Abstract

The organization in the primary auditory cortex (Au1) is critical to the basic function of auditory information processing and integration. However, recent mapping experiments using in vivo two-photon imaging with different Ca2+ indicators have reached controversial conclusions on this topic, possibly because of the different sensitivities and properties of the indicators used. Therefore, it is essential to identify a reliable Ca2+ indicator for use in in vivo functional imaging of the Au1, to understand its functional organization. Here, we demonstrate that a previously reported indicator, Cal-520, performs well in both anesthetized and awake conditions. Cal-520 shows a sufficient sensitivity for the detection of single action potentials, and a high signal-to-noise ratio. Cal-520 reliably reported on both spontaneous and sound-evoked neuronal activity in anesthetized and awake mice. After testing with pure tones at a range of frequencies, we confirmed the local heterogeneity of the functional organization of the mouse Au1. Therefore, Cal-520 is a reliable and useful Ca2+ indicator for in vivo functional imaging of the Au1.

© 2017 Optical Society of America

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References

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2017 (1)

J. B. Issa, B. D. Haeffele, E. D. Young, and D. T. Yue, “Multiscale mapping of frequency sweep rate in mouse auditory cortex,” Hear. Res. 344, 207–222 (2017).
[Crossref] [PubMed]

2016 (3)

A. Nelson and R. Mooney, “The basal forebrain and motor cortex provide convergent yet distinct movement-related inputs to the auditory cortex,” Neuron 90(3), 635–648 (2016).
[Crossref] [PubMed]

O. Novák, O. Zelenka, T. Hromádka, and J. Syka, “Immediate manifestation of acoustic trauma in the auditory cortex is layer specific and cell type dependent,” J. Neurophysiol. 115(4), 1860–1874 (2016).
[Crossref] [PubMed]

H. Baba, H. Tsukano, R. Hishida, K. Takahashi, A. Horii, S. Takahashi, and K. Shibuki, “Auditory cortical field coding long-lasting tonal offsets in mice,” Sci. Rep. 6(1), 34421 (2016).
[Crossref] [PubMed]

2015 (3)

S. Inayat, J. Barchini, H. Chen, L. Feng, X. Liu, and J. Cang, “Neurons in the most superficial lamina of the mouse superior colliculus are highly selective for stimulus direction,” J. Neurosci. 35(20), 7992–8003 (2015).
[Crossref] [PubMed]

S. Tsutsumi, M. Yamazaki, T. Miyazaki, M. Watanabe, K. Sakimura, M. Kano, and K. Kitamura, “Structure-function relationships between aldolase C/zebrin II expression and complex spike synchrony in the cerebellum,” J. Neurosci. 35(2), 843–852 (2015).
[Crossref] [PubMed]

J. T. Lock, I. Parker, and I. F. Smith, “A comparison of fluorescent Ca2+ indicators for imaging local Ca2+ signals in cultured cells,” Cell Calcium 58(6), 638–648 (2015).
[Crossref] [PubMed]

2014 (9)

A. Volterra, N. Liaudet, and I. Savtchouk, “Astrocyte Ca2+ signalling: an unexpected complexity,” Nat. Rev. Neurosci. 15(5), 327–335 (2014).
[Crossref] [PubMed]

H. Jia, Z. Varga, B. Sakmann, and A. Konnerth, “Linear integration of spine Ca2+ signals in layer 4 cortical neurons in vivo,” Proc. Natl. Acad. Sci. U.S.A. 111(25), 9277–9282 (2014).
[Crossref] [PubMed]

Y. Lou, W. Luo, G. Zhang, C. Tao, P. Chen, Y. Zhou, and Y. Xiong, “Ventral tegmental area activation promotes firing precision and strength through circuit inhibition in the primary auditory cortex,” Front. Neural Circuits 8, 25 (2014).
[Crossref] [PubMed]

J. B. Issa, B. D. Haeffele, A. Agarwal, D. E. Bergles, E. D. Young, and D. T. Yue, “Multiscale optical Ca2+ imaging of tonal organization in mouse auditory cortex,” Neuron 83(4), 944–959 (2014).
[Crossref] [PubMed]

D. F. Aschauer and S. Rumpel, “Measuring the functional organization of the neocortex at large and small scales,” Neuron 83(4), 756–758 (2014).
[Crossref] [PubMed]

