Ornithol Sci 5: 23–29 (2006)

SPECIAL FEATURE Neuroecology of birdsong Song preferences by females: male song complexity and gene expression in the female brain

Hiroko EDA-FUJIWARA1,#, Ryohei SATOH2 and Takenori MIYAMOTO1

1 Department of Chemical & Biological Sciences, Japan Women’s University, Mejirodai, Bunkyo, Tokyo 112–8681, Japan 2 Department of Physiology, Kitasato University School of Medicine, Sagamihara, Kanagawa 228–8555, Japan

Abstract The males of songbirds, parrots and hummingbirds develop complex song ORNITHOLOGICAL through learning. Males of some species mimic the vocalizations of other species and SCIENCE make their song more complex through vocal mimicry. Females of several songbird © The Ornithological Society species respond preferentially to more complex song. The sensory exploitation hy- of Japan 2006 pothesis is an explanation how female preferences for complex song historically came to exist in birds. Female response to song readily habituates to repeated presentation of simple (that is, monotonous) song, while complex song can reduce habituation in female response to song. Males singing complex song might have exploited such pre- existing property (or bias) in the female’s response to song. This explanation is sup- ported by experiments involving measurement of the expression of immediate early genes (IEGs). Analysis of IEG expression has been useful to reveal brain activation patterns associated with specific sensory stimuli. When exposed to male song, female songbirds and parrots show increased IEG expression in the auditory system in the caudal telencephalon, notably the caudomedial nidopallium (NCM) and the caudome- dial mesopallium (CMM). Current data from female brains suggest that the NCM is related to song complexity. In addition, both of the NCM and the CMM may be in- volved in discriminating conspecific from heterospecific vocalizations.

Key words NCM, Sensory exploitation, Sexual selection, Vocal mimicry, ZENK

SONG COMPLEXITY AND males are able to discriminate conspecific from het- PREFERENCES BY FEMALES erospecific song, and also between song variations within their own species (Searcy 1992a). A consider- Birdsong is among the most acoustically complex able number of studies have shown that females of all non-human vocal communication signals. Song respond preferentially to more complex song is found in three avian taxa: Passeriformes (mostly (Kroodsma 1976; Catchpole & Slater 1995; Lampe & songbirds), Psittaciformes (parrots) and Trochilo- Saetre 1995; Hasselquist et al. 1996; Mountjoy & formes (hummingbirds), and often constitutes a Lemon 1996; Searcy & Yasukawa 1996; Gentner & prominent part of male display during the breeding Hulse 2000). It is considered that females select season (Catchpole & Slater 1995). This complex vo- males with more complex songs and that sexual se- calization is composed of many syllables, varying in lection by female choice has made song more com- acoustic structure. One way to measure the complex- plex. ity of song is to determine what is known as syllable repertoire size, where the number of different sylla- EXPRESSION OF IMMEDIATE EARLY bles of each male’s song is counted. GENE IN FEMALE BRAINS The song of male birds plays an important role in attracting females and in stimulating female repro- How is it that female preferences for complex song ductive behavior and physiology. In many species, fe- came to exist in birds? One explanation is the sensory exploitation hypothesis which suggests that a male is (Received 22 December 2005; Accepted 11 April 2006) favored by sexual selection, if he uses a trait to ex- # Corresponding author, E-mail: [email protected] ploit preexisting biases in the female’s response to

