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13 - Song selectivity, singing, and synaptic plasticity in songbirds

Published online by Cambridge University Press:  08 August 2009

Michele M. Solis
Affiliation:
5733 26th Ave NE Seattle, WA 98105
Neal A. Hessler
Affiliation:
Keck Center for Integrative Neuroscience Department of Physiology Box 0444 University of California San Francisco, CA 94143-0444
Charlotte A. Boettiger
Affiliation:
Department of Psychology University of California 3210 Tolman Hall #1650 Berkeley, CA 94720-1650
Allison J. Doupe
Affiliation:
University of California UCSF, 513 Parnassus (HSE-818) Box 0444 San Francisco, CA 94143-0444
James R. Pomerantz
Affiliation:
Rice University, Houston
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Summary

Introduction

Birdsong, like human speech, is a learned vocal behavior that requires auditory feedback. Both as juveniles, while they learn to sing, and as adults, songbirds use auditory feedback to compare their own vocalizations with an internal model of a memorized target song. Here we describe experiments that explore the properties of the songbird anterior forebrain pathway (AFP), a basal ganglia–forebrain circuit known to be critical for normal song learning and for adult modification of vocal output, but not for normal adult singing. First, neural recordings in anesthetized, juvenile birds show that single AFP neurons become specialized to process the song stimuli that are compared during sensorimotor learning. AFP neurons develop tuning to the bird's own song, and in many cases to the tutor song as well, even when these stimuli are manipulated to be very different from each other. Second, neural recordings from adult, singing birds reveal robust singing-related activity in the AFP, which is present even in deaf birds. This activity is likely to originate from premotor areas, and could represent an efference copy of motor commands for song, predicting the sensory consequences of motor commands. Finally, in vitro studies of the AFP show that recurrent synapses between neurons in the AFP outflow nucleus can undergo activity-dependent and timing-sensitive strengthening that appears to be restricted to young birds.

Type
Chapter
Information
Topics in Integrative Neuroscience
From Cells to Cognition
, pp. 363 - 384
Publisher: Cambridge University Press
Print publication year: 2008