P. O. Kanold, I. Nelken, and D. B. Polley, “Local versus global scales of organization in auditory cortex,” Trends Neurosci. 37(9), 502–510 (2014).
[Crossref] [PubMed]

M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
[Crossref] [PubMed]

B. M. Krause, A. Raz, D. J. Uhlrich, P. H. Smith, and M. I. Banks, “Spiking in auditory cortex following thalamic stimulation is dominated by cortical network activity,” Front. Syst. Neurosci. 8, 170 (2014).
[Crossref] [PubMed]

T. Rose, P. M. Goltstein, R. Portugues, and O. Griesbeck, “Putting a finishing touch on GECIs,” Front. Mol. Neurosci. 7, 88 (2014).
[Crossref] [PubMed]

2013 (6)

Y. Honma, H. Tsukano, M. Horie, S. Ohshima, M. Tohmi, Y. Kubota, K. Takahashi, R. Hishida, S. Takahashi, and K. Shibuki, “Auditory cortical areas activated by slow frequency-modulated sounds in mice,” PLoS One 8(7), e68113 (2013).
[Crossref] [PubMed]

T. W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

X. Chen, N. L. Rochefort, B. Sakmann, and A. Konnerth, “Reactivation of the same synapses during spontaneous up states and sensory stimuli,” Cell Reports 4(1), 31–39 (2013).
[Crossref] [PubMed]

G. Rothschild, L. Cohen, A. Mizrahi, and I. Nelken, “Elevated correlations in neuronal ensembles of mouse auditory cortex following parturition,” J. Neurosci. 33(31), 12851–12861 (2013).
[Crossref] [PubMed]

C. C. Petersen and S. Crochet, “Synaptic computation and sensory processing in neocortical layer 2/3,” Neuron 78(1), 28–48 (2013).
[Crossref] [PubMed]

I. T. Bayazitov, J. J. Westmoreland, and S. S. Zakharenko, “Forward suppression in the auditory cortex is caused by the Ca(v)3.1 calcium channel-mediated switch from bursting to tonic firing at thalamocortical projections,” J. Neurosci. 33(48), 18940–18950 (2013).
[Crossref] [PubMed]

2012 (5)

B. Haider, M. Häusser, and M. Carandini, “Inhibition dominates sensory responses in the awake cortex,” Nature 493(7430), 97–100 (2012).
[Crossref] [PubMed]

B. Bathellier, L. Ushakova, and S. Rumpel, “Discrete neocortical dynamics predict behavioral categorization of sounds,” Neuron 76(2), 435–449 (2012).
[Crossref] [PubMed]

C. Grienberger and A. Konnerth, “Imaging calcium in neurons,” Neuron 73(5), 862–885 (2012).
[Crossref] [PubMed]

X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
[Crossref] [PubMed]

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP calcium indicator for neural activity imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
[Crossref] [PubMed]

2011 (2)

X. Chen, U. Leischner, N. L. Rochefort, I. Nelken, and A. Konnerth, “Functional mapping of single spines in cortical neurons in vivo,” Nature 475(7357), 501–505 (2011).
[Crossref] [PubMed]

N. Kuga, T. Sasaki, Y. Takahara, N. Matsuki, and Y. Ikegaya, “Large-scale calcium waves traveling through astrocytic networks in vivo,” J. Neurosci. 31(7), 2607–2614 (2011).
[Crossref] [PubMed]

2010 (5)

S. Bandyopadhyay, S. A. Shamma, and P. O. Kanold, “Dichotomy of functional organization in the mouse auditory cortex,” Nat. Neurosci. 13(3), 361–368 (2010).
[Crossref] [PubMed]

G. Rothschild, I. Nelken, and A. Mizrahi, “Functional organization and population dynamics in the mouse primary auditory cortex,” Nat. Neurosci. 13(3), 353–360 (2010).
[Crossref] [PubMed]

H. Jia, N. L. Rochefort, X. Chen, and A. Konnerth, “Dendritic organization of sensory input to cortical neurons in vivo,” Nature 464(7293), 1307–1312 (2010).
[Crossref] [PubMed]