23 H. E. FUJIWARA et al. stimuli (Searcy 1992b). If a female has a bias toward responding to certain signal parameters, such as louder sounds or brighter colors, because they are easier to detect, we would expect that males having signals with such parameters (louder sounds or brighter colors) are selected (Ryan 1998). Thus, it is important to know the nature of neural system in fe- males in order to understand why a particular male trait is attractive to females. Birds have the auditory system in the caudal telen- cephalon, which is conserved among a wide range of taxonomic orders of birds. Field L2 (which is analo- gous to mammalian primary auditory cortex) receives Fig. 1. A schematic diagram of a composite of parasagittal input from the thalamic auditory nucleus ovoidalis sections of the Budgerigar (a parrot) brain. Drawing gives ap- and constitutes the caudal forebrain auditory system proximate positions of nuclei and brain regions. Thick black that includes fields L1 and L3, the caudomedial arrows represent the major ascending auditory projections. nidopallium (NCM, formerly caudomedial neostria- The caudal forebrain auditory system comprises primary (field tum, Reiner et al. 2004), and the caudomedial L) and secondary (the NCM and the CMM) regions. Thick gray arrows represent a lemniscal projection to the rostral mesopallium (CMM, formerly caudomedial hypers- forebrain auditory system including the NF. The NLC, as the triatum or CMHV, Reiner et al. 2004) (Fig. 1, Jarvis HVC in songbirds, is a nucleus in the song system and re- et al. 2000). This system sends auditory information ceives indirect auditory input from the NF. The HVC in song- to brain nuclei in the so-called ‘song system’ which birds receives indirect auditory input from the primary and are considered to be involved in song production, in secondary regions in the caudal forebrain auditory system addition to their role in song perception and learning (Vates et al. 1996). Thin black arrows indicate the indirect (Nottebohm 2000). In recent studies, the expression connection between the primary region in the caudal forebrain of certain immediate early genes (IEGs) was ana- auditory system and the song system in the Budgerigar. The connection between the secondary regions (i.e., the NCM and lyzed in the forebrain of female birds that had been the CMM) and the song system remains to be confirmed in exposed to conspecific song in the Canary (Serinus parrots. canaria, Ribeiro et al. 1998; Leitner et al. 2005), the Abbreviations: Cb, Cerebellum; CMM, caudomedial mesopal- Starling (Sturnus vulgaris, Duffy et al. 1999; Gentner lium (formerly caudomedial hyperstriatum or CMHV); Hp, et al. 2001; Sockman et al. 2002; Sockman et al. Hippocampus; L1, L2, and L3, field L subdivisions; HVC, 2005), the Zebra Finch (Taeniopygia guttata, Terpstra used as a proper name; LL, nucleus of the lateral lemniscus; et al. 2001; Bailey et al. 2002; Avey et al. 2005; NCM, caudomedial nidopallium (formerly caudomedial neos- triatum); NF, frontal nidopallium; NLC, central nucleus of the Bailey & Wade 2005; Terpstra et al. 2006), the Bud- lateral nidopallium; Ov, nucleus ovoidalis of the thalamus. gerigar (Melopsittacus undulatus, a parrot, Eda- Scale bar2 mm. Based on Brauth et al. 1987, Jarvis & Mello Fujiwara et al. 2003), the White Crowned Sparrow 2000, Brauth et al. 2002, and Plummer & Striedter 2002. (Zonotrichia leucophrys, Maney et al. 2003), the Black-Capped Chickadee (Poecile atricapilla, Phill- number of different syllables to which female more et al. 2003) and the House Finch (Carpodacus budgerigars were exposed, suggesting that the NCM mexicanus, Hernandez & MacDougall-Shackleton is involved in the perception of song complexity in 2004). Expression of these IEGs or their protein female birds. Mello et al. (1995) showed that ZENK product is thought to be a reflection of neuronal acti- expression in the NCM of male zebra finches in- vation (Sagar et al. 1988). IEG studies of female creases with repetition of a single song stimulus over birds revealed brain regions which are involved in the first 30 min of presentation. The level of expres- song perception. These regions include the NCM and sion then returns to baseline levels despite continued the CMM in the auditory system (Bolhuis & Eda-Fu- stimulation with the same song. The study by Mello jiwara 2003), and furthermore, the hippocampus out- et al. (1995) demonstrates that the NCM shows habit- side the auditory system and the song system (Bailey uation to the repeated stimulus, which is a general et al. 2002). Eda-Fujiwara et al. (2003) showed that phenomenon of the neural system. A monotonous the expression of the IEG known as ZENK in the song with a small repertoire size might lead to habitu- NCM correlated significantly and positively with the ation of the neural response to the song in the NCM

