Temporary inactivation of NCM, an auditory region, increases social interaction and decreases song perception in female zebra finches

Behavioural Processes 108 (2014) 65–70

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Temporary inactivation of NCM, an auditory region, increases social interaction and decreases song perception in female zebra finches Michelle L. Tomaszycki a,∗ , Sara K. Blaine b,1 a b

Department of Psychology, Wayne State University, 5057 Woodward Avenue, 7th Floor, Detroit, MI 48202, USA Department of Psychology and Neuroscience, University of Colorado, Boulder, Muenzinger D244, 345 UCB, Boulder, CO 80309-0345, USA

a r t i c l e

i n f o

Article history: Received 21 April 2014 Received in revised form 18 September 2014 Accepted 20 September 2014 Available online 30 September 2014 Keywords: NCM Zebra finch Female Song perception Partner preference

a b s t r a c t The caudomedial nidopallium (NCM) is an important site for the storage of auditory memories, particularly song, in passerines. In zebra finches, males sing and females do not, but females use song to choose mates. The extent to which the NCM is necessary for female mate choice is not well understood. To investigate the role of NCM in partner preferences, adult female zebra finches were bilaterally implanted with chronic cannulae directed at the NCM. Lidocaine, a sodium channel blocker, or saline (control) was infused into the NCM of females using a repeated measures design. Females were then tested in 3 separate paradigms: song preference, sexual partner preference, and pairing behavior/partner preference. We hypothesized that lidocaine would increase interactions with males by decreasing song discrimination and that this would be further evident in the song discrimination task. Indeed, females, when treated with lidocaine, had no preference for males singing unaltered song over males singing distorted song. These same females, when treated with saline, demonstrated a significant preference for males singing normal song. Furthermore, females affiliated with males more after receiving lidocaine than after receiving saline in the pairing paradigm, although neither treatment led to the formation of a partner preference. Our results support the hypothesis that NCM plays an important role not only in song discrimination, but also affiliation with a male. © 2014 Elsevier B.V. All rights reserved.

1. Introduction For group-living species that form long-term monogamous bonds with other individuals, social recognition is crucial for survival and reproductive success. The medial amygdala and the hippocampus are responsible for social recognition in mice (Ferguson et al., 2001). In prairie voles, the nucleus accumbens and prefrontal cortex are tightly linked to the formation of partner preferences in females (Wang and Aragona, 2004), whereas the ventral pallidum and lateral septum facilitate partner preferences in males (Young and Wang, 2004). Regions responsible for the formation of partner preferences in mammals are connected to the olfactory bulb, and are therefore involved in olfactory recognition (Hammock and Young, 2006). Not all monogamous species rely on olfactory cues for social recognition, and thus animals that rely on different signal modalities likely have different neural underpinnings of social recognition. Specifically, the brain regions responsible for the

∗ Corresponding author. Tel.: +1 313 577 0341; fax: +1 313 577 7636. E-mail address: [email protected] (M.L. Tomaszycki). 1 Present address: http://dx.doi.org/10.1016/j.beproc.2014.09.031 0376-6357/© 2014 Elsevier B.V. All rights reserved.

retention and acquisition of social memories would be expected to be quite different in species that rely more on visual and auditory cues than on olfactory ones. Thus, further research is necessary to determine the neural basis of partner preferences across species. Songbirds are well-suited to studying the neural basis of auditory recognition associated with partner preferences. Zebra finches, in particular, are a highly social, colonially breeding songbird that forms long-term pair bonds (Zann, 1996). Zebra finches recognize a mate after many weeks of acoustic and visual separation (Immelmann, 1959), but the neural substrate for this recognition is not well understood. Memories for individual songs are consolidated and stored in the caudomedial nidopallium (NCM) (Mello et al., 1992, 2004; Bolhuis et al., 2000; Woolley and Doupe, 2008; Phan et al., 2006), a telencephalic region that is part of a circuit that is homologous to the mammalian auditory cortex (Doupe and Kuhl, 1999). Different song syllable types evoke distinct patterns of immediate early gene activation in the canary NCM (Mello et al., 2004). Electrophysiological studies further confirm the importance of NCM in song processing (Jarvis et al., 1995; Bolhuis and Gahr, 2006; Terpstra et al., 2006). Specifically, NCM is more active during unfamiliar song than during familiar song (Woolley and Doupe, 2008; Terpstra et al., 2006).