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References

Aamodt, S. M., Kozlowski, M. R., Nordeen, E. J., and Nordeen, K. W. (1992). Distribution and developmental change in [3H]MK-801 binding within zebra finch song nuclei. Journal of Neurobiology, 23, 997–1005.CrossRefGoogle ScholarPubMed
Abbott, L. F. and Blum, K. I. (1996). Functional significance of long-term potentiation for sequence learning and prediction. Cerebral Cortex, 6, 406–16.CrossRefGoogle ScholarPubMed
Basham, M. E., Nordeen, E. J., and Nordeen, K. W. (1996). Blockade of NMDA receptors in the anterior forebrain impairs sensory acquisition in the zebra finch (Poephila guttata). Neurobiology of Learning and Memory, 66, 295–304.CrossRefGoogle Scholar
Bell, C. (1989). Sensory coding and corollary discharge effects in mormyrid electric fish. Journal of Experimental Biology, 146, 229–53.Google ScholarPubMed
Bell, C. C., Han, V. Z., Sugawara, Y., and Grant, K. (1997). Synaptic plasticity in a cerebellum-like structure depends on spike timing, synaptic strength and cell type. Nature, 387, 278–81.CrossRefGoogle Scholar
Bi, G. and Poo, M.-M. (1998). Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. Journal of Neuroscience, 18, 10464–72.CrossRefGoogle ScholarPubMed
Boettiger, C. A. and Doupe, A. J. (1998). Intrinsic and thalamic excitatory inputs onto songbird LMAN neurons differ in their pharmacological and temporal properties. Journal of Neurophysiology, 79, 2615–28.CrossRefGoogle ScholarPubMed
Boettiger, C. A. and Doupe, A. J. (2001). Developmentally restricted synaptic plasticity in a songbird nucleus required for song learning. Neuron, 31, 809–18.CrossRefGoogle Scholar
Bolhuis, J. J., Zijlstra, G. G. O., Boer-Visser, A. M., and Zee, E. A. (2000). Localized neuronal activation in the zebra finch brain is related to the strength of song learning. Proceedings of the National Academy of Sciences USA, 97, 2282–5.CrossRefGoogle ScholarPubMed
Bottjer, S. W., Brady, J. D., and Walsh, J. P. (1998). Intrinsic and synaptic properties of neurons in the vocal-control nucleus lMAN from in vitro slice preparations of juvenile and adult zebra finches. Journal of Neurobiology, 37, 642–58.3.0.CO;2-G>CrossRefGoogle Scholar
Bottjer, S. W. and Johnson, F. (1997). Circuits, hormones, and learning: vocal behavior in songbirds. Journal of Neurobiology, 33, 602–18.3.0.CO;2-8>CrossRefGoogle ScholarPubMed
Bottjer, S. W., Miesner, E. A., and Arnold, A. P. (1984). Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science, 224, 901–3.CrossRefGoogle ScholarPubMed
Brainard, M. S. and Doupe, A. J. (2000). Interruption of a basal ganglia–forebrain circuit prevents plasticity of learned vocalizations. Nature, 404, 762–6.CrossRefGoogle ScholarPubMed
Bridgeman, B. (1995). A review of the role of efference copy in sensory and oculomotor control systems. Annals of Biomedical Engineering, 23, 409–22.CrossRefGoogle ScholarPubMed
Cowie, R. and Douglas-Cowie, E. (1992). Postlingually acquired deafness: speech deterioration and the wider consequences. In Winter, W., ed., Trends in Linguistics. Mouton de Gruyter, Berlin: Mouton de Gruyter.Google Scholar
Creutzfeldt, O., Ojemann, G., and Lettich, E. (1989). Neuronal activity in the human lateral temporal lobe. II. Responses to the subjects own voice. Experimental Brain Research, 77, 476–89.CrossRefGoogle ScholarPubMed
Dave, A. and Margoliash, D. (2000). Song replay during sleep and computational rules for sensorimotor vocal learning. Science, 270, 812–16.CrossRefGoogle Scholar
Debanne, D., Gahwiler, B. H., and Thompson, S. M. (1998). Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampus slice cultures. Journal of Physiology, 507, 237–47.CrossRefGoogle Scholar
Doupe, A. J. (1997). Song- and order-selective neurons in the songbird anterior forebrain and their emergence during vocal development. Journal of Neuroscience, 17, 1147–67.CrossRefGoogle ScholarPubMed
Doupe, A. J. and Kuhl, P. K. (1999). Birdsong and human speech: common themes and mechanisms. Annual Review of Neuroscience, 22, 567–631.CrossRefGoogle ScholarPubMed
Eales, L. A., (1985). Song learning in zebra finches: some effects of song model availability on what is learnt and when. Animal Behavior, 33, 1293–300.CrossRefGoogle Scholar