24 Song preferences and gene expression in brains

Fig. 2. Sonograms of part of a song of the Budgerigar. Budgerigar song consists of syllables that are diverse in acoustic structure. Small letters indicate syllable types. Upper: The mimicry of a Japanese word, SA-KU-RA is en- meshed in the song. Lower: A compound of an abbreviated pattern (SA-KU) and a trained pattern (O-HA-YO) is vocalized in the song. of females. The neuronal responses to male song with with three Japanese trisyllables: ‘O-HA-YO’, ‘SA- a larger repertoire size would be expected to be less KU-RA’, and ‘SU-I-KA’ by a live tutor (a female ex- susceptible to habituation in the NCM of females. perimenter). They developed song and used Japanese Males singing complex songs might have exploited words as song syllables (Fig. 2). Mimetic syllables the bias in the NCM of females to stimulate the NCM contained, in addition to matched tutored patterns neurons more effectively. (‘O-HA-YO’, ‘SA-KU-RA’, and ‘SU-I-KA’), abbre- viations of tutored patterns (e.g., ‘O-HA’, ‘SA-KU’, VOCAL MIMICRY AND ‘KU-RA’, ‘SU-I) and compounds of trained pat- SONG COMPLEXITY terns (e.g., ‘O-HA-SA-KU’, ‘O-HA-KU-RA’). The Budgerigar can enlarge the syllable repertoire size by Vocal learning is found in three avian taxa: song- arranging the memorized patterns as well as by sim- birds (Passeriformes: Oscines), parrots (Psittaci- ply reproducing tutored patterns. formes, Gahr 2000), and hummingbirds (Trochilo- formes, Jarvis et al. 2000). Males usually learn SELECTIVITY FOR CONSPECIFIC OVER sounds of their own species (Marler & Peters 1977). HETEROSPECIFIC VOCALIZATIONS Young males are considered to have innate predispo- IN FEMALE BRAINS sitions that guide the learning of conspecific song. On the other hand, some passerine birds mimic the vocal- As mentioned above, complex male song is more izations of other species (Baylis 1982). An extensive effective to females than simple song in many bird study of the migratory Marsh Warbler Acrocephalus species, while females respond more to conspecific palustris showed that males mimicked vocalizations song than heterospecific song. In the song of mimick- of 102 and 113 species found in their breeding and ing species, complex song containing many het- wintering areas, respectively (Lemaire 1975, erospecific sounds becomes to lose conspecific char- Dowsett-Lemaire 1979). It is known that the mimick- acteristics. This is a problem for females which ing birds such as the Marsh Warbler, the Black- should be under strong selection to avoid mating with browed Reed Warbler (Acrocephalus bistrigiceps, males of other species. It remains to be investigated Hamao & Eda-Fujiwara 2004), and the Starling whether females in mimicking species respond (Hausberger et al. 1991) use mimetic sounds as their strongly to complex song with heterospecific sounds. song syllables and can enlarge their syllable reper- Discrimination between conspecific and heterospe- toire size by vocal mimicry. The Budgerigar (a par- cific vocalizations is biologically important in female rot) in captivity is known to mimic heterospecific birds, thus research efforts have been directed at re- sounds including human words (Eda-Fujiwara & vealing neural mechanism underling the discrimina- Okumura 1992). In the study of Eda-Fujiwara & tion. IEG studies of female birds have revealed brain Okumura (1992), young Budgerigars were presented regions which play a role in discriminating conspe-

