Context-specific habituation of the zenk gene response to song in adult zebra finches

Kruse, Amy; Stripling, Roy; Clayton, David F.

doi:10.1016/j.nlm.2004.05.001

Cited by 75 publications

(70 citation statements)

References 46 publications

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“…Social factors known to affect the magnitude of the behavioral response, such as song complexity, dialect, or familiarity to the listener, also affect the zenk response (Gentner et al, 2001;Sockman et al, 2002;Maney et al, 2003;Terpstra et al, 2006;cf Dong and Clayton, 2008;Woolley and Doupe, 2008). The response to a song can be enhanced by experimentally increasing its behavioral relevance, for example by pairing it with foot shocks or flashing lights (Jarvis et al, 1995;Kruse et al, 2004). Thus, the zenk response in NCM seems to be proportional to the salience of the signal, and NCM may be involved in encoding behavioral relevance (Pinaud and Terleph, 2008).…”

Section: Introductionmentioning

confidence: 99%

Topography of estradiol‐modulated genomic responses in the songbird auditory forebrain

Sanford

Lange

Maney

2009

Developmental Neurobiology

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Sex steroids facilitate dramatic changes in behavioral responses to sociosexual signals and are increasingly implicated in the sensory processing of those signals. Our previous work demonstrated that in female white-throated sparrows, which are seasonal breeders, genomic responses in the auditory forebrain are selective for conspecific song over frequency-matched tones only when plasma estradiol (E2) reaches breeding levels. Here, we sought to map this E2-dependent selectivity in the best-studied area of the auditory forebrain, the caudomedial nidopallium (NCM). Nonbreeding females with low endogenous levels of E2 were treated with E2 or a placebo and exposed to conspecific song, tones, or no sound playback. Immunoreactive protein product of the immediate early gene zenk (egr-1) was then quantified within seven distinct subregions, or domains, of NCM. We report three main findings: (1) regardless of hormone treatment, the zenk response is significantly higher in dorsal than in ventral NCM, and higher in medial than in lateral NCM; (2) E2-dependent selectivity of the response is limited to the rostral and medial domains of NCM; in the more caudal domains, song induces more zenk expression than tones regardless of hormone treatment; (3) even when no sound stimuli were presented, E2 treatment significantly increased zenk expression in the rostral, but not the caudal, domains of NCM. Together, the latter two findings suggest that E2-dependent plasticity in NCM is concentrated in rostral NCM, which is hodologically and neurochemically distinct from caudal NCM. Activity in rostral NCM may therefore be seasonally regulated in this species.

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Section: Introductionmentioning

confidence: 99%

Topography of estradiol‐modulated genomic responses in the songbird auditory forebrain

Sanford

Lange

Maney

2009

Developmental Neurobiology

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“…After the stimulus was repeated for a few hours the ZENK RNA declined back to its initial starting level (5,6). Subsequent presentations no longer elicited a response, but presentation of a different song (6) or even of the same song in a different spatial or visual context (7) activated the response once again. Stimulus-specific ZENK response habituation requires the initial activation of the ERK signaling pathway (8).…”

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confidence: 98%

Discrete molecular states in the brain accompany changing responses to a vocal signal

