Trends in Neurosciences
Volume 23, Issue 6, 1 June 2000, Pages 251-258
Journal home page for Trends in Neurosciences

Review
Seasonal plasticity in the adult brain

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Abstract

Seasonal plasticity of structure and function is a fundamental feature of nervous systems in a wide variety of animals that occupy seasonal environments. Excellent examples of seasonal brain changes are found in the avian song control system, which has become a leading model of morphological and functional plasticity in the adult CNS. The volumes of entire brain regions that control song increase dramatically in anticipation of the breeding season. These volumetric changes are induced primarily by vernal increases in circulating sex steroids and are accompanied by increases in neuronal size, number and spacing. In several species, these structural changes in the song control circuitry are associated with seasonal changes in song production and learning. Songbirds provide important insights into the mechanisms and behavioral consequences of plasticity in the adult brain.

Section snippets

The volumes of song control nuclei change seasonally

Song is a learned behavior used by birds to attract mates and to defend breeding territories21. In oscine passerines (songbirds), song behavior is controlled by a network of discrete interconnected brain regions or nuclei (Fig. 1). Song behavior and the brain regions that control it are seasonally plastic in every species of seasonally breeding adult songbird that has been systematically studied36, 37, 38, 39. The entire volumes of several song nuclei, including the neostriatal region HVc

Neuron number changes seasonally in HVc

Seasonal changes in the morphology of HVc were first demonstrated in male canaries by Nottebohm. He used Nissl-stained tissue to show that HVc volume3 and neuron number60 were twice as large during the spring than during autumn (Table 3). The reliability of Nissl criteria to define the borders of song nuclei, especially HVc, was subsequently called into question (see Box 1). A wide series of studies have since shown, however, that the Nissl-defined borders of HVc coincide with those defined by

Dendritic growth and synaptogenesis in RA

The cellular basis of the volumetric growth of RA differs from that observed in HVc. Neuron number does not change seasonally in RA, but neuron size and spacing in this nucleus are both greater during the breeding season37, 39, 44, 49, 61, 62, 75. The increase in neuronal spacing is associated with a vernal increase in the dendritic arborizations of RA neurons60. Synaptic morphology also varies seasonally in RA, such that the sizes of presynaptic and postsynaptic profiles are largest during the

Testosterone mediates seasonal changes in the song system

Several lines of evidence strongly suggest that testosterone (or its active metabolites) is the primary physiological cue that mediates the cyclical anatomical changes in the song circuitry. Several song nuclei, including HVc, RA, the medial and lateral portions of the magnocellular nucleus of the anterior neostriatum (mMAN and lMAN), the tracheosyringeal portion of the hypoglossal nucleus (nXIIts), and the dorsolateral nucleus of the medial thalamus (DLM) contain gonadal steroid receptors79, 80

Non-steroidal cues contribute to seasonal plasticity

The seasonal plasticity in the song control system is not governed solely by gonadal steroids. Studies from two laboratories have indicated that manipulations of day length can induce changes in the song nuclei of castrated animals. Long days increased the volume of HVc slightly in castrated white-crowned sparrows44 and starlings95. Another study suggested that photostimulation increased the volumes of HVc, RA and area X in castrated American tree sparrows (Spizella arborea)46. These

Why does the structure of the song system change seasonally? An hypothesis

The sustained peak performance of a seasonally predictable behavioral task is often preceded by hypertrophy of the organs or tissues, that support that task101. For example, the size of the gonads and other reproductive structures increases dramatically in preparation for the annual breeding season and these organs regress when the breeding season is terminated47. Long-distance migration in birds is preceded by a host of physiological changes including elevated fat stores and increased flight

Concluding remarks and prospects for the future

Seasonal plasticity of the song system can serve as a model to address the following questions, which are of fundamental importance to the study of neural plasticity in general.

  • What are the mechanisms that mediate hormone action in the adult brain? Does hormone metabolism contribute to adult brain changes? How does trans-synaptic support from afferent and efferent targets support or influence, hormone action in a given brain region?

  • What growth factors and trophic agents influence adult brain

Acknowledgements

The authors’ research is supported by the Virginia Merrill Bloedel Hearing Research Center, grant MH53032 from the NIH, and grant DGE-9616736AM02 from the NSF.

References (105)

  • D.J. Bernard et al.

    Two histological markers reveal a similar photoperiodic difference in the volume of the high vocal center in male European starlings

    J. Comp. Neurol.

    (1995)
  • K. Herrmann et al.

    Lesions of HVc block the developmental masculinizing effects of estradiol in the female zebra finch song system

    J. Neurobiol.

    (1991)
  • E. Akutagawa et al.

    Transient expression and transport of brain-derived neurotrophic factor in the male zebra finch’s song system during vocal development

    Proc. Natl. Acad. Sci. U. S. A.

    (1998)
  • F. Nottebohm

    Testosterone triggers growth of brain vocal control nuclei in adult female canaries

    Brain Res.

    (1980)
  • M. Konishi et al.

    Androgen increases protein synthesis within the avian brain vocal control system

    Brain Res.

    (1981)
  • S. Rasika

    BDNF mediates the effects of testosterone on the survival of new neurons in an adult brain

    Neuron

    (1999)
  • M. Holzenberger

    Selective expression of insulin-like growth factor II in the songbird brain

    J. Neurosci.

    (1997)
  • L. Bottoni et al.