25 H. E. FUJIWARA et al. cific from heterospecific vocalizations. Conspecific study, that neurons in the caudal mesopallium (CM), song elicited higher IEG expression than heterospe- the area that comprises CMM, respond more strongly cific song in the NCM of female Zebra Finches to conspecific song than to synthetic song designed to (Mello et al. 1992; Bailey et al. 2002; Bailey & Wade mimic the temporal and spectral features of natural 2005). Presentation of each type of syllables nor- conspecific song. Neurons in the CMM is considered mally present in the Canary song results in each of to be sensitive to the acoustic feature commonly distinct patterns of IEG expression in the NCM found in conspecific song, but not in non-conspecific (Ribeiro et al. 1998). The pattern of IEG expression song, and to play a role in discriminating conspecific (neural representation) of one type, the whistle sylla- from heterospecific song. Taken together, the avail- ble was drastically different from the representation able evidence suggests that the CMM is important for of the artificial whistle of a comparable frequency. the discrimination of conspecific from heterospecific There remain some unidentified acoustic features of vocalizations in female songbirds. Furthermore, it the conspecific whistle syllable that are particularly was found that there is substantial IEG expression in salient to the response of the NCM neurons. Such the CMM of the Ring Dove (Streptopelia risoria), a subtle acoustic features specific to the conspecific non-songbird that does not need to learn its vocaliza- whistle is considered to produce the topographical tions (Terpstra et al. 2005). Conspecific vocalization pattern of neural activation in the NCM that is differ- elicited significantly higher IEG expression than si- ent from the pattern for the artificial non-conspecific lence in the CMM, while heterospecific vocalization whistle. These IEG studies suggest that the NCM is did not. Thus, the CMM may play a role in discrimi- involved in discriminating conspecific from het- nating conspecific from heterospecific vocalizations erospecific vocalizations. A recent study gives a clue in female birds among a wide range of taxonomic to the question whether early song experience plays a groups. role in adult selectivity for conspecific over het- Recently, Terpstra et al. (2006) exposed female erospecific song in the NCM. Female Zebra Finches Zebra Finches to their fathers’ song early in life and, reared with little or no exposure to song have fewer later when adult, reexposed them to the fathers’ song. dendritic spines per unit length of dendrites in the These females that were reexposed showed signifi- NCM, suggesting that the NCM is involved in audi- cantly greater expression of ZENK in the CMM than tory learning. The selectivity for conspecific song in controls that were exposed to novel song. In female the NCM may be shaped through auditory learning in Zebra Finches the CMM may be the neural substrate female Zebra Finches. for the representation of the memory of their fathers’ In the CMM, another auditory region close to the song. In studies to examine ZENK expression to con- NCM, Bailey et al. (2002) did not show a significant specific song in the CMM, conspecific song stimuli difference in IEG expression between females ex- would result in different ZENK expression patterns posed to conspecific song and birds exposed to het- depending on that they are familiar or novel to sub- erospecific song in the Zebra Finch. However, lesions ject females. Thus, future investigation of species dis- of the CMM resulted in a loss of discrimination be- crimination will require cautions for song stimuli tween conspecific and heterospecific vocalizations in used in playback experiments. female Zebra Finches (MacDougall-Shackleton et al. Conspecific song elicited higher IEG expression 1998). These different findings could be due to sam- than heterospecific song in the hippocampus of adult pling or lesioning in different parts of the CMM. Her- female Zebra Finches (Bailey et al. 2002). Such dif- nandez and MacDougall-Shackleton (2004) exam- ference, however, was not found in other IEG studies ined IEG expression in the NCM and the CMM of fe- using adult Zebra Finches (male: Terpstra et al. 2004; male House Finches exposed to conspecific or het- female: Terpstra et al. 2001, 2006). A possible expla- erospecific vocalizations. They did not analyze the nation of these different findings is the suggestion NCM and the CMM separately, and found that con- that non-auditory stimuli (such as a change in envi- specific song elicited significantly higher IEG expres- ronmental context) can influence IEG expression sion than heterospecific song in the broad area con- (Kruse et al. 2004). The birds in the study of Bailey sisting of the NCM and the CMM. Figure 3A of Her- et al. (2002) had a relatively short period of pre-isola- nandez and MacDougall-Shackleton (2004) suggests tion and were exposed to song in a novel environ- that there might be a difference in the CMM. Grace et ment, which may have affected IEG expression in the al. (2003) have shown, in their electrophysiological hippocampus. Whether the hippocampus plays a role

