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Design principles of sensory processing in cerebellum-like structures

Early stage processing of electrosensory and auditory objects

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Abstract

Cerebellum-like structures are compared for two sensory systems: electrosensory and auditory. The electrosensory lateral line lobe of mormyrid electric fish is reviewed and the neural representation of electrosensory objects in this structure is modeled and discussed. The dorsal cochlear nucleus in the auditory brainstem of mammals is reviewed and new data are presented that characterize the responses of neurons in this structure in the mouse. Similarities between the electrosensory and auditory cerebellum-like structures are shown, in particular adaptive processes that may reduce responses to predictable stimuli. We suggest that the differences in the types of sensory objects may drive the differences in the anatomical and physiological characteristics of these two cerebellum-like structures.

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References

  • Abbott LF, Nelson SB (2000) Synaptic plasticity: taming the beast. Nature Neurosci 3(Suppl): 1178–183

    PubMed  Google Scholar 

  • Albus JS (1971) A theory of cerebellar function. Math Biosci 10: 25–1

    Google Scholar 

  • Bastian J (1996) Plasticity in an electrosensory system. II. Postsynaptic events associated with a dynamic sensory filter. J Neurophysiol 76: 2497–507

    PubMed  Google Scholar 

  • Bell CC (1981) An efference copy in electric fish. Science 214: 450–53

    PubMed  Google Scholar 

  • Bell CC (1989) Sensory coding and corollary discharge effects in mormyrid electric fish. J Exp Biol 146: 229–53

    PubMed  Google Scholar 

  • Bell CC, Grant K, Serrier J (1992) Sensory processing and corollary discharge effects in the mormyromast regions of the mormyrid electrosensory lobe: I. Field potentials and cellular activity in associated structures. J Neurophysiol 68: 843–58

    PubMed  Google Scholar 

  • Bell CC, Caputi A, Grant K, Serrier J (1993) Storage of a sensory pattern by anti-Hebbian synaptic plasticity in an electric fish. Proc Natl Acad Sci USA 90: 4650–654

    PubMed  Google Scholar 

  • Bell CC, Bodznick D, Montgomery J, Bastian J (1997b) The generation and subtraction of sensory expectations within cerebellum-like structures. Brain Beh Evol 50(Suppl. 1): 17–1

    Google Scholar 

  • Bell CC, Han V, Sugawara Y, Grant K (1997b) Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387: 278–81

    PubMed  Google Scholar 

  • Beroukha A, Gruen E, Woody CD (1998) Facilitation of acoustic responses of cartwheel neurons of the cat dorsal cochlear nucleus. Neuroreport 9(15): 3457–461

    PubMed  Google Scholar 

  • Berrebi AS, Mugnaini E (1991) Distribution and targets of the cartwheel cell axon in the dorsal cochlear nucleus of the guinea pig. Anat Embryol (Berl) 183(5): 427–54

    Google Scholar 

  • Blum JJ, Reed MC (1998) Effects of wide band inhibitors in the dorsal cochlear nucleus. ii. model calculations of the responses to complex sounds. J Acoust Soc Am 103(4): 2000–009

    PubMed  Google Scholar 

  • Bodznick D, Montgomery JC, Bradley DJ (1992) Suppression of common mode signals within the electrosensory system of the little skate Raja erinacea. J Exp Biol 171: 107–25

    Google Scholar 

  • Brown EN, Barbieri R, Ventura V, Kass RE, Frank LM (2002) The time-rescaling theorem and its application to neural spike train data analysis. Neural Comput 14(2): 325–46

    PubMed  Google Scholar 

  • Brown M, Berglund A, Kiang N, Ryugo D (1988) Central trajectories of type ii spiral ganglion neurons. J Comp Neurol 278: 581–90

    PubMed  Google Scholar 

  • Caicedo A, Herbert H (1993) Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat. J Comp Neurol 328: 377–92

    PubMed  Google Scholar 

  • Caputi AA, Budelli R (2006) Peripheral electrosensory imaging by weakly electric fish. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 192(6): 587–00

