Abstract
Song behavior and its underlying neural substrate can change seasonally in adult songbirds. To test whether environmental cues induce seasonal changes in electrophysiological characteristics of song control neurons, we measured in vitro intrinsic neuronal activity in the song control nucleus RA of adult male song sparrows (Melospiza melodia) in both the fall non-breeding and spring breeding seasons. We found that RA neurons in spring-captured birds show a more than threefold increase in spontaneous firing rate compared to those from fall-captured birds. We conclude that environmental cues are sufficient to induce seasonal changes in electrophysiological properties of song control neurons, and that changes in these properties may underlie seasonal changes in song behavior.
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Abbreviations
- 13:11:
-
13 h light:11 h dark
- ACSF:
-
Artificial cerebrospinal fluid
- AFP:
-
Anterior forebrain pathway
- DLM:
-
The medial portion of the dorsolateral nucleus of the anterior thalamus
- HVC:
-
Used as a proper name
- LD + T:
-
Long-day photoperiod (20 h light:4 h dark) and a systemic testosterone implant
- LMAN:
-
The lateral magnocellular nucleus of anterior nidopallium
- RA:
-
The robust nucleus of the arcopallium
- RIA:
-
Radioimmunoassay
- SD:
-
Short-day photoperiod (8 h light:16 h dark)
- SEM:
-
Standard error of the mean
- T:
-
Testosterone
- WC:
-
White-crowned sparrow
- X:
-
Area X, a subdivision of the medial striatum
References
Adret P, Margoliash D (2002) Metabolic and neural activity in the song system nucleus robustus archistriatalis: effect of age and gender. J Comp Neurol 454:409–423
Ames A 3rd (2000) CNS energy metabolism as related to function. Brain Res Rev 34:42–68
Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133–1145
Ball GF, Auger CJ, Bernard DJ, Charlier TD, Sartor JJ, Riters LV, Balthazart J (2004) Seasonal plasticity in the song control system: multiple brain sites of steroid hormone action and the importance of variation in song behavior. Ann N Y Acad Sci 1016:586–610
Bottjer SW, Miesner EA, Arnold AP (1986) Changes in neuronal number, density and size account for increases in volume of song-control nuclei during song development in zebra finches. Neurosci Lett 67:263–268
Brenowitz EA (2004) Plasticity of the adult avian song control system. Ann N Y Acad Sci 1016:560–585
Brenowitz EA, Beecher MD (2005) Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci 28:127–132
Canady RA, Burd GD, DeVoogd TJ, Nottebohm F (1988) Effect of testosterone on input received by an identified neuron type of the canary song system: a Golgi/electron microscopy/degeneration study. J Neurosci 8:3770–3784
Carson RJ, Spicer GS (2003) A phylogenetic analysis of the emberizid sparrows based on three mitochondrial genes. Mol Phylogenet Evol 29:43–57
Del Negro C, Edeline JM (2002) Sex and season influence the proportion of thin spike cells in the canary HVc. Neuroreport 13:2005–2009
Del Negro C, Lehongre K, Edeline JM (2005) Selectivity of canary HVC neurons for the bird’s own song: modulation by photoperiodic conditions. J Neurosci 25:4952–4963
Fusani L, Canoine V, Goymann W, Wikelski M, Hau M (2005) Difficulties and special issues associated with field research in behavioral neuroendocrinology. Horm Behav 48:484–491
Gittis AH, du Lac S (2006) Intrinsic and synaptic plasticity in the vestibular system. Curr Opin Neurobiol 16:385–390
Goldman SA, Nottebohm F (1983) Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci USA 80:2390–2394
Häusser M, Raman IM, Otis T, Smith SL, Nelson A, du Lac S, Loewenstein Y, Mahon S, Pennartz C, Cohen I, Yarom Y (2004) The beat goes on: spontaneous firing in mammalian neuronal microcircuits. J Neurosci 24:9215–9219
Konishi M, Akutagawa E (1985) Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain. Nature 315:145–147
Konishi M, Akutagawa E (1990) Growth and atrophy of neurons labeled at their birth in a song nucleus of the zebra finch. Proc Natl Acad Sci USA 87:3538–3541
Lennie P (2003) The cost of cortical computation. Curr Biol 13:493–497
Loewenstein Y, Mahon S, Chadderton P, Kitamura K, Sompolinsky H, Yarom Y, Hausser M (2005) Bistability of cerebellar Purkinje cells modulated by sensory stimulation. Nat Neurosci 8:202–211
Lucas JR, Freeberg TM, Long GR, Krishnan A (2007) Seasonal variation in avian auditory evoked responses to tones: a comparative analysis of Carolina chickadees, tufted titmice, and white-breasted nuthatches. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193:201–215
Lucas JR, Freeberg TM, Krishnan A, Long GR (2002) A comparative study of avian auditory brainstem responses: correlations with phylogeny and vocal complexity, and seasonal effects. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 188:981–992
Marler P, Peters S (1987) A sensitive period for song acquisition in the song sparrow, Melospiza melodia: a case of age-limited learning. Ethology 76:89–100
Marler P, Slabbekoorn H (2004) Nature’s music, the science of birdsong. Elsevier, San Diego
Marler P, Tamura M (1964) Culturally transmitted patterns of vocal behavior in sparrows. Science 146:1483–1486
Mooney R (1992) Synaptic basis for developmental plasticity in a birdsong nucleus. J Neurosci 12:2464–2477
Moore IT, Wingfield JC, Brenowitz EA (2004) Plasticity of the avian song control system in response to localized environmental cues in an equatorial songbird. J Neurosci 24:10182–10185