26 Song preferences and gene expression in brains in the discrimination remains to be further investi- Bailey DJ, Rosebush JC & Wade J (2002) The hip- gated. pocampus and caudomedial neostriatum show selec- Female songbirds have the song system, even tive responsiveness to conspecific song in the female though normally they do not sing. Brenowitz (1991) zebra finch. J Neurobiol 52: 43–51. tested whether nuclei in the song system play a role Bailey DJ & Wade J (2005) FOS and ZENK responses in song perception in females. In female Canaries, le- in 45-day-old zebra finches vary with auditory stimu- sions of the nucleus HVC, a site of sensory and motor lus and brain region, but not sex. Behav Brain Res, integration in the song system, result in the loss of 162: 108–115. their ability to discriminate conspecific from het- Baylis JR (1982) Avian vocal mimicry: its function and erospecific song. Contrary to this study, in female evolution. In: Kroodsma DE & Miller EH (eds) Acoustic Communication in Birds, Vol. 2 Zebra Finches, lesions of the HVC did not disrupt . pp 51–93. Academic Press, New York. their ability to discriminate conspecific from het- Bolhuis JJ & Eda-Fujiwara H (2003) Bird brains and erospecific song (MacDougall-Shackleton et al. songs: neural mechanisms of birdsong perception and 1998). There is no available data about nuclei in the memory. Anim Biol 53: 129–145. song system from IEG studies, because exposure to Brauth S, Liang W, Roberts TF, Scott LL & Quinlan song does not lead to IEG expression in nuclei in the EM (2002) Contact-call driven Zenk protein induc- song system. Song production by itself does lead to tion and habituation in telencephalic auditory path- IEG expression in nuclei in the song system. With the ways in the budgerigar (Melopsittacus undulatus): limited studies, it is not clear whether nuclei in the implications for understanding vocal learning song system are involved in discriminating conspe- processes. Learning Mem 9: 76–88. cific from heterospecific song. Brauth SE, McHale CM, Brasher CA & Dooling RJ (1987) Auditory pathway in the budgerigar. I. Thal- CONCLUSIONS amo-telencephalic projections. Brain Behav Evol 30: 174–199. IEG expression analysis in the field of neurobiol- Brenowitz EA (1991) Altered perception of species-spe- ogy has led to the identification of brain regions that cific song by female birds after lesions of a forebrain are activated in association with hearing song and nucleus. Science 251: 303–305. that are likely involved in song perception. Recent Catchpole CK & Slater PJB (1995) Bird Song: Biologi- evidence suggests the involvement of the NCM and cal Themes and Variations. Cambridge University the CMM of female brains in the perception of male Press, Cambridge. song. The suggested role of the NCM in the percep- Dowsett-Lemaire F (1979) The imitative range of the tion of song complexity supports the sensory ex- song of the Marsh Warbler Acrocephalus palustris, ploitation hypothesis to explain the origin of syllable with special reference to imitations of African birds. repertoires of male song, which has been discussed in Ibis 121: 453–468. the field of behavioral ecology. Males of some Duffy DL, Bentley GE & Ball GF (1999) Does sex or photoperiodic condition influence ZENK induction in species make their song more complex through vocal response to song in European starlings? Brain Res mimicry. Species-specificity and vocal mimicry in 844: 78–82. birdsong have been regarded as a paradox. Our Eda-Fujiwara H & Okumura H (1992) The temporal knowledge of the neural substrate of song perception pattern of vocalizations in the budgerigar Melopsitta- may be useful to explain this paradox in future. Fu- cus undulatus. J Yamashina Inst Ornithol 24: 18–31. ture research is necessary to focus on a possible role Eda-Fujiwara H, Satoh R, Bolhuis JJ & Kimura T for the NCM and the CMM in discriminating conspe- (2003) Neuronal activation in female budgerigars is cific from heterospecific vocalizations. localized and related to male song complexity. Eur J Neurosci 17: 149–154. REFERENCES Gahr M (2000) Neural song control system of hum- mingbirds: comparison to swifts, vocal learning Avey MT, Phillmore LS & MacDougall-Shackleton SA (songbirds) and nonlearning (suboscines) passerines, (2005) Immediate early gene expression following and vocal learning (budgerigars) and nonlearning exposure to acoustic and visual components of (dove, owl, gull, quail, chicken) nonpasserines. J courtship in zebra finches. Behav Brain Res 165: Comp Neurol 426: 182–196. 247–253. Gentner TQ & Hulse SH (2000) Female European star-