X. Chen, Y. Kovalchuk, H. Adelsberger, H. A. Henning, M. Sausbier, G. Wietzorrek, P. Ruth, Y. Yarom, and A. Konnerth, “Disruption of the olivo-cerebellar circuit by Purkinje neuron-specific ablation of BK channels,” Proc. Natl. Acad. Sci. U.S.A. 107(27), 12323–12328 (2010).
[Crossref] [PubMed]

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

2009 (3)

P. Golshani, J. T. Gonçalves, S. Khoshkhoo, R. Mostany, S. Smirnakis, and C. Portera-Cailliau, “Internally mediated developmental desynchronization of neocortical network activity,” J. Neurosci. 29(35), 10890–10899 (2009).
[Crossref] [PubMed]

R. J. Richardson, J. A. Blundon, I. T. Bayazitov, and S. S. Zakharenko, “Connectivity patterns revealed by mapping of active inputs on dendrites of thalamorecipient neurons in the auditory cortex,” J. Neurosci. 29(20), 6406–6417 (2009).
[Crossref] [PubMed]

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[Crossref] [PubMed]

2008 (4)

R. M. Paredes, J. C. Etzler, L. T. Watts, W. Zheng, and J. D. Lechleiter, “Chemical calcium indicators,” Methods 46(3), 143–151 (2008).
[Crossref] [PubMed]

C. G. Schipke, B. Haas, and H. Kettenmann, “Astrocytes discriminate and selectively respond to the activity of a subpopulation of neurons within the barrel cortex,” Cereb. Cortex 18(10), 2450–2459 (2008).
[Crossref] [PubMed]

T. Hromádka, M. R. Deweese, and A. M. Zador, “Sparse representation of sounds in the unanesthetized auditory cortex,” PLoS Biol. 6(1), e16 (2008).
[Crossref] [PubMed]

M. T. Alkire, A. G. Hudetz, and G. Tononi, “Consciousness and anesthesia,” Science 322(5903), 876–880 (2008).
[Crossref] [PubMed]

2007 (3)

T. R. Sato, N. W. Gray, Z. F. Mainen, and K. Svoboda, “The functional microarchitecture of the mouse barrel cortex,” PLoS Biol. 5(7), e189 (2007).
[Crossref] [PubMed]

V. C. Kotak, M. Sadahiro, and C. P. Fall, “Developmental expression of endogenous oscillations and waves in the auditory cortex involves calcium, gap junctions, and GABA,” Neuroscience 146(4), 1629–1639 (2007).
[Crossref] [PubMed]

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2006 (1)

O. Garaschuk, R. I. Milos, and A. Konnerth, “Targeted bulk-loading of fluorescent indicators for two-photon brain imaging in vivo,” Nat. Protoc. 1(1), 380–386 (2006).
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2005 (1)

X. Wang, T. Lu, R. K. Snider, and L. Liang, “Sustained firing in auditory cortex evoked by preferred stimuli,” Nature 435(7040), 341–346 (2005).
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H. Hirase, L. Qian, P. Barthó, and G. Buzsáki, “Calcium dynamics of cortical astrocytic networks in vivo,” PLoS Biol. 2(4), e96 (2004).
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C. Stosiek, O. Garaschuk, K. Holthoff, and A. Konnerth, “In vivo two-photon calcium imaging of neuronal networks,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7319–7324 (2003).
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H. Hirase, L. Qian, P. Barthó, and G. Buzsáki, “Calcium dynamics of cortical astrocytic networks in vivo,” PLoS Biol. 2(4), e96 (2004).
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G. Rothschild, I. Nelken, and A. Mizrahi, “Functional organization and population dynamics in the mouse primary auditory cortex,” Nat. Neurosci. 13(3), 353–360 (2010).
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Nat. Protoc. (2)

X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
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O. Garaschuk, R. I. Milos, and A. Konnerth, “Targeted bulk-loading of fluorescent indicators for two-photon brain imaging in vivo,” Nat. Protoc. 1(1), 380–386 (2006).
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Nat. Rev. Neurosci. (1)

A. Volterra, N. Liaudet, and I. Savtchouk, “Astrocyte Ca2+ signalling: an unexpected complexity,” Nat. Rev. Neurosci. 15(5), 327–335 (2014).
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Nature (5)