Nordby JC, Campbell SE, Beecher MD (2002) Adult song sparrows do not alter their song repertoires. Ethology 108:39–50
Nottebohm F (1981) A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science 214:1368–1370
Nottebohm F, Nottebohm ME, Crane LA (1986) Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song control nuclei. Behav Neural Biol 46:445–471
Nottebohm F, Nottebohm ME, Crane LA, Wingfield JC (1987) Seasonal changes in gonadal hormone levels of adult male canaries and their relationship to song. Behav Neural Biol 47:197–211
Park KH, Meitzen J, Moore IT, Brenowitz EA, Perkel DJ (2005) Seasonal-like plasticity of spontaneous firing rate in a songbird pre-motor nucleus. J Neurobiol 64:181–191
Perfito N, Meddle SL, Tramontin AD, Sharp PJ, Wingfield JC (2005) Seasonal gonadal recrudescence in song sparrows: response to temperature cues. Gen Comp Endocrinol 143:121–128
Perfito N, Tramontin AD, Meddle S, Sharp P, Afik D, Gee J, Ishii S, Kikuchi M, Wingfield JC (2004) Reproductive development according to elevation in a seasonally breeding male songbird. Oecologia 140:201–210
Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Guturkun O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J, Siang C, Jarvis ED (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377–414
Sartor JJ, Ball GF (2005) Social suppression of song is associated with a reduction in volume of a song-control nucleus in European starlings (Sturnus vulgaris). Behav Neurosci 119:233–244
Schlinger BA, London SE (2006) Neurosteroids and the songbird model system. J Exp Zool A Comp Exp Biol 305:743–748
Smith GT (1996) Seasonal plasticity in the song nuclei of wild rufous-sided towhees. Brain Res 734:79–85
Smith GT, Brenowitz EA, Beecher MD, Wingfield JC (1997a) Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. J Neurosci 17:6001–6010
Smith GT, Brenowitz EA, Wingfield JC (1997b) Roles of photoperiod and testosterone in seasonal plasticity of the avian song control system. J Neurobiol 32:426–442
Smith GT, Brenowitz EA, Wingfield JC, Baptista LF (1995) Seasonal changes in song nuclei and song behavior in Gambel’s white-crowned sparrows. J Neurobiol 28:114–125
Solis MM, Perkel DJ (2006) Noradrenergic modulation of activity in a vocal control nucleus in vitro. J Neurophysiol 95:2265–2276
Soma KK (2006) Testosterone and aggression: Berthold, birds and beyond. J Neuroendocrinol 18:543–551
Soma KK, Tramontin AD, Featherstone J, Brenowitz EA (2004) Estrogen contributes to seasonal plasticity of the adult avian song control system. J Neurobiol 58:413–422
Spiro JE, Dalva MB, Mooney R (1999) Long-range inhibition within the zebra finch song nucleus RA can coordinate the firing of multiple projection neurons. J Neurophysiol 81:3007–3020
Thompson CK, Brenowitz EA (2005) Seasonal change in neuron size and spacing but not neuronal recruitment in a basal ganglia nucleus in the avian song control system. J Comp Neurol 481:276–283
Tramontin AD, Brenowitz EA (1999) A field study of seasonal neuronal incorporation into the song control system of a songbird that lacks adult song learning. J Neurobiol 40:316–326
Tramontin AD, Brenowitz EA (2000) Seasonal plasticity in the adult brain. Trends Neurosci 23:251–258
Tramontin AD, Hartman VN, Brenowitz EA (2000) Breeding conditions induce rapid and sequential growth in adult avian song circuits: a model of seasonal plasticity in the brain. J Neurosci 20:854–861
Tramontin AD, Perfito N, Wingfield JC, Brenowitz EA (2001) Seasonal growth of song control nuclei precedes seasonal reproductive development in wild adult song sparrows. Gen Comp Endocrinol 122:1–9
Tramontin AD, Smith GT, Breuner CW, Brenowitz EA (1998) Seasonal plasticity and sexual dimorphism in the avian song control system: stereological measurement of neuron density and number. J Comp Neurol 396:186–192
Tramontin AD, Wingfield JC, Brenowitz EA (1999) Contributions of social cues and photoperiod to seasonal plasticity in the adult avian song control system. J Neurosci 19:476–483
Wennstrom KL, Reeves BJ, Brenowitz EA (2001) Testosterone treatment increases the metabolic capacity of adult avian song control nuclei. J Neurobiol 48:256–264
Wingfield JC, Hahn TP (1994) Testosterone and territorial behaviour in sedentary and migratory sparrows. Anim Behav 47:77–89
Wingfield JC, Kenagy GJ (1991) Natural regulation of reproductive cycles. In: Pang PKT, Schreibrman MP (eds) Vertebrate endocrinology: fundamentals and biomedical implications. Academic, San Diego, pp 181–241
Acknowledgments
We thank the members of the Perkel and Brenowitz labs for critical discussion and support, and Karin Lent for expert technical assistance. E.A.B. and D.J.P. are affiliates of the Virginia Merrill Bloedel Hearing Research Center. All experimental procedures followed National Institute of Health guidelines for the care and use of animals and were approved by the University of Washington Institutional Animal Care and Use Committee. Grant sponsors: NIH: MH068530 (D.J.P.), MH53032 (E.A.B.) P30 DC-04661 (E.W. Rubel); NSF: Graduate Research Fellowship (J.M.).
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Meitzen, J., Perkel, D.J. & Brenowitz, E.A. Seasonal changes in intrinsic electrophysiological activity of song control neurons in wild song sparrows. J Comp Physiol A 193, 677–683 (2007). https://doi.org/10.1007/s00359-007-0222-1
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DOI: https://doi.org/10.1007/s00359-007-0222-1