Dong¹,

Replogle

Hasadsri³

et al. 2009

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

100

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New experiences can trigger changes in gene expression in the brain. To understand this phenomenon better, we studied zebra finches hearing playbacks of birdsong. Earlier research had shown that initial playbacks of a novel song transiently increase the ZENK (ZIF-268, EGR1, NGFIA, KROX-24) mRNA in the auditory forebrain, but the response selectively habituates after repetition of the stimulus. Here, using DNA microarray analysis, we show that novel song exposure induces rapid changes in thousands of RNAs, with even more RNAs decreasing than increasing. Habituation training leads to the emergence of a different gene expression profile a day later, accompanied by loss of essentially all of the rapid ''novel'' molecular responses. The novel molecular profile is characterized by increases in genes involved in transcription and RNA processing and decreases in ion channels and putative noncoding RNAs. The ''habituated'' profile is dominated by changes in genes for mitochondrial proteins. A parallel proteomic analysis [2-dimensional difference gel electrophoresis (2D-DIGE) and sequencing by mass spectrometry] also detected changes in mitochondrial proteins, and direct enzyme assay demonstrated changes in both complexes I and IV in the habituated state. Thus a natural experience, in this case hearing the sound of birdsong, can lead to major shifts in energetics and macromolecular metabolism in higher centers in the brain.habituation ͉ microarray ͉ mitochondria ͉ proteomic ͉ songbird T he genome was once regarded as a passive agent in brain function, directing brain development but having little role in the moment-to-moment operation of the mature brain. Through the widespread application of technologies for measuring gene expression in experimental model systems, however, it now appears that changing social conditions, perceptual experience, and behavioral activity can all result in rapid changes in the expression of specific genes in the brain (1, 2). The challenge ahead is to understand the links between gene expression and natural experience, behavior, and cognition.A striking example for study is the phenomenon of song response habituation in songbirds (3). In one of the first demonstrations of brain gene activation in response to a natural experience, Mello and colleagues (4) showed that the sound of another bird singing triggers a transient increase in expression of the ZENK gene EGR1, NGFIA, in an auditory/associative region of the songbird forebrain. This was not simply a sensory or an auditory response, as its magnitude showed clear categorical discrimination (conspecific song Ͼ heterospecific song Ͼ noise Ͼ pure tones). Further research showed that the same song stimulus would either activate ZENK expression or not, depending on the recent history of exposure to the stimulus and its context. After the stimulus was repeated for a few hours the ZENK RNA declined back to its initial starting level (5, 6). Subsequent presentations no longer elicited a response, but presentation of a different song (6) or even of ...

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“…Also, songs that are more attractive to female European starlings induce higher IEG responses in NCM (Gentner et al, 2001). In addition, neurons within NCM show physiological responses to song presentation (Chew et al, 1996;Stripling et al, 1997;Kruse et al, 2004). Together, these data suggest a substantial role for NCM in auditory discrimination.…”

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confidence: 71%

Adult female and male zebra finches show distinct patterns of spine deficits in an auditory area and in the song system when reared without exposure to normal adult song

et al. 2005

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Male songbirds typically require exposure to normal adult conspecific song during development in order to learn a normal song of their own. Females require exposure to conspecific song during development in order to select high-quality, learned song over the incomplete song produced by males reared in isolation. Altering males' opportunity for song learning during development affects the neuroanatomy of brain regions involved in song production (the song system), but in females the neural effects of song learning are unknown. We raised male and female zebra finches (Taeniopygia guttata) with differing amounts of exposure to singing males during development. At 120 days, we Golgi-stained their brains and measured the frequency of dendritic spines in brain areas used in song perception or production. We found that females reared with little or no exposure to song have 31% fewer dendritic spines per unit length of dendrite in caudomedial nidopallium (NCM), a brain area activated by song perception, compared to control females. The deprived females had small deficits in the frequency of spines in HVC, a region activated by song production in males. Males with limited exposure to song had a 24% lower spine density in HVC than controls but only a 10% lower density in NCM. These data support the hypothesis that NCM is important in auditory learning, while HVC is involved in sensorimotor learning, and that these capacities are differentially emphasized in the two sexes.

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Context-specific habituation of the zenk gene response to song in adult zebra finches

Cited by 75 publications

References 46 publications

Topography of estradiol‐modulated genomic responses in the songbird auditory forebrain

Topography of estradiol‐modulated genomic responses in the songbird auditory forebrain

Discrete molecular states in the brain accompany changing responses to a vocal signal

Adult female and male zebra finches show distinct patterns of spine deficits in an auditory area and in the song system when reared without exposure to normal adult song

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