    PubMed  Google Scholar 

  • Caputi AA, Budelli R, Grant K, Bell CC (1998) The electric image in weakly electric fish: physical images of resistive objects in gnathonemus petersii. J Exp Biol 201: 2115–128

    PubMed  Google Scholar 

  • Carney LH (1993) A model for the responses of low-frequency auditory-nerve fibers in cat. J Acoust Soc Am 93(1): 401–17

    PubMed  Google Scholar 

  • Chen C, Thompson RF (1995) Temporal specificity of long-term depression in parallel fiber-Purkinje synapses in rat cerebellar slices. Learn Memory 2: 185–98

    Google Scholar 

  • Coesmans M, Weber JT, Zeeuw CID, Hansel C (2004) Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron 44(4): 691–00

    PubMed  Google Scholar 

  • Crick F (1984) Function of the thalamic reticular complex: the searchlight hypothesis. Proc Natl Acad Sci USA 81: 4586–590

    PubMed  Google Scholar 

  • Davis KA, Gdowski GT, Voigt HF (1995) A statistically based method to generate response maps objectively. Journal of Neuroscience Methods 57(1): 107–18

    PubMed  Google Scholar 

  • Davis KA, Ding J, Benson TE, Voigt HF (1996a) Response properties of units in the dorsal cochlear nucleus of unanesthetized decerebrate gerbil. J Neurophysiol 75(4): 1411–431

    PubMed  Google Scholar 

  • Davis KA, Miller RL, Young ED (1996b) Effects of somatosensory and parallel-fiber stimulation on neurons in dorsal cochlear nucleus. J Neurophysiol 76(5): 3012–024

    PubMed  Google Scholar 

  • Ding J, Benson TE, Voigt HF (1999) Acoustic and Current-Pulse Responses of Identified Neurons in the Dorsal Cochlear Nucleus of Unanesthetized, Decerebrate Gerbils. J Neurophysiol 82(6): 3434–457

    PubMed  Google Scholar 

  • Emde G, Schwarz S, Gomez L, Budelli R, Grant K (1998) Electric fish measure distance in the dark. Nature 395(6705): 890–94

    PubMed  Google Scholar 

  • Evans E, Nelson P (1973) The responses of single neurones in the cochlear nucleus of the cat as a function of their location and the anaesthetic state. Exp Brain Res 17: 402–27

    PubMed  Google Scholar 

  • Franosch JM, Kempter R, Fastl H, van Hemmen JL (2003) Zwicker tone illusion and noise reduction in the auditory system. Phys Rev Lett 90(17):178, 103

    Google Scholar 

  • Frisina RD, Walton JP, Karcich KJ (1994) Dorsal cochlear nucleus single neurons can enhance temporal processing capabilities in background noise. Exp Brain Res 102(1): 160–64

    PubMed  Google Scholar 

  • Fujino K, Oertel D (2003) Bidirectional synaptic plasticity in the cerebellum-like mammalian dorsal cochlear nucleus. Proc Natl Acad Sci USA 100(1): 265–70

    PubMed  Google Scholar 

  • Gerstner W, Ritz R, van Hemmen JL (1993) Why spikes? Hebbian learning and retrieval of time-resolved excitation patterns. Biol Cybern 69: 503–15

    PubMed  Google Scholar 

  • Godfrey D, Kiang N, Norris B (1975) Single unit activity in the dorsal cochlear nucleus of the cat. J Comp Neurol 162: 269–84

    PubMed  Google Scholar 

  • Golding N, Oertel D (1997) Physiological identification of the targets of cartwheel cells of the dorsal cochlear nucleus. J Neurophysiol 78: 248–60

    PubMed  Google Scholar 

  • Golding NL, Robertson D, Oertel D (1995) Recordings from slices indicate that octopus cells of the cochlear nucleus detect coincident firing of auditory nerve fibers with temporal precision. J Neurosci 15(4): 3138–153

    PubMed  Google Scholar 

  • Gomez L, Budelli R, Grant K, Caputi AA (2004) Pre-receptor profile of sensory images and primary afferent neuronal representation in the mormyrid electrosensory system. J Exp Biol 207(Pt 14): 2443–453

