete neocortical dynamics predict behavioral categorization of sounds. Neuron. 2012;76:435–449. doi: 10.1016/j.neuron.2012.07.008. PubMed DOI

BIESZCZAD KM, WEINBERGER NM. Representational gain in cortical area underlies increase of memory strength. Proc Natl Acad Sci U S A. 2010;107:3793–3798. doi: 10.1073/pnas.1000159107. PubMed DOI PMC

BLANCHARD DC. Translating dynamic defense patterns from rodents to people. Neurosci Biobehav Rev. 2017;76:22–28. doi: 10.1016/j.neubiorev.2016.11.001. PubMed DOI

BRADLEY MM. Natural selective attention: Orienting and emotion. Psychophysiology. 2009;46:1–11. doi: 10.1111/j.1469-8986.2008.00702.x. PubMed DOI PMC

CHEN TW, WARDILL TJ, SUN Y, PULVER SR, RENNINGER SL, BAOHAN A, SCHREITER ER, KERR RA, ORGER MB, JAYARAMAN V, LOOGER LL, SVOBODA K, KIM DS. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature. 2013;499:295–300. doi: 10.1038/nature12354. PubMed DOI PMC

COHEN L, MIZRAHI A. Plasticity during motherhood: changes in excitatory and inhibitory layer 2/3 neurons in auditory cortex. J Neurosci. 2015;35:1806–1815. doi: 10.1523/JNEUROSCI.1786-14.2015. PubMed DOI PMC

DIAMOND DM, WEINBERGER NM. Classical-conditioning rapidly induces specific changes in frequency receptive-fields of single neurons in secondary and ventral ectosylvian auditory cortical fields. Brain Res. 1986;372:357–360. doi: 10.1016/0006-8993(86)91144-3. PubMed DOI

EDELINE JM, PHAM P, WEINBERGER NM. Rapid development of learning-induced receptive-field plasticity in the auditory-cortex. Behav Neurosci. 1993;107:539–551. doi: 10.1037/0735-7044.107.4.539. PubMed DOI

FRITZ J, SHAMMA S, ELHILALI M, KLEIN D. Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex. Nat Neurosci. 2003;6:1216–1223. doi: 10.1038/nn1141. PubMed DOI

FRITZ JB, DAVID SV, RADTKE-SCHULLER S, YIN P, SHAMMA SA. Adaptive, behaviorally gated, persistent encoding of task-relevant auditory information in ferret frontal cortex. Nat Neurosci. 2010;13:1011–1119. doi: 10.1038/nn.2598. PubMed DOI PMC

FROEMKE RC, CARCEA I, BARKER AJ, YUAN K, SEYBOLD BA, MARTINS ARO, ZAIKA N, BERNSTEIN H, WACHS M, LEVIS PA, POLLEY DB, MERZENICH MM, SCHREINER CE. Long-term modification of cortical synapses improves sensory perception. Nat Neurosci. 2013;16:79–88. doi: 10.1038/nn.3274. PubMed DOI PMC

FROEMKE RC, MERZENICH MM, SCHREINER CE. A synaptic memory trace for cortical receptive field plasticity. Nature. 2007;450:425–429. doi: 10.1038/nature06289. PubMed DOI

FROEMKE RC, SCHREINER CE. Synaptic plasticity as a cortical coding scheme. Curr Opin Neurobiol. 2015;35:185–199. doi: 10.1016/j.conb.2015.10.003. PubMed DOI PMC

GREWE BF, GRUNDEMANN J, KITCH LJ, LECOQ JA, PARKER JG, MARSHALL JD, LARKIN MC, JERCOG PE, GRENIER F, LI JZ, LÜTHI A, SCHNITZER MJ. Neural ensemble dynamics underlying a long-term associative memory. Nature. 2017;543:670–675. doi: 10.1038/nature21682. PubMed DOI PMC

GREWE BF, LANGER D, KASPER H, KAMPA BM, HELMCHEN F. High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision. Nat Methods. 2010;7:399–405. doi: 10.1038/nmeth.1453. PubMed DOI

GUO F, INTSKIRVELI I, BLAKE DT, METHERATE R. Tone-detection training enhances spectral integration mediated by intracortical pathways in primary auditory cortex. Neurobiol Learn Mem. 2013;101:75–84. doi: 10.1016/j.nlm.2013.01.006. PubMed DOI PMC

GUO W, CHAMBERS AR, DARROW KN, HANCOCK KE, SHINN-CUNNINGHAM BG, POLLEY DB. Robustness of cortical topography across fields, laminae, anesthetic states, and neurophysiological signal types. J Neurosci. 2012;32:9159–9172. doi: 10.1523/JNEUROSCI.0065-12.2012. PubMed DOI PMC