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Furthermore, hearing conspecific songs causes an increase in the number of cells in NCM immuno-positive for the immediate early gene ZENK over hearing heterospecific songs, in both juvenile and adult female zebra finches (Bailey et al., 2002; Bailey and Wade, 2003; Gentner et al., 2001). ZENK-ir in females is also higher in response to high quality compared to low quality conspecific song (Tomaszycki et al., 2006; Leitner et al., 2005). This ability to discriminate between songs may require experience (Clayton, 1988; Lauay et al., 2004; Tomaszycki et al., 2006; Hernandez et al., 2008; Braaten et al., 2006; Riebel, 2000). Specifically, the number of syllables that males copy from a song tutor correlate with the number of cells immunopositive for ZENK and c-Fos, another immediate early gene, in NCM (Bolhuis et al., 2000, 2001). Estradiol in the NCM also increases rapidly during song processing (Remage-Healey and Joshi, 2012; Remage-Healey et al., 2008). These effects occur not only in males, but also in females. Taken together, these results suggest that NCM plays an important role in song recognition in females. Behaviorally, adult female songbirds can make fine-grained distinctions between songs (Vernaleo and Dooling, 2011; Nagel et al., 2010; Cynx, 1993; Cynx et al., 1990; Clayton, 1988; Miller, 1979). This ability is particularly important for female zebra finches, who choose long-term mates on the basis of song quality (Tomaszycki and Adkins-Regan, 2005). Thus, females distinguish between song quality and quantity (Tomaszycki and Adkins-Regan, 2005), use this ability to choose mates, and this choice likely involves the NCM. The present study directly investigated the role of NCM in female partner preferences. To accomplish this, we temporarily inactivated NCM in adult females with lidocaine, a sodium channel blocker. We chose this method to allow for a repeated measures design. HVC lesions decrease preferences for conspecific over heterospecific song in canaries (Brenowitz, 1991; Del Negro et al., 1998) and reduce ZENK-ir in NCM (Lynch et al., 2013). GABA infusions into another auditory region, the caudomedial mesopallium (CMM), decrease electrophysiological responses in HVC to a male’s own song (Bauer et al., 2008). In female zebra finches, lesions to the CMM reduce the ability to discriminate conspecific from heterospecific song, whereas lesions to HVC do not alter female song discrimination (MacDougall-Shackleton et al., 1998). Lesions of NCM in males decrease recognition of familiar (tutor) song (Gobes and Bolhuis, 2007) and impair the maintenance of song (Canopoli et al., 2014). No study, to the best of our knowledge, has tested the effects of inactivation of NCM on female song discrimination and partner preference formation. Females were tested in three different paradigms. First, to test the effects of temporary inactivation on song perception, females were given the choice between males singing normal song and those singing distorted song [males that had their right tracheosyringeal nerve transected (TS)]. Songs by TS males are the same duration and rate as SHAM (control) songs, but tonal notes are absent (Tomaszycki and Adkins-Regan, 2005). Untreated females prefer SHAM males over TS males (Tomaszycki and Adkins-Regan, 2005). Next, to determine how song discrimination relates to female mate choice, females were allowed to freely interact with a male and were tested the next day for the formation of a partner preference by presenting the female with the familiar male and an unfamiliar male in a 2-choice paradigm. This paradigm is similar to the way in which partner preferences are tested in prairie voles (Young and Wang, 2004). Finally, to probe for behavioral specificity of the lesion, females were tested for a sexual partner preference (given the choice between a male and a female). We hypothesized that inactivation of NCM would decrease preferences for normal over TS song, and that by decreasing song perception, this would increase affiliation with males (by decreasing selectivity), but also decrease a female’s preference for a familiar partner, thereby indicating that the NCM is necessary for the formation of

a partner preference. Finally, we expected that temporary inactivation of NCM would not affect sexual partner preferences, since plumage coloration would aid in the discrimination of males from females, and NCM was only predicted to alter auditory processing. 2. Materials and methods 2.1. Subjects Subjects were adult female wild-type zebra finches (Taeniopygia guttata) that had no prior sexual or pairing experience and had been raised by their parents in social aviaries until sexual maturity. All subjects were identified by leg bands of various colors that are not known to influence mate choice. A total of 9 female subjects were implanted with bilateral cannulae directed at the NCM. 2.2. Housing Female subjects were housed in 0.6 m × 0.4 m × 0.35 m wire mesh cages between tests (3 females per cage), since social isolation can cause deficits in social recognition (Kogan et al., 2000). Rooms were maintained on a 14:10 light cycle at a consistent temperature (24 ◦ C) and humidity (50%) level. Food and water were available ad libitum. Additionally, their diet was supplemented with hard boiled eggs twice per week. 2.3. Cannulation techniques All procedures were approved by the IACUC at Cornell University. Birds were anesthetized with 5 mg/kg xylazine and 87.5 mg/kg ketamine. Using standard stereotaxic techniques, two stainless steel cannulae (26-gauge, Plastics One, Roanoke, VA) were affixed to the skull with cyanoacrylate glue and dental cement. Stereotaxic coordinates were obtained from the Nixdorf-Bergweiler and Bischof zebra finch atlas. We positioned the cannulae in the dorsalventral plane such that the ventral tip of each cannula contacted the dorsal surface of NCM in each hemisphere (0.7 mm rostral to lambda, 1 mm lateral, 1 mm ventral to the brain surface). Females were given 2 weeks to recover. 2.4. Lidocaine infusion Subjects were habituated to the paradigm in 4 trials (involving restraint, infusions, and a 2-choice paradigm) prior to testing. Subjects received bilateral 0.2 ␮l infusions of either 2% lidocaine (Vedco, Inc., St. Joseph, MO) or sterile saline (0.9%) via a 32-gauge needle attached to a 5 ␮l Hamilton syringe prior to each behavioral test. For the 3rd experiment (a 2-day test), infusions were only given on the first day of testing. Infusions were administered manually over the course of 1 min, and the needle was left in place for an additional min to allow for fluid dispersal. Lidocaine blocks sodium channels and these effects persist for about an hour (Lomber, 1999; Coleman et al., 2007). Subjects appeared normal after lidocaine infusion; all females were able to perch normally and fly. 2.5. Vocal disruption techniques A total of 16 males (8 in each group) underwent either the experimental or SHAM surgery. Surgeries were conducted as in (Tomaszycki and Adkins-Regan, 2005). Briefly, males were anesthetized using 5 mg/kg xylazine and 87.5 mg/kg ketamine. In the TS surgery, a 1 mm section of the right tracheosyringeal nerve is cut and removed. In the SHAM surgery, the skin of the neck was cut (as in the TS surgery) and resealed. In both cases, the wound was sealed with Vetbond tissue glue (3M, St. Paul, MN). Males behaved

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normally within hours of these surgeries. Males were allowed at least 48 h to recover prior to use in the experiments. 2.6. Behavioral testing Subjects were tested using a repeated measures design. Testing order and drug treatment were randomized across subjects. The two observers (MLT and SKB) were blind to the drug condition. Each female received each condition twice, to counterbalance for side presentation in the 2-choice tests. 2.6.1. Song perception Females were infused, placed in the center compartment (0.6 m × 0.4 m × 0.35 m) of a 3-compartment testing chamber, and allowed to habituate for 10 min. Then, 2 males were placed into the side chambers (0.6 m × 0.4 m × 0.35 m): one singing normal song (SHAM) and one singing TS song. The amount of time the female spent nearest to, and facing, each male was recorded over 15 min. Proximity zones were marked off on the perch that ran length-wise through the middle of the center compartment. The closest fourth of the center compartment nearest to each male was considered a proximity zone. Perches also ran length-wise through the middle of the side compartments. Although we did not quantitatively observe singing, all males sang and our previous research indicates that courtship rates by TS and SHAM males are similar in these conditions (Tomaszycki and Adkins-Regan, 2005). Indeed, no courtship differences were apparent. 2.6.2. Sexual partner preferences Females were placed into the center compartment of the 2choice apparatus (described in Section 2.6.1) and allowed to habituate for 10 min. The time the female spent nearest to, and facing, the male or the female was recorded over 15 min. 2.6.3. Partner preferences On the first day of testing, each female subject received an infusion and was placed in a cage (0.6 m × 0.4 m × 0.35 m) with a male and allowed to interact for 1 h. This cage contained a nest box and plenty of nesting materials. The animals were observed for 15 min halfway through the test. Courtship and pairing behaviors were measured as in our other work (Pedersen and Tomaszycki, 2012; Smiley et al., 2012; Vahaba et al., 2013) and are described in Table 1. Twenty-four hours later, each female was presented with the familiar partner and an unfamiliar male (matched for physical characteristics) in the 2-choice apparatus described in Section 2.6.1. The amount of time the female spent on the perch nearest to, and facing, each male was recorded over 15 min. Table 1 Behaviors observed in a study of the effects of temporary inactivation of NCM on female partner preferences. Behavior

Male- or female- typical behavior?

Measured duration or frequency?

Description of behavior

Directed singing Undirected singing

Male Male

Duration Duration

Dancing

Male

Frequency

Clumping Allopreening Beak wiping

Both Both Female

Duration Frequency Frequency

Tail quiver

Female

Frequency

Copulation

Male

Frequency

Song directed at a female Song not directed at a female Hop-Twist-Pivot directed at a female Direct physical contact Mutual grooming Wiping beak on perch while male sings Rapid shaking of tail feathers Mating

Fig. 1. Placement of cannulae in female zebra finches. In 8 subjects, the cannulae were correctly placed in NCM. In one female, the cannulae were misplaced (indicated by an *). This female was excluded from the analyses.

2.7. Histology After the experiments, all females were infused with 0.2 ␮l of 5% Fluorescein into each cannula to determine the area of dispersion of the lidocaine infusions throughout the experiment. They were then deeply anesthetized and perfused transcardially with 0.9% phosphate buffered saline and 4% paraformaldehyde. Tissue was lightly counterstained with Nissl to aid in the localization of cannula placement, along with the use of the Nixdorf-Bergweiler and Bischof zebra finch atlas. Placement of cannulae was confirmed by examining alternate 40 ␮m sections using a fluorescence microscope (Nikon E800). In 8 subjects, cannulae were successfully directed at NCM (see Fig. 1). In one case, the cannulae were positioned dorsally to NCM, in CMM. This female’s data were therefore excluded from the analyses. Similar to findings in our previous work (Shiflett et al., 2004a,b), the infusions affected a mean area of 0.74 ± 0.06 mm in the medial–lateral plane and 0.5 ± 0.04 mm in the rostral–caudal plane. 2.8. Data analysis Data were analyzed using SPSS