    Seasonal changes in testosterone metabolism in the pituitary gland and central nervous system of the European starling (Sturnus vulgaris)

    Gen. Comp. Endocrinol.

    (1981)
  • G.E. Bentley

    Seasonal neuroplasticity in the songbird telencephalon: A role for melatonin

    Proc. Natl. Acad. Sci. U. S. A.

    (1999)
  • B.A. Schlinger

    Androgen synthesis in a songbird: a study of cyp17 (17alpha-hydroxylase/C17,20-lyase) activity in the zebra finch

    Gen. Comp. Endocrinol.

    (1999)
  • M.G. Whitfield-Rucker et al.

    Melatonin binding in the house sparrow song control system: Sexual dimorphism and the effect of photoperiod

    Horm. Behav.

    (1996)
  • J. Altman

    Are new neurons formed in the brains of adult animals?

    Science

    (1962)
  • F. Nottebohm

    A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain

    Science

    (1981)
  • N.L. Wayne

    Seasonal fluctuations in the secretory response of neuroendocrine cells of Aplysia californica to inhibitors of protein kinase A and protein kinase C

    Gen. Comp. Endocrinol.

    (1998)
  • K.J. Belkin et al.

    The effect of the neuropeptide FMRFamide on Aplysia californica siphon motoneurons involves multiple ionic currents that vary seasonally

    J. Exp. Biol.

    (1998)
  • G.A. Lnenicka et al.

    Seasonal differences in the physiology and morphology of crayfish motor terminals

    J. Neurobiol.

    (1991)
  • M. Pasmanik et al.

    A high abundance androgen receptor in goldfish brain: Characteristics and seasonal changes

    Endocrinology

    (1988)
  • J.A. McNulty

    Morphologic evidence for seasonal changes in the pineal organ of the goldfish, Carassius auratus: a quantitative study

    Reprod. Nutr. Dev.

    (1982)
  • S. Takami et al.

    The volume of the toad medial amygdala-anterior preoptic complex is sexually dimorphic and seasonally variable

    Neurosci. Lett.

    (1984)
  • J. Wade et al.

    The relationship between reproductive state and ‘sexually’ dimorphic brain areas in sexually reproducing and parthenogenetic whiptail lizards

    J. Comp. Neurol.

    (1991)
  • A. Barnea et al.

    Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees

    Proc. Natl. Acad. Sci. U. S. A.

    (1994)
  • T.V. Smulders

    Seasonal variation in hippocampal volume in a food-storing bird, the black-capped chickadee

    J. Neurobiol.

    (1995)
  • D.M. Parry

    Immunocytochemical localization of GnRH precursor in the hypothalamus of European starlings during sexual maturation and photorefractoriness

    J. Neuroendocrinol.

    (1997)
  • N.G. Forger et al.

    Seasonal variation in mammalian striated muscle mass and motoneuron morphology

    J. Neurobiol.

    (1987)
  • R. Buijs

    Seasonal variation in vasopressin innervation in the brain of the European hamster (Cricetus cricetus)

    Brain Res.

    (1986)
  • J.J. Xiong

    Evidence for seasonal plasticity in the gonadotropin-releasing hormone (GnRH) system of the ewe: Changes in synaptic inputs onto GnRH neurons

    Endocrinology

    (1997)
  • W. Lee

    Photoperiod affects the expression of neural cell adhesion molecule and polysialic acid in the hypothalamus of the Siberian hamster

    Brain Res.

    (1995)
  • M.A. Hofman et al.

    Seasonal changes in the suprachiasmatic nucleus of man

    Neurosci. Lett.

    (1992)
  • C.K. Catchpole et al.

    Bird Song: Biological Themes and Variations

    (1995)
  • D.S. Vicario

    Neural mechanisms of vocal production in songbirds

    Curr. Opin. Neurobiol.

    (1991)
  • D. Margoliash

    Functional organization of forebrain pathways for song production and perception

    J. Neurobiol.

    (1997)
  • F. Nottebohm

    Central control of song in the canary, Serinus canarius

    J. Comp. Neurol.

    (1976)
  • E.A. Brenowitz

    Altered perception of species-specific song by female birds after lesions of a forebrain nucleus

    Science

    (1991)
  • A.J. Doupe

    Song- and order-selective neurons in the songbird anterior forebrain and their emergence during vocal development

    J. Neurosci.

    (1997)
  • F. Sohrabji

    Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch

    Behav. Neural Biol.

    (1990)
  • C. Scharff

    Conspecific and heterospecific song discrimination in male zebra finches with lesions in the anterior forebrain pathway

    J. Neurobiol.

    (1998)
  • E.F. Foster

    Axonal connections of the medial magnocellular nucleus of the anterior neostriatum in zebra finches

    J. Comp. Neurol.

    (1997)
  • G.E. Vates

    Reafferent thalamo-‘cortical’ loops in the song system of oscine songbirds

    J. Comp. Neurol.

    (1997)
  • G.E. Vates

    Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches

    J. Comp. Neurol.

    (1996)
  • G.T. Smith

    Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds

    J. Neurosci.

    (1997)
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