X. Wang, T. Lu, R. K. Snider, and L. Liang, “Sustained firing in auditory cortex evoked by preferred stimuli,” Nature 435(7040), 341–346 (2005).
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T. W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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H. Jia, N. L. Rochefort, X. Chen, and A. Konnerth, “Dendritic organization of sensory input to cortical neurons in vivo,” Nature 464(7293), 1307–1312 (2010).
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B. Haider, M. Häusser, and M. Carandini, “Inhibition dominates sensory responses in the awake cortex,” Nature 493(7430), 97–100 (2012).
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X. Chen, U. Leischner, N. L. Rochefort, I. Nelken, and A. Konnerth, “Functional mapping of single spines in cortical neurons in vivo,” Nature 475(7357), 501–505 (2011).
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Neuron (6)

C. Grienberger and A. Konnerth, “Imaging calcium in neurons,” Neuron 73(5), 862–885 (2012).
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B. Bathellier, L. Ushakova, and S. Rumpel, “Discrete neocortical dynamics predict behavioral categorization of sounds,” Neuron 76(2), 435–449 (2012).
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J. B. Issa, B. D. Haeffele, A. Agarwal, D. E. Bergles, E. D. Young, and D. T. Yue, “Multiscale optical Ca2+ imaging of tonal organization in mouse auditory cortex,” Neuron 83(4), 944–959 (2014).
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A. Nelson and R. Mooney, “The basal forebrain and motor cortex provide convergent yet distinct movement-related inputs to the auditory cortex,” Neuron 90(3), 635–648 (2016).
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C. C. Petersen and S. Crochet, “Synaptic computation and sensory processing in neocortical layer 2/3,” Neuron 78(1), 28–48 (2013).
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Neuroscience (1)

V. C. Kotak, M. Sadahiro, and C. P. Fall, “Developmental expression of endogenous oscillations and waves in the auditory cortex involves calcium, gap junctions, and GABA,” Neuroscience 146(4), 1629–1639 (2007).
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PLoS Biol. (3)

T. R. Sato, N. W. Gray, Z. F. Mainen, and K. Svoboda, “The functional microarchitecture of the mouse barrel cortex,” PLoS Biol. 5(7), e189 (2007).
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T. Hromádka, M. R. Deweese, and A. M. Zador, “Sparse representation of sounds in the unanesthetized auditory cortex,” PLoS Biol. 6(1), e16 (2008).
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H. Hirase, L. Qian, P. Barthó, and G. Buzsáki, “Calcium dynamics of cortical astrocytic networks in vivo,” PLoS Biol. 2(4), e96 (2004).
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PLoS One (1)

Y. Honma, H. Tsukano, M. Horie, S. Ohshima, M. Tohmi, Y. Kubota, K. Takahashi, R. Hishida, S. Takahashi, and K. Shibuki, “Auditory cortical areas activated by slow frequency-modulated sounds in mice,” PLoS One 8(7), e68113 (2013).
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Proc. Natl. Acad. Sci. U.S.A. (3)

C. Stosiek, O. Garaschuk, K. Holthoff, and A. Konnerth, “In vivo two-photon calcium imaging of neuronal networks,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7319–7324 (2003).
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H. Jia, Z. Varga, B. Sakmann, and A. Konnerth, “Linear integration of spine Ca2+ signals in layer 4 cortical neurons in vivo,” Proc. Natl. Acad. Sci. U.S.A. 111(25), 9277–9282 (2014).
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X. Chen, Y. Kovalchuk, H. Adelsberger, H. A. Henning, M. Sausbier, G. Wietzorrek, P. Ruth, Y. Yarom, and A. Konnerth, “Disruption of the olivo-cerebellar circuit by Purkinje neuron-specific ablation of BK channels,” Proc. Natl. Acad. Sci. U.S.A. 107(27), 12323–12328 (2010).
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Sci. Rep. (1)

H. Baba, H. Tsukano, R. Hishida, K. Takahashi, A. Horii, S. Takahashi, and K. Shibuki, “Auditory cortical field coding long-lasting tonal offsets in mice,” Sci. Rep. 6(1), 34421 (2016).
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Science (1)

M. T. Alkire, A. G. Hudetz, and G. Tononi, “Consciousness and anesthesia,” Science 322(5903), 876–880 (2008).
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Trends Neurosci. (1)

P. O. Kanold, I. Nelken, and D. B. Polley, “Local versus global scales of organization in auditory cortex,” Trends Neurosci. 37(9), 502–510 (2014).
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Figures (5)