    PubMed  Google Scholar 

  • Pongstaporn T, Pongstaporn T, Doucet J, Ryugo D (2005) Projections from the spinal trigeminal nucleus to the cochlear nucleus in the rat. J Comparative Neurol 484(2): 191–05

    Google Scholar 

  • Han V, Bell CC, Grant K, Sugawara Y (1999) Mormyrid electrosensory lobe in vitro: I. Morphology of cells and circuits. J Comp Neurol 404: 359–74

    PubMed  Google Scholar 

  • Han V, Grant K, Bell CC (2000) Reversible associative depression and nonassociative potentiation at a parallel fiber synapse. Neuron 27: 611–22

    PubMed  Google Scholar 

  • Hancock KE, Voigt HF (1999) Wideband inhibition of dorsal cochlear nu- cleus type iv units in cat: a computational model. Ann Biomed Eng 27: 73–7

    PubMed  Google Scholar 

  • Harvey RJ, Napper RM (1991) Quantitative studies on the mammalian cerebellum. Prog Neurobiol 36: 437–63

    PubMed  Google Scholar 

  • Holy TE, Guo Z (2005) Ultrasonic songs of male mice. PLoS Biol 3(12): e386

    PubMed  Google Scholar 

  • Izhikevich EM (2003) Simple model of spiking neurons. IEEE Trans Neural Networks 14: 1569–572

    Google Scholar 

  • Izhikevich EM (2006) Dynamical systems in neuroscience: the geometry of excitability and bursting. MIT Press, Cambridge, MA

    Google Scholar 

  • Jenkins WM, Masterton RB (1982) Sound localization: effects of unilateral lesions in central auditory system. J Neurophysiol 47(6): 987–016

    PubMed  Google Scholar 

  • Kaltenbach J, Saunders J (1987) Spectral and temporal response patterns of single units in the chinchilla dorsal cochlear nucleus. J Exp Neurol 96: 406–19

    Google Scholar 

  • Kaltenbach JA, Meleca RJ, Falzarano PR, Myers SF, Simpson TH (1993) Forward masking properties of neurons in the dorsal cochlear nucleus: possible role in the process of echo suppression. Hear Res 67(1–): 35–4

    PubMed  Google Scholar 

  • Kanold PO, Manis PB (2001) A physiologically based model of discharge pattern regulation by transient k+ currents in cochlear nucleus pyramidal cells. J Neurophysiol 85(2): 523–38

    PubMed  Google Scholar 

  • Karachot L, Kado RT, Ito M (1994) Stimulus parameters for induction of long-term depression in in vitro rat Purkinje cells. Neurosci Res 21: 161–68

    PubMed  Google Scholar 

  • Kim Y, Trussell LO (2007) Ion channels generating complex spikes in cartwheel cells of the dorsal cochlear nucleus. J Neurophysiol 97(2): 1705–725

    PubMed  Google Scholar 

  • Lev-Ram V, Makings LR, Keitz PF, Kao JPY, Tsien RY (1995) Long-term depression in cerebellar Purkinje neurons results from coincidence of nitric oxide and depolarization-induced Ca2+ transients. Neuron 15: 407–15

    PubMed  Google Scholar 

  • Lev-Ram V, Wong ST, Storm DR, Tsien RY (2002) A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not camp. Proc Natl Acad Sci USA 99(12): 8389–393

    PubMed  Google Scholar 

  • Li H, Mizuno N (1997) Single neurons in the spinal trigeminal and dorsal column nuclei project to both the cochlear nucleus and the inferior colliculus by way of axon collaterals: a fluorescent retrograde double-labeling study in the rat. Neuroscience Research 29(2): 135–42

    PubMed  Google Scholar 

  • Linden DJ, Connor JA (1993) Cellular mechanisms of long-term depression in the cerebellum. Curr Op Neurobiol 3: 401–06