Eales, L. A. (1987). Song learning in female-raised zebra finches: another look at the sensitive phase. Animal Behavior, 35, 1356–65.CrossRefGoogle Scholar
Eales, L. A. (1989). The influences of visual and vocal interaction on song learning in zebra finches. Animal Behavior, 37, 507–8.CrossRefGoogle Scholar
Egger, V., Feldmeyer, D., and Sakmann, B. (1999). Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex. Nature Neuroscience, 2, 1098–105.CrossRefGoogle ScholarPubMed
Eimas, P. D., Miller, J. L., and Jusczyk, P. W. (1987). On infant speech perception and language acquisition. In Harnard, S., ed., Categorical Perception. New York: Cambridge University Press, pp. 161–95.Google Scholar
Feldman, D. E. (2000). Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron, 27, 45–56.CrossRefGoogle ScholarPubMed
Gerstner, W., Ritz, R., and Hemmen, J. L. (1993). Why spikes? Hebbian learning and retrieval of time-resolved excitation patterns. Biology Cybernetics, 69, 503–15.CrossRefGoogle ScholarPubMed
Hessler, N. A. and Doupe, A. J. (1999a). Social context modulates singing-related neural activity in the songbird forebrain. Nature Neuroscience, 2, 209–11.CrossRefGoogle Scholar
Hessler, N. A. and Doupe, A. J. (1999b). Singing-related neural activity in a dorsal forebrain-basal ganglia circuit of adult zebra finches. Journal of Neuroscience, 19, 10461–81.CrossRefGoogle Scholar
Hikosaka, O., Sakamoto, M., and Usui, S. (1989). Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. Journal of Neurophysiology, 61, 814–32.CrossRefGoogle ScholarPubMed
Hollerman, J. R., Tremblay, L., and Schultz, W. (1998). Influence of reward expectation on behavior-related neuronal activity in primate striatum. Journal of Neurophysiology, 80, 947–63.CrossRefGoogle ScholarPubMed
Houde, J. F. and Jordan, M. I. (1998). Sensorimotor adaptation in speech production. Science, 36, 1213–16.CrossRefGoogle Scholar
Hua, S. E., Houk, J. C., and Mussa-Ivaldi, F. A. (1999). Emergence of symmetric, modular, and reciprocal connections in recurrent networks with Hebbian learning. Biology Cybernetics, 81, 211–25.CrossRefGoogle ScholarPubMed
Immelmann, K. (1969). Song development in the zebra finch and other estrildid finches. In Hinde, R. A., ed., Bird Vocalizations. London: Cambridge University Press, pp. 61–74.Google Scholar
Konishi, M. (1965). The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Zeitschrift fuer Tierpsychologie, 22, 770–83.Google ScholarPubMed
Kuhl, P. K. (1994). Learning and representation in speech and language. Current Opinion Neurobiology, 4, 812–22.CrossRefGoogle ScholarPubMed
Lee, B. S. (1950). Effects of delayed speech feedback. Journal of the Acoustical Society of America, 22, 824–6.CrossRefGoogle Scholar
Leonardo, A. and Konishi, M. (1999). Decrystallization of adult birdsong by perturbation of auditory feedback. Nature, 399, 466–70.CrossRefGoogle ScholarPubMed
Livingston, F. S. and Mooney, R. (1997). Development of intrinsic and synaptic properties in a forebrain nucleus essential to avian song learning. Journal of Neuroscience, 17, 8997–9009.CrossRefGoogle Scholar
Luo, M. and Perkel, D. J. (1999). A GABAergic, strongly inhibitory projection to a thalamic nucleus in the zebra finch song system. Journal of Neuroscience, 19, 6700–11.CrossRefGoogle ScholarPubMed
Magee, J. C. and Johnston, D. (1997). A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science, 275, 209–13.CrossRefGoogle ScholarPubMed
Margoliash, D. (1983). Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow. Journal of Neuroscience, 3, 1039–57.CrossRefGoogle ScholarPubMed
Markram, H., Lübke, J., Frotscher, M., and Sakmann, B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science, 275, 213–15.CrossRefGoogle ScholarPubMed
Marler, P. (1970). A comparative approach to vocal learning: song development in white-crowned sparrows. Journal of Comparative and Physiological Psychology Monographs, 71, 1–25.CrossRefGoogle Scholar
McCasland, J. S. (1987). Neuronal control of bird song production. Journal of Neuroscience, 7, 23–39.CrossRefGoogle ScholarPubMed
McCasland, J. S. and Konishi, M. (1981). Interaction between auditory and motor activities in an avian song control nucleus. Proceedings of the National Academy of Sciences USA, 78, 7815–19.CrossRefGoogle Scholar