Fig. 1
Fig. 1 Two-photon Ca2+ imaging of the Au1 in vivo by using Cal-520 AM. (A) Schematic demonstrating the protocol for loading Cal-520 AM into the mouse Au1. (B) A merged image showing Au1 L2/3 neurons stained with Cal-520 AM in green and glial cells stained with both Cal-520 AM and sulforhodamine 101 (SR101, red) in yellow. (C) Simultaneous cell-attached recording and two-photon Ca2+ imaging. The glass electrode is indicated by yellow dashed lines. (D) Ca2+ transients (lower) and their corresponding action potentials (upper) from the neuron are indicated in panel C. The numbers of action potentials are indicated above the electrical trace. (E) Detection rate of Ca2+ transients for different numbers of action potentials (n = 6 neurons). The time window of detection was 200 ms. Error bars represent SEM.
Fig. 2
Fig. 2 Spontaneous and sound-evoked responses of Au1 neurons in anesthetized mice. (A) Two-photon image of Cal-520 AM-labeled neurons at a depth of 258 µm from the pial surface in an anesthetized mouse. (B) No contamination of somatic Ca2+ signals of neurons by nearby neuropil. Data were from 15 neurons and their corresponding 15 adjacent neuropil region (3 mice). Upper panel, 52 traces from neurons and neuropil were superimposed. Lower panel, 79 traces from neurons and neuropil were superimposed. Each Ca2+ trace was selected from the period when either neurons showed Ca2+ signals (upper) or neuropil showed Ca2+ signals (lower). The traces were aligned to the onset of the Ca2+ signals. (C) Spontaneous (left) and sound-evoked responses (right) of five neurons as indicated in panel A. The vertical gray bars denote sound stimuli. (D) Distribution of the spontaneous response frequency (left) and success rate for evoked responses to sound stimulation including broadband noise and pure tones (broadband noise, n = 486 neurons from 4 mice, pure tone, n = 777 neurons from 8 mice).
Fig. 3
Fig. 3 Whole-cell patch-clamp recordings in Au1 neurons in awake mice. (A) (A and B) Two example neurons from two different awake mice. Left, whole-cell recording . Right, distribution of the membrane potential (binned at 0.5 ms) from the corresponding neuron shown in the left panel.
Fig. 4
Fig. 4 Spontaneous and broadband noise-evoked responses of Au1 neurons in awake mice. (A) Two-photon image of Cal-520 AM-labeled neurons at a depth of 227 µm from the pial surface in an awake mouse. (B) Spontaneous activation (left) and sound-evoked responses (right) of five neurons as indicated in panel A. The vertical gray bars denote sound stimuli. (C) Distribution of spontaneous response frequency (left) and success rate for evoked responses to broadband noise (n = 855 neurons from 8 mice).
Fig. 5
Fig. 5 Pure tone-evoked responses of Au1 neurons in both anesthetized and awake mice. (A) Two-photon image of Cal-520 AM-labeled L2/3 neurons in an anesthetized mouse. (B) Pure tone-evoked Ca2+ transients (average of 20 trials) in two example neurons indicated in panel A. Eleven pure tones were presented. Each frequency was applied 20 times. (C) Frequency tuning curves of the two neurons in panel A and B. Data points are the mean integrals of the Ca2+ responses (fitted with a Gaussian function). (D) The normalized and aligned frequency tuning curve of 361 neurons from anesthetized mice (left) and 194 neurons from awake mice (right). (E and G) Spatial distribution of responsive neurons to pure tones in two example imaged fields from two anesthetized (E) and two awake mice (G). The frequencies are shown on the right side of panel G. (F and H) Left: Distribution of the Δbest frequency of imaged neurons as the function of their spatial distance in the anesthetized condition (F) or awake condition (H); Right: Distance distribution of the neuron pairs whose Δbest frequency is less than one octave in anesthetized mice (F) or awake mice (H). (I and J) Left: Distribution of the Δbest frequency of imaged neurons as the function of their spatial distance at sound intensity of −20 dB (I) or −40 dB (J); Right: Distance distribution of the neuron pairs whose Δbest frequency is less than one octave at sound intensity of −20 dB (I) or −40 dB (J) (n = 361 neurons, 6 anesthetized mice).

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