27 H. E. FUJIWARA et al.

ling preference and choice for variation in conspecific Lemaire F (1975) The song of the Marsh Warbler (Acro- male song. Anim Behav 59: 443–458. cephalus palustris): faithfulness of imitations and re- Gentner TQ, Hulse SH, Duffy D & Ball GF (2001) Re- lations with the imitated species and with the con- sponse biases in auditory forebrain regions of female geners. Gerfaut 65: 3–28 (in French with English songbirds following exposure to sexually relevant summary). variation in male song. J Neurobiol 46: 48–58. MacDougall-Shackleton SA, Hulse SH & Ball GF Grace JA, Amin N, Singh NC & Theunissen FE (2003) (1998) Neural bases of song preferences in female Selectivity for conspecific song in the zebra finch au- zebra finches (Taeniopygia guttata). Neuroreport 9: ditory forebrain. J Neurophysiol 89: 472–487. 3047–3052. Hamao S & Eda-Fujiwara H (2004) Vocal mimicry by Maney DL, MacDougall-Shackleton EA, MacDougall- the Black-browed Reed Warbler Acrocephalus bist- Shackleton SA, Ball GF & Hahn TP (2003) Immedi- rigiceps: objective identification of mimetic sounds. ate early gene response to hearing song correlates Ibis 146: 61–68. with receptive behavior and depends on dialect in a Hasselquist D, Bensch S & von Schantz T (1996) Corre- female songbird. J Comp Physiol A 189: 667–674. lation between male song repertoire, extra-pair pater- Marler P & Peters S (1977) Selective vocal learning in a nity and offspring survival in the great reed warbler. sparrow. Science 198: 519–521. Nature 381: 229–232. Mello C, Nottebohm F & Clayton D (1995) Repeated Hausberger M, Jenkins PF & Keene J (1991) Species- exposure to one song leads to a rapid and persistent specificity and mimicry in bird song: are they para- decline in an immediate early gene’s response to that doxes? Behaviour 117: 53–81. song in zebra finch telencephalon. J Neurosci 15: Hernandez AM & MacDougall-Shackleton SA (2004) 6919–6925. Effects of early song experience on song preferences Mello CV, Vicario DS & Clayton DF (1992) Song pres- and song control and auditory brain regions in female entation induces gene expression in the songbird fore- house finches (Carpodacus mexicanus). J Neurobiol brain. Proc Natl Acad Sci USA 89: 6818–6822. 59: 247–258. Mountjoy DJ & Lemon RE (1996) Female choice for Jarvis ED & Mello CV (2000) Molecular mapping of complex song in the European starling: a field experi- brain areas involved in parrot vocal communication. J ment. Behav Ecol Sociobiol 38: 65–71. Comp Neurol 419: 1–31. Nottebohm F (2000) The anatomy and timing of vocal Jarvis ED, Ribeiro S, da Silva ML, Ventura D, Vielliard learning in birds. In: Hauser MD & Konishi M (eds) J & Mello CV (2000) Behaviourally driven gene ex- The Design of Animal Communication. pp 63–110. pression reveals song nuclei in hummingbird brain. MIT Press, Cambridge. Nature 406: 628–632. Phillmore LS, Bloomfield LL & Weisman RG (2003) Kroodsma DE (1976) Reproductive development in a Effects of songs and calls on ZENK expression in the female songbird: differential stimulation by quality of auditory telencephalon of field- and isolate-reared male song. Science 192: 574–575. black capped chickadees. Behav Brain Res 147: Kruse AA, Stripling R & Clayton DF (2004) Context- 125–134. specific habituation of the zenk gene response to song Plummer TK & Striedter GF (2002) Brain lesions that in adult zebra finches. Neurobiol Learn Mem 82: impair vocal imitation in adult budgerigars. J Neuro- 99–108. biol 53, 413–428. Lampe HM & Sætre GP (1995) Female pied flycatchers Ribeiro S, Cecchi GA, Magnasco MO & Mello CV prefer males with larger song repertoires. Proc R Soc (1998) Toward a song code: evidence for a syllabic Lond B 262: 163–167. representation in the canary brain. Neuron 21: Lauay C, Komorowski RW, Beaudin AE & Devoogd 359–371. TJ. (2005) Adult female and male zebra finches show Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, distinct patterns of spine deficits in an auditory area Kuenzel W, Medina L, Paxinos G, Shimizu T, and in the song system when reared without exposure Striedter GF, Wild M, Ball GF, Durand S, to normal adult song. J Comp Neurol 487: 119–126, Guentuerkuen O, Lee DW, Mello CV, Powers A, 2005. White SA, Hough G, Kubikova L, Smulders TV, Leitner S, Voigt C, Metzdorf R & Catchpole CK (2005) Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu Immediate early gene (ZENK, Arc) expression in the J, Siang C & Jarvis ED (2004) Revised nomenclature auditory forebrain of female canaries varies in re- for avian telencephalon and some related brainstem sponse to male song quality. J Neurobiol 64: nuclei. J Comp Neurol 473: 377–414. 275–284. Ryan MJ (1998) Sexual selection, receiver biases, and