Mello, C. V., Vicario, D. S., and Clayton, D. F. (1992). Song presentation induces gene expression in the songbird forebrain. Proceedings of the National Academy of Sciences USA, 89, 6818–22.CrossRefGoogle ScholarPubMed
Nordeen, K. W. and Nordeen, E. J. (1992). Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. Behavioral Neural Biology, 57, 58–66.CrossRefGoogle Scholar
Nottebohm, F., Stokes, T. M., and Leonard, C. M. (1976). Central control of song in the canary, Serinus canarius. Journal of Comparative Neurology, 165, 457–86.CrossRefGoogle Scholar
Ojemann, G. A. (1991). Cortical organization of language. Journal of Neuroscience, 11, 2281–7.CrossRefGoogle ScholarPubMed
Price, P. H. (1979). Developmental determinants of structure in zebra finch song. Journal of Comparative and Physiology Psychology, 93, 260–77.CrossRefGoogle Scholar
Roberts, P. D. (1999). Computational consequences of temporally asymmetric learning rules: I. Differential Hebbian learning. Journal of Computation in Neuroscience, 7, 235–46.CrossRefGoogle ScholarPubMed
Scharff, C. and Nottebohm, F. (1991). A comparative study of the behavioral deficits following lesions of the various parts of the zebra finch song system: implications for vocal learning. Journal of Neuroscience, 11, 2896–913.CrossRefGoogle Scholar
Sohrabji, F., Nordeen, E. J., and Nordeen, K. W. (1990). Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch. Behavioral Neurology Biology, 53, 51–63.CrossRefGoogle ScholarPubMed
Solis, M. M. and Doupe, A. J. (1997). Anterior forebrain neurons develop selectivity by an intermediate stage of birdsong learning. Journal of Neuroscience, 17, 6447–62.CrossRefGoogle ScholarPubMed
Solis, M. M. and Doupe, A. J. (1999). Contributions of tutor and bird's own song experience to neural selectivity in the songbird anterior forebrain. Journal of Neuroscience, 19, 4559–84.CrossRefGoogle ScholarPubMed
Solis, M. M. and Doupe, A. J. (2000). Compromised neural selectivity for song in birds with impaired sensorimotor learning. Neuron, 25, 109–21.CrossRefGoogle Scholar
Song, S., Miller, K. D., and Abbott, L. F. (2000). Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nature Neuroscience, 3, 919–23.CrossRefGoogle ScholarPubMed
Theunissen, F. E. and Doupe, A. J. (1998). Temporal and spectral sensitivity of complex auditory neurons in the nucleus HVc of male zebra finches. Journal of Neuroscience, 18, 3786–802.CrossRefGoogle ScholarPubMed
Tremblay, L., Hollerman, J. R., and Schultz, W. (1998). Modifications of reward expectation-related neuronal activity during learning in primate striatum. Journal of Neurophysiology, 80, 964–77.CrossRefGoogle ScholarPubMed
Troyer, T. and Doupe, A. J. (2000a). An associational model of birdsong sensorimotor learning I. Efference copy and the learning of song syllables. Journal of Neurophysiology, 84(3), 1204–23.CrossRefGoogle Scholar
Troyer, T. and Doupe, A. J. (2000b). An associational model of birdsong sensorimotor learning. II. Temporal hierarchies and the learning of song sequence. Journal of Neurophysiology, 84, 1224–39.CrossRefGoogle Scholar
Holst, E. and Mittelstaedt, H. (1950). Das Reafferenzprinzip. Wechselwirkungen zwischen Zentralnervensystem und Peripherie. Naturwissenschaften, 37, 464–76.CrossRefGoogle Scholar
Waldstein, R. S. (1989). Effects of postlingual deafness on speech production: implications for the role of auditory feedback. Journal of the Acoustical Society of America, 88, 2099–114.CrossRefGoogle Scholar
Werker, J. F. and Tees, R. C. (1992). The organization and reorganization of human speech perception. Annual Review of Neuroscience, 15, 377–402.CrossRefGoogle ScholarPubMed
Williams, H. and Mehta, N. (1999). Changes in adult zebra finch song require a forebrain nucleus that is not necessary for song production. Journal of Neurobiology, 39, 14–28.3.0.CO;2-X>CrossRefGoogle Scholar
Yu, A. C. and Margoliash, D. (1996). Temporal hierarchical control of singing in birds. Science, 273, 1871–5.CrossRefGoogle ScholarPubMed
Zhang, L. I., Tao, H. W., Holt, C. E., Harris, W. A., and Poo, M.-M. (1998). A critical window for cooperation and competition among developing retinotectal synapses. Nature, 395, 37–44.CrossRefGoogle ScholarPubMed

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