    PubMed  Google Scholar 

  • Manis PB, Spirou GA, Wright DD, Paydar S, Ryugo DK (1994) Physiology and morphology of complex spiking neurons in the guinea pig dorsal cochlear nucleus. J Comp Neurol 348(2): 261–76

    PubMed  Google Scholar 

  • Marr D (1969) A theory of cerebellar cortex. J Physiol 202: 437–70

    PubMed  Google Scholar 

  • May BJ (2000) Role of the dorsal cochlear nucleus in the sound localization behavior of cats. Hear Res 148(1–): 74–7

    PubMed  Google Scholar 

  • Medina JF, Mauk MD (2000) Computer simulation of cerebellar information processing. Nat Neurosci 3(Suppl): 1205–211

    PubMed  Google Scholar 

  • Mohr C, Roberts PD, Bell CC (2002a) Cells of the mormyrid electrosensory lobe: I. Responses to the electric organ corollary discharge and to electrosensory stimuli. J Neurophysiol 90: 1193–210

    Google Scholar 

  • Mohr C, Roberts PD, Bell CC (2002b) Cells of the mormyrid electrosensory lobe: II. Responses to input from central sources. J Neurophysiol 90: 1211–223

    Google Scholar 

  • Montgomery JC, Bodznick D (1994) An adaptive filter that cancels self-induced noise in the electrosensory and lateral line mechanosensory systems of fish. Neurosci Letters 174: 145–48

    Google Scholar 

  • Nelson ME, Paulin MG (1995) Neural simulations of adaptive reafference suppression in the elasmobranch electrosensory system. J Comp Physiol A 177: 723–36

    PubMed  Google Scholar 

  • Nelson PC, Carney LH (2004) A phenomenological model of peripheral and central neural responses to amplitude-modulated tones. J Acoust Soc Am 116(4 Pt 1): 2173–6

    PubMed  Google Scholar 

  • Oertel D, Young ED (2004) What’s a cerebellar circuit doing in the auditory system. Trends Neurosci 27: 104–10

    PubMed  Google Scholar 

  • Ohlrogge M, Doucet J, Ryugo D (2001) Projections of the pontine nuclei to the cochlear nucleus in rats. J Comp Neurol 436: 290–03

    PubMed  Google Scholar 

  • Osen K (1969) Cytoarchitecture of the cochlear nuclei in cat. J Comp Neurol 136: 453–84

    PubMed  Google Scholar 

  • Parham K, Kim DO (1995) Spontaneous and sound-evoked discharge characteristics of complex-spiking neurons in the dorsal cochlear nucleus of the unanesthetized decerebrate cat. J Neurophysiol 73(2): 550–61

    PubMed  Google Scholar 

  • Parham K, Bonaiuto G, Carlson S, Turner JG, R DW, Bross LS, Fox A, Willott JF, Kim DO (2000) Purkinje cell degeneration and control mice: responses of single units in the dorsal cochlear nucleus and the acoustic startle response. Hearing Research 148(1–): 137–52

    PubMed  Google Scholar 

  • Pfeiffer R (1966) Classification of response patterns of spike discharges for units in the cochlear nucleus: tone burst stimulation. Exp Brain Res 1: 220–35

    PubMed  Google Scholar 

  • Portfors CV, Roberts PD (2007) Temporal and frequency characteristics of cartwheel cells in the awake mouse dcn, J Neurophysiol (June 20, Epub)

  • Reiss LAJ, Young ED (2005) Spectral edge sensitivity in neural circuits of the dorsal cochlear nucleus. J Neurosci 25: 3680–691

    PubMed  Google Scholar 

  • Rhode W, Smith P, Oertel D (1983) Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat dorsal cochlear nucleus. J Comp Neurol 213: 426–47

    PubMed  Google Scholar 

  • Rhode WS, Kettner RE (1987) Physiological study of neurons in the dorsal and posteroventral cochlear nucleus of the unanesthetized cat. J Neurophysiol 57(2): 414–42

    PubMed  Google Scholar 

  • Rhode WS, Smith PH (1986) Physiological studies on neurons in the dorsal cochlear nucleus of cat. J Neurophysiol 56(2): 287–07