28 Song preferences and gene expression in brains

the evolution of sex differences. Science 281: integration of mate-choice cues in European starlings. 1999–2003. J Neurobiol 62: 72–81. Sagar SM, Sharp FR & Curran T (1988) Expression of Terpstra NJ, Bolhuis JJ & den Boer-Visser AM (2004) c-fos protein in brain: metabolic mapping at the cellu- An analysis of the neural representation of birdsong lar level. Science 240: 1328–1331. memory. J Neurosci 24: 4971–4977. Searcy WA (1992a) Measuring responses of female Terpstra NJ, Bolhuis JJ, den Boer-Visser AM & ten Cate birds to male song. In: McGregor PK (ed) Playback C (2005) Neuronal activation related to auditory per- and Studies of Animal Communication. pp 175–189. ception in the brain of non-songbird, the Ring Dove. J Plenum Press, New York. Comp Neurol 488: 342–351. Searcy WA (1992b) Song repertoire and mate choice in Terpstra NJ, Bolhuis JJ, van der Burg JJM & den Boer- birds. Am Zool 32: 71–80. Visser AM (2001) Song learning-related immediate Searcy WA & Yasukawa K (1996) Song and Female early gene expression in the forebrain of zebra finch Choice. In: Kroodsma DE & Miller EH (eds) Ecology females. Behav Pharmacol 12: S101. and Evolution of Acoustic Communication in Birds. Terpstra NJ, Bolhuis JJ, Riebel K, van der Burg JM & pp 454–473. Cornell Univ Press, New York. den Boer-Visser AM (2006) Localized brain activa- Sockman KW, Gentner TQ & Ball GF (2002) Recent tion specific to auditory memory in a female song- experience modulates forebrain gene expression in re- bird. J Comp Neurol 494: 784–791. sponse to mate-choice cues in European starlings. Vates GE, Broome BM, Mello CV & Nottebohm F Proc R Soc Lond B 269: 2479–2485. (1996) Auditory pathways of caudal telencephalon Sockman KW, Gentner TQ & Ball GF (2005) Comple- and their relation to the song system of adult male mentary neural systems for the experience-dependent zebra finches. J Comp Neurol 366: 613–642.

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