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Long-latency optical responses from the dorsal inferior colliculus of Seba’s fruit bat

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Abstract

We used a novel microendoscope system to record simultaneously optical activity (fluorescence of a calcium indicator dye) and electrical activity (multi-unit activity and local field potentials) from the dorsal inferior colliculus of the echolocating bat, Carollia perspicillata. Optically recorded calcium responses to wide-band noise and to frequency-modulated bursts were recorded at probe depths down to 1300 µm, with the majority of active sites encountered at more shallow depths down to 800 µm. Calcium activity exhibited long latencies, within the time span of 50–100 ms after stimulus onset, significantly longer than onset latencies of either multi-unit activity or local field potentials. Latencies and amplitude/latency trading of these electrical responses were consistent with those seen in standard electrophysiological recordings, confirming that the microendoscope was able to record both neural and optical activity successfully. Optically recorded calcium responses rose and decayed slowly and were correlated in time with long-latency negative deflections in local field potentials. These data suggest that calcium-evoked responses may reflect known, sustained inhibitory interactions in the inferior colliculus.

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Abbreviations

ANOVA:

Analysis of variance

F b :

Baseline fluorescence

F m :

Post-stimulus fluorescence

ΔF/F :

Fluorescence change from baseline

FM:

Frequency-modulated

GLM:

General linear model

IC:

Inferior colliculus

LFP:

Local field potential

MUA:

Multi-unit activity

OGB:

Oregon green BAPTA

WBN:

Wide-band noise

References

  • Bandyopadhyay S, Shamma SA, Kanold PO (2010) Dichotomy of functional organization in the mouse auditory cortex. Nat Neurosci 13:361–368

    Article  CAS  Google Scholar 

  • Beetz MJ, Kordes S, García-Rosales F, Kössl M, Hechavarría JC (2017) Processing of natural echolocation sequences in the inferior colliculus of Seba’s fruit eating bat, Carollia perspicillata. eNeuro 4:0314–0317. https://doi.org/10.1523/ENEURO.0314-17.2017

    Article  Google Scholar 

  • Carter M, Casseday JH, Covey E (2004) A stereotactic brain atlas of the big brown bat, Eptesicus fuscus. University of Washington, Seattle

    Google Scholar 

  • Covey E, Casseday JH (1999) Timing in the auditory system of the bat. Ann Rev Physiol 61:457–476

    Article  CAS  Google Scholar 

  • Ferragamo MJ, Haresign T, Simmons JA (1998) Frequency tuning, latencies, and responses to FM sweeps in the inferior colliculus of the echolocating bat, Eptesicus fuscus. J Comp Physiol A 182:65–79

    Article  CAS  Google Scholar 

  • Flusberg BA, Cocker ED, Piyawattanametha W, Jung JC, Cheung EL, Schnitzer MJ (2005) Fiber-optic fluorescence imaging. Nat Methods 2:941–950

    Article  CAS  Google Scholar 

  • Goto A, Nakahara I, Yamaguchi T, Kamioka Y, Sumiyama K, Matsuda M, Nakanishi S, Funabiki K (2015) Circuit-dependent striatal PKA and ERK signaling underlies rapid behavioral shift in mating reaction of male mice. Proc Natl Acad Sci USA 112:6718–6723

    Article  CAS  Google Scholar 

  • Griffin DR (1958) Listening in the dark: The acoustic orientation of bats and men. Yale University Press, New Haven

    Google Scholar 

  • Haplea S, Covey E, Casseday JH (1994) Frequency tuning and response latencies at three levels in the brainstem of the echolocating bat, Eptesicus fuscus. J Comp Physiol A 174:671–683

    Article  CAS  Google Scholar 

  • Hayashi Y, Tagawa Y, Yawata S, Nakanishi S, Funabiki K (2012) Spatio-temporal control of neural activity in vivo using fluorescence microendoscopy. Eur J Neurosci 36:2722–2732

    Article  Google Scholar 

  • Ikegaya Y, Bon-Jego ML, Yuste R (2005) Large-scale imaging of cortical network activity with calcium indicators. Neurosci Res 52:132–138

    Article  CAS  Google Scholar 

  • Jen PHS, Feng RB (1999) Bicuculline application affects discharge pattern and pulse-duration tuning characteristics of bat inferior collicular neurons. J Comp Physiol 184:185–194

    Article  CAS  Google Scholar 

  • Klug A, Khan A, Burger RM, Bauer EE, Hurley LM, Yang L, Grothe B, Halvorsen MB, Park TJ (2000) Latency as a function of intensity in auditory neurons: influences of central processing. Hear Res 148:107–123

    Article  CAS  Google Scholar 

  • Kössl M, Hechavarría J, Voss C, Schaeffer M, Vater M (2015) Bat auditory cortex—Model for general mammalian auditory computation or special design solution for active time perception? Eur J Neurosci 41(5):518–532

    Article  Google Scholar 

  • Lu Y, Jen PHS (2001) GABAergic and glycinergic neural inhibition in excitatory frequency tuning of bat inferior collicular neurons. Exp Brain Res 141:331–339

    Article  CAS  Google Scholar 

  • Lu Y, Jen PHS, Zheng QY (1997) GABA-ergic disinhibition changes the recovery cycle of bat inferior collicular neurons. J Comp Physiol A 181(4):331–341

    Article  CAS  Google Scholar 

  • Ma X, Suga N (2008) Corticofugal modulation of the paradoxical latency shifts of inferior collicular neurons. J Neurophysiol 100:1127–1134