HANGYA B, RANADE SP, LORENC M, KEPECS A. Central cholinergic neurons are rapidly recruited by reinforcement feedback. Cell. 2015;162:1155–1168. doi: 10.1016/j.cell.2015.07.057. PubMed DOI PMC

HARRIS KD, QUIROGA RQ, FREEMAN J, SMITH SL. Improving data quality in neuronal population recordings. Nat Neurosci. 2016;19:1165–1174. doi: 10.1038/nn.4365. PubMed DOI PMC

ISSA JB, HAEFFELE BD, AGARWAL A, BERGLES DE, YOUNG ED, YUE DT. Multiscale optical Ca2+ imaging of tonal organization in mouse auditory cortex. Neuron. 2014;83:944–959. doi: 10.1016/j.neuron.2014.07.009. PubMed DOI PMC

JI WQ, SUGA N. Serotonergic modulation of plasticity of the auditory cortex elicited by fear conditioning. J Neurosci. 2007;27:4910–4918. doi: 10.1523/JNEUROSCI.5528-06.2007. PubMed DOI PMC

JIANG XL, SHEN S, CADWELL CR, BERENS P, SINZ F, ECKERT AS, PATEL S, TOLIAS AS. Principles of connectivity among morphologically defined cell types in adult neocortex. Science. 2015;350:aac9462. doi: 10.1126/science.aac9462. PubMed DOI PMC

KANOLD PO, NELKEN I, POLLEY DB. Local versus global scales of organization in auditory cortex. Trends Neurosci. 2014;37:502–510. doi: 10.1016/j.tins.2014.06.003. PubMed DOI PMC

KATO HK, GILLET SN, ISAACSON JS. Flexible sensory representations in auditory cortex driven by behavioral relevance. Neuron. 2015;88:1027–1039. doi: 10.1016/j.neuron.2015.10.024. PubMed DOI PMC

KEPECS A, FISHELL G. Interneuron cell types are fit to function. Nature. 2014;50:318–326. doi: 10.1038/nature12983. PubMed DOI PMC

KILGARD MP, MERZENICH MM. Cortical map reorganization enabled by nucleus basalis activity. Science. 1998;279:1714–1718. doi: 10.1126/science.279.5357.1714. PubMed DOI

KONG E, MONJE FJ, HIRSCH J, POLLAK DD. Learning not to fear: neural correlates of learned safety. Neuropsychopharmacology. 2014;39:515–527. doi: 10.1038/npp.2013.191. PubMed DOI PMC

KRABBE S, PARADISO E, D’AQUIN S, BITTERMAN Y, COURTIN, XU C, YONEHARA K, MARKOVIC M, MÜLLER C, EICHLISBERGER T, GRÜNDEMANN J, FERRAGUTI F, LÜTHI A. Adaptive disinhibitory gating by VIP interneurons permits associative learning. Nat Neurosci. 2019;22:1834–1843. doi: 10.1038/s41593-019-0508-y. PubMed DOI

KRAUS N, DISTERHOFT JF. Response plasticity of single neurons in rabbit auditory association cortex during tone-signalled learning. Brain Res. 1982;246:205–215. doi: 10.1016/0006-8993(82)91168-4. PubMed DOI

KUCHIBHOTLA KV, GILL JV, LINDSAY GW, PAPADOYANNIS ES, FIELD RE, HINDMARSH STEN TA, MILLER KD, FROEMKE RC. Parallel processing by cortical inhibition enables context-dependent behavior. Nat Neurosci. 2017;20:62–71. doi: 10.1038/nn.4436. PubMed DOI PMC

LAI CSW, FRANKE TF, GAN WB. Opposite effects of fear conditioning and extinction on dendritic spine remodelling. Nature. 2012;483:87–91. doi: 10.1038/nature10792. PubMed DOI

LAKATOS P, MUSACCHIA G, O’CONNEL MN, FALCHIER AY, JAVITT DC, SCHROEDER CE. The spectrotemporal filter mechanism of auditory selective attention. Neuron. 2013;77:750–761. doi: 10.1016/j.neuron.2012.11.034. PubMed DOI PMC

LAKUNINA AA, NARDOCI MB, AHMADIAN Y, JARAMILLO S. Somatostatin-expressing interneurons in the auditory cortex mediate sustained suppression by spectral surround. J Neurosci. 2020;40:3564–3575. doi: 10.1523/JNEUROSCI.1735-19.2020. PubMed DOI PMC

LEE S, KRUGLIKOV I, HUANG ZJ, FISHELL G, RUDY B. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat Neurosci. 2013;16:1662–1670. doi: 10.1038/nn.3544. PubMed DOI PMC

LETZKUS JJ, WOLFF SBE, LUTHI A. Disinhibition, a circuit mechanism for associative learning and memory. Neuron. 2015;88:264–276. doi: 10.1016/j.neuron.2015.09.024. PubMed DOI