    PubMed  Google Scholar 

  • Roberts PD (1999) Computational consequences of temporally asymmetric learning rules: I. Differential Hebbian learning. J Comput Neurosci 7: 235–46

    PubMed  Google Scholar 

  • Roberts PD (2000) Dynamics of temporal learning rules. Phys Rev E 62: 4077–082

    Google Scholar 

  • Roberts PD (2004) Recurrent biological neural networks: The weak and noisy limit. Phys Rev E 69:031, 910

    Google Scholar 

  • Roberts PD (2005) Recurrent neural network generates a basis for sensory image cancellation. Neurocomputing 65(66): 237–42

    Google Scholar 

  • Roberts PD (2007) Stability of complex spike timing-dependent plasticity in cerebellar learning. J Comput Neurosci 22(3): 283–6

    PubMed  Google Scholar 

  • Roberts PD, Bell CC (2000) Computational consequences of temporally asymmetric learning rules: II. Sensory image cancellation. J Comput Neurosci 9: 67–3

    PubMed  Google Scholar 

  • Roberts PD, Bell CC (2002) Spike timing dependent synaptic plasticity in biological systems. Biol Cybern 87: 392–03

    PubMed  Google Scholar 

  • Roberts PD, Lafferriere G, Sawtell N, Williams A, Bell CC (2006a) Dynamic regulation of spike-timing dependent plasticity in electrosensory processing. Neurocomputing 69: 1195–198

    Google Scholar 

  • Roberts PD, Portfors CV, Sawtell N, Felix R (2006b) Model of auditory prediction in the dorsal cochlear nucleus via spike-timing dependent plasticity. Neurocomputing 69: 1191–194

    Google Scholar 

  • Rogers ME, Butler RA (1992) The linkage between stimulus frequency and covert peak areas as it relates to monaural localization. Percept Psychophys 52(5): 536–46

    PubMed  Google Scholar 

  • Ryugo D, Willard F (1985) The dorsal cochlear nucleus of the mouse: a light microscopic analysis of neurons that project to the inferior colliculus. J Comp Neurol 242: 381–96

    PubMed  Google Scholar 

  • Sawtell NB, Williams A (2008) Transformations of electrosensory encoding associated with an adaptive filter. J Neurosci 28(7): 1598–612

    PubMed  Google Scholar 

  • Sawtell NB, Williams A, Bell CC (2007) Central control of dendritic spikes shapes the responses of purkinje-like cells through spike timing-dependent synaptic plasticity. J Neurosci 27(7): 1552–565

    PubMed  Google Scholar 

  • Schofield B, Cant NB (1999) Descending auditory pathways: Projections from the inferior colliculus contact superior olivary cells that project bilaterally to the cochlear nuclei. The Journal of Comparative Neurology 409(2): 210–23

    PubMed  Google Scholar 

  • Shofner WP, Young ED (1985) Excitatory/inhibitory response types in the cochlear nucleus: relationships to discharge patterns and responses to electrical stimulation of the auditory nerve. J Neurophysiol 54(4): 917–39

    PubMed  Google Scholar 

  • Shore S, Vass Z, Wys N, Altschuler R (2000) Trigeminal ganglion innervates the auditory brainstem. J Comp Neurol 419: 271–85

    PubMed  Google Scholar 

  • Shore SE (2005) Multisensory integration in the dorsal cochlear nucleus: unit responses to acoustic and trigeminal ganglion stimulation. Eur J Neurosci 21(12): 3334–348

    PubMed  Google Scholar 

  • Smith P, Rhode W (1989) Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus. J Comp Neurol 282: 595–16

    PubMed  Google Scholar 

  • Taberner AM, Liberman MC (2005) Response properties of single auditory nerve fibers in the mouse. J Neurophysiol 93(1): 557–69

    PubMed  Google Scholar 

  • Thompson GC, Masterton RB (1978) Brain stem auditory pathways involved in reflexive head orientation to sound. J Neurophysiol 41(5): 1183–202