    Article  Google Scholar 

  • Moreaux L, Laurent G (2007) Estimating firing rates from calcium signals in locust projection neurons in vivo. Front Neural Circuits 1:1–13. https://doi.org/10.3389/neuro.04.002.2007

    Article  Google Scholar 

  • Nimmerjahn A, Mukamel EA, Schnitzer MJ (2009) Motor behavior activates Bergmann glial networks. Neuron 62:400–412

    Article  CAS  Google Scholar 

  • Park TJ, Pollak GD (1993) GABA shapes a topographic organization of response latency in the mustache bat’s inferior colliculus. J Neurosci 13:5172–5187

    Article  CAS  Google Scholar 

  • Pollak GD (1988) Time is traded for intensity in the bat’s auditory system. Hear Res 36:107–124

    Article  CAS  Google Scholar 

  • Pollak GD, Casseday JH (1989) The neural basis of echolocation in bats. Springer, New York

    Book  Google Scholar 

  • Sanderson MI, Simmons JA (2000) Neural responses to overlapping FM sounds in the inferior colliculus of echolocating bats. J Neurophysiol 83:1840–1855

    Article  CAS  Google Scholar 

  • Sanderson MI, Simmons JA (2005) Target representation for naturalistic echolocation sequences in single unit responses from the inferior colliculus of big brown bats. J Acoust Soc Am 118:3352–3361

    Article  Google Scholar 

  • Simmons JA (2012) Bats use a neuronally implemented computational acoustic model to form sonar images. Curr Opin Neurobiol 22:311–319

    Article  CAS  Google Scholar 

  • Simmons JA (2014) Temporal binding of neural responses for focused attention in biosonar. J Exp Biol 217:2834–2843

    Article  Google Scholar 

  • Stosiek C, Garaschuk O, Holthoff K, Konnerth A (2003) In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci USA 100:7319–7324

    Article  CAS  Google Scholar 

  • Suga N (2015) Neural processing of auditory signals in the time domain: delay-tuned coincidence detectors in the mustached bat. Hear Res 324:19–36

    Article  Google Scholar 

  • Thies W, Kalko EKV, Schnitzler HU (1998) The roles of echolocation and olfaction in two Neotropical fruit-eating bats, Carollia perspicillata and C. castanea, feeding on Piper. Behav Ecol Sociobiol 42:397–409

    Article  Google Scholar 

  • Tsien RY (1980) New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 19:2396–2404

    Article  CAS  Google Scholar 

  • Vincent P, Maskos U, Charvet I, Bourgeais L, Stoppini L, Leresche N, Changeux JP, Lambert R, Meda P, Paupardin-Tritsch D (2006) Live imaging of neural structure and function by fibred fluorescence microscopy. EMBO Rep 7:1154–1161

    Article  CAS  Google Scholar 

  • Yashiro H, Funabiki K, Simmons AM, Simmons JA, Riquimaroux H (2016) Functional optical imaging from bat inferior colliculus using a micro-endoscope. Proc Mtgs Acoust 29:010003. https://doi.org/10.1121/2.0000403

    Article  Google Scholar 

  • Yashiro H, Nakahara I, Funabiki K, Riquimaroux H (2017) Micro-endoscopic system for functional assessment of neural circuits in deep brain regions: simultaneous optical and electrical recordings of auditory responses in mouse’s inferior colliculus. Neurosci Res 119:61–69

    Article  Google Scholar 

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Acknowledgements

We thank SM Swartz for providing fruit bats and P Polanco for assistance with data analysis.

Funding

US Office of Naval Research (grant # N00014-14-1-05880 to JAS, grant # N00014-17-1-2736 to JAS and AMS); Japan Society for the Promotion of Science KAKENHI (grant # 15J04434 to HY).

Author information

Authors and Affiliations

  1. Department of Neuroscience, Brown University, 185 Meeting St, Providence, RI, 02912, USA

    James A. Simmons, Abigail L. Kohler, Hiroshi Riquimaroux & Andrea Megela Simmons

  2. Graduate School of Life and Medical Sciences, Doshisha University, 1-3, Miyakodani, Tatara, Kyotanabe, Kyoto, 610-0321, Japan

    Hidetaka Yashiro

  3. Shandong University, Jinan, 250100, China

    Hiroshi Riquimaroux

  4. National Hospital Organization Tokyo Medical Center, Tokyo, 152-8902, Japan

    Hiroshi Riquimaroux

  5. Institute of Biomedical Research and Innovation, Foundation for Biomedical Research and Innovation, Kobe, 650-0047, Japan

    Kazuo Funabiki

  6. Center for Life Science and Technology, Kobe, Japan

    Kazuo Funabiki

  7. Department of Cognitive, Linguistic, and Psychological Sciences, Brown University, Providence, RI, 02912, USA

    Andrea Megela Simmons

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  1. James A. Simmons
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  2. Hidetaka Yashiro
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  3. Abigail L. Kohler
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  4. Hiroshi Riquimaroux
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  5. Kazuo Funabiki
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  6. Andrea Megela Simmons
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Contributions

JAS, HY, KF, HR, AMS designed research; JAS, HY performed research; HY, AK, AMS analyzed data; KF, AMS, JAS provided equipment; JAS, AMS provided space and funding; JAS, AMS wrote manuscript; all authors edited and approved the manuscript.

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Correspondence to James A. Simmons.

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Simmons, J.A., Yashiro, H., Kohler, A.L. et al. Long-latency optical responses from the dorsal inferior colliculus of Seba’s fruit bat. J Comp Physiol A 206, 831–844 (2020). https://doi.org/10.1007/s00359-020-01441-7

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  • DOI: https://doi.org/10.1007/s00359-020-01441-7

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