LETZKUS JJ, WOLFF SBE, MEYER EMM, TOVOTE P, COURTIN J, HERRY C, LÜTHI A. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature. 2011;480:331–335. doi: 10.1038/nature10674. PubMed DOI

LI L-Y, XIONG XR, IBRAHIM LA, YUAN W, TAO HW, ZHANG LI. Differential receptive field properties of parvalbumin and somatostatin inhibitory neurons in mouse auditory cortex. Cereb Cortex. 2014;25:1782–1791. doi: 10.1093/cercor/bht417. PubMed DOI PMC

LI LY, JI XY, LIANG FX, LI YT, XIAO Z, TAO HW, ZHANG LI. A feedforward inhibitory circuit mediates lateral refinement of sensory representation in upper layer 2/3 of mouse primary auditory cortex. J Neurosci. 2014;34:13670–13683. doi: 10.1523/JNEUROSCI.1516-14.2014. PubMed DOI PMC

LIU BH, WU GK, ARBUCKLE R, TAO HW, ZHANG LI. Defining cortical frequency tuning with recurrent excitatory circuitry. Nat Neurosci. 2007;10:1594–1600. doi: 10.1038/nn2012. PubMed DOI PMC

MAOR I, SHALEV A, MIZRAHI A. Distinct spatiotemporal response properties of excitatory versus inhibitory neurons in the mouse auditory cortex. Cereb Cortex. 2016;26:4242–4252. doi: 10.1093/cercor/bhw266. PubMed DOI PMC

MARLIN BJ, MITRE M, D’AMOUR JA, CHAO MV, FROEMKE RC. Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature. 2015;520:499–504. doi: 10.1038/nature14402. PubMed DOI PMC

McGANN JP. Associative learning and sensory neuroplasticity: how does it happen and what is it good for? Learn Mem. 2015;22:567–576. doi: 10.1101/lm.039636.115. PubMed DOI PMC

MOCZULSKA KE, TINTER-THIEDE J, PETER M, USHAKOVA L, WERNLE T, BATHELLIER B, RUMPEL S. Dynamics of dendritic spines in the mouse auditory cortex during memory formation and memory recall. Proc Natl Acad Sci U S A. 2013;110:18315–18320. doi: 10.1073/pnas.1312508110. PubMed DOI PMC

NAKAYAMA D, BARAKI Z, ONOUE K, IKEGAYA Y, MATSUKI N, NOMURA H. Frontal association cortex is engaged in stimulus integration during associative learning. Curr Biol. 2015;25:117–123. doi: 10.1016/j.cub.2014.10.078. PubMed DOI

NODA T, TAKAHASHI H. Anesthetic effects of isoflurane on the tonotopic map and neuronal population activity in the rat auditory cortex. Eur J Neurosci. 2015;42:2298–2311. doi: 10.1111/ejn.13007. PubMed DOI

NOVAK O, ZELENKA O, HROMADKA T, SYKA J. Immediate manifestation of acoustic trauma in the auditory cortex is layer-specific and cell type-dependent. J Neurophysiol. 2016;115:1860–1874. doi: 10.1152/jn.00810.2015. PubMed DOI PMC

PACHITARIU M, LYAMZIN DR, SAHANI M, LESICA NA. State-dependent population coding in primary auditory cortex. J Neurosci. 2015;35:2058–2073. doi: 10.1523/JNEUROSCI.3318-14.2015. PubMed DOI PMC

PI HJ, HANGYA B, KVITSIANI D, SANDERS JI, HUANG ZJ, KEPECS A. Cortical interneurons that specialize in disinhibitory control. Nature. 2013;503:521–524. doi: 10.1038/nature12676. PubMed DOI PMC

PIENKOWSKI M, EGGERMONT JJ. Cortical tonotopic map plasticity and behavior. Neurosci Biobehav Rev. 2011;35:2117–2128. doi: 10.1016/j.neubiorev.2011.02.002. PubMed DOI

POLLEY DB, STEINBERG EE, MERZENICH MM. Perceptual learning directs auditory cortical map reorganization through top-down influences. J Neurosci. 2006;26:4970–4982. doi: 10.1523/JNEUROSCI.3771-05.2006. PubMed DOI PMC

POORT J, KHAN AG, PACHITARIU M, NEMRI A, ORSOLIC I, KRUPIC J, BAUZA M, SAHANI M, KELLER GB, MRSIC-FLOGEL TD, HOFER SB. Learning enhances sensory and multiple non-sensory representations in primary visual cortex. Neuron. 2015;86:1478–1490. doi: 10.1016/j.neuron.2015.05.037. PubMed DOI PMC

RECANZONE GH, SCHREINER CE, MERZENICH MM. Plasticity in the frequency representation of primary auditory-cortex following discrimination-training in adult owl monkeys. J Neurosci. 1993;13:87–103. doi: 10.1523/JNEUROSCI.13-01-00087.1993. PubMed DOI PMC

RODGERS CC, DEWEESE MR. Neural correlates of task switching in prefrontal cortex and primary auditory cortex in a novel stimulus selection task for rodents. Neuron. 2014:1157–1170. doi: 10.1016/j.neuron.2014.04.031. PubMed DOI

ROTHSCHILD G, COHEN L, MIZRAHI A, NELKEN I. Elevated correlations in neuronal ensembles of mouse auditory cortex following parturition. J Neurosci. 2013;33:12851–12861. doi: 10.1523/JNEUROSCI.4656-12.2013. PubMed DOI PMC

ROTHSCHILD G, MIZRAHI A. Global order and local disorder in brain maps. Annu Rev Neurosci. 2015;38:247–268. doi: 10.1146/annurev-neuro-071013-014038. PubMed DOI

ROTHSCHILD G, NELKEN I, MIZRAHI A. Functional organization and population dynamics in the mouse primary auditory cortex. Nat Neurosci. 2010;13:353–360. doi: 10.1038/nn.2484. PubMed DOI

RUTKOWSKI RG, WEINBERGER NM. Encoding of learned importance of sound by magnitude of representational area in primary auditory cortex. Proc Natl Acad Sci U S A. 2005;102:13664–13669. doi: 10.1073/pnas.0506838102. PubMed DOI PMC

SARRO EC, Von TRAPP G, MOWERY TM, KOTAK VC, SANES DH. Cortical synaptic inhibition declines during auditory learning. J Neurosci. 2015;35:6318–6325. doi: 10.1523/JNEUROSCI.4051-14.2015. PubMed DOI PMC

SCHREINER CE, POLLEY DB. Auditory map plasticity: diversity in causes and consequences. Curr Opin Neurobiol. 2014;24:143–156. doi: 10.1016/j.conb.2013.11.009. PubMed DOI PMC

SHEPARD KN, CHONG KK, LIU RC. Contrast enhancement without transient map expansion for species-specific vocalizations in core auditory cortex during learning. eNeuro. 2016;3:1–13. doi: 10.1523/ENEURO.0318-16.2016. PubMed DOI PMC

SVOBODA K, YASUDA R. Principles of two-photon excitation microscopy and its applications to neuroscience. Neuron. 2006;50:823–839. doi: 10.1016/j.neuron.2006.05.019. PubMed DOI

SYKA J. Plastic changes in the central auditory system after hearing loss, restoration of function, and during learning. Physiol Rev. 2002;82:601–636. doi: 10.1152/physrev.00002.2002. PubMed DOI

TAKEMOTO M, SONG WJ. Cue-dependent safety and fear learning in a discriminative auditory fear conditioning paradigm in the mouse. Learn Mem. 2019;26:284–290. doi: 10.1101/lm.049577.119. PubMed DOI PMC

TOMEK J, NOVAK O, SYKA J. Two-Photon Processor and SeNeCA: a freely available software package to process data from two-photon calcium imaging at speeds down to several milliseconds per frame. J Neurophysiol. 2013;110:243–256. doi: 10.1152/jn.00087.2013. PubMed DOI

TREMBLAY R, LEE S, RUDY B. GABAergic Interneurons in the neocortex: from cellular properties to circuits. Neuron. 2016;91:260–292. doi: 10.1016/j.neuron.2016.06.033. PubMed DOI PMC

WEINBERGER NM. Associative representational plasticity in the auditory cortex: A synthesis of two disciplines. Learn Mem. 2007;14:1–16. doi: 10.1101/lm.421807. PubMed DOI PMC

WINKOWSKI DE, BANDYOPADHYAY S, SHAMMA SA, KANOLD PO. Frontal cortex activation causes rapid plasticity of auditory cortical processing. J Neurosci. 2013;33:18134–18148. doi: 10.1523/JNEUROSCI.0180-13.2013. PubMed DOI PMC

YIN PB, FRITZ JB, SHAMMA SA. Rapid spectrotemporal plasticity in primary auditory cortex during behavior. J Neurosci. 2014;34:4396–4408. doi: 10.1523/JNEUROSCI.2799-13.2014. PubMed DOI PMC

ZHANG SY, XU M, KAMIGAKI T, DO JPH, CHANG W-C, JENWAY S, MIYAMICHI K, LUOL, DAN Y. Long-range and local circuits for top-down modulation of visual cortex processing. Science. 2014;345:660–665. doi: 10.1126/science.1254126. PubMed DOI PMC

Climbing Fiber Activation Induced by Footshock in the Cerebellar Vermis Lobule IV/V of Freely Moving Mice