    PubMed  Google Scholar 

  • Tzounopoulos T, Kim Y, Oertel D, Trussell LO (2004) Cell-specific, spike timing-dependent plasticities in the dorsal cochlear nucleus. Nat Neurosci 7: 719–25

    PubMed  Google Scholar 

  • Weedman DL, Ryugo DK (1996) Projections from auditory cortex to the cochlear nucleus in rats: synapses on granule cell dendrites. J Comp Neurol 371(2): 311–24

    PubMed  Google Scholar 

  • Wickesberg RE, Oertel D (1990) Delayed, frequency-specific inhibition in the cochlear nuclei of mice: a mechanism for monaural echo suppression. J Neurosci 10(6): 1762–768

    PubMed  Google Scholar 

  • Williams A, Roberts PD, Leen TK (2003) Stability of negative-image equilibria in spike-timing-dependent plasticity. Phys Rev E 68(2–):021, 923

    Google Scholar 

  • Woody CD, Wang XF, Gruen E, Landeira-Fernandez J (1992) Unit activity to click cs changes in dorsal cochlear nucleus after conditioning. Neuroreport 3(5): 385–88

    PubMed  Google Scholar 

  • Wouterlood F, Mugnaini E (1984) Cartwheel neurons of the dorsal cochlear nucleus: a golgi-electron microscopic study in rat. J Comp Neurol 227: 136–57

    PubMed  Google Scholar 

  • Wouterlood F, Mugnaini E, Osen K, Dahl A (1984) Stellate neurons in rat dorsal cochlear nucleus studies with combined golgi impregnation and electron microscopy: synaptic connections and mutual coupling by gap junctions. J Neurocytol 13: 639–64

    PubMed  Google Scholar 

  • Young ED (1984) Response characteristics of neurons of the cochlear nuclei. In: Berlin CI(eds) Hearing science, recent advances. College Hill, San Diego, pp 423–60

    Google Scholar 

  • Young ED, Brownell WE (1976) Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats. J Neurophysiol 39(2): 282–00

    PubMed  Google Scholar 

  • Young ED, Davis KA (2002) Circuitry and function of the dorsal cochlear nucleus. In: Oertel D, Fay R, Popper A(eds) Integrative functions in the mammalian auditory pathway. Springer, New York, pp 160–06

    Google Scholar 

  • Young ED, Voigt HF (1982) Response properties of type ii and type iii units in dorsal cochlear nucleus. Hear Res 6: 153–69

    PubMed  Google Scholar 

  • Young ED, Nelken I, Conley RA (1995) Somatosensory effects on neurons in dorsal cochlear nucleus. J Neurophysiol 73(2): 743–65

    PubMed  Google Scholar 

  • Zhang S, Oertel D (1993) Cartwheel and superficial stellate cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices. J Neurophysiol 69(5): 1384–397

    PubMed  Google Scholar 

  • Zhang X, Heinz MG, Bruce IC, Carney LH (2001) A phenomenological model for the responses of auditory-nerve fibers: I. nonlinear tuning with compression and suppression. J Acoust Soc Am 109(2): 648–70

    PubMed  Google Scholar 

  • Zheng X, Voigt HF (2006) A modeling study of notch noise responses of type iii units in the gerbil dorsal cochlear nucleus. Ann Biomed Eng 34(4): 697–08

    PubMed  Google Scholar 

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  1. Neurological Sciences Institute, Oregon Health & Sciences University, Beaverton, OR, 97006, USA

    Patrick D. Roberts

  2. School of Biological Sciences, Washington State University, Vancouver, WA, 98686, USA

    Christine V. Portfors

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  1. Patrick D. Roberts
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  2. Christine V. Portfors
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Correspondence to Patrick D. Roberts.

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This research is supported in part by National Science Foundation Grant No. IOB-0445648 to PDR and IOS-0620560 to CVP.

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Roberts, P.D., Portfors, C.V. Design principles of sensory processing in cerebellum-like structures. Biol Cybern 98, 491–507 (2008). https://doi.org/10.1007/s00422-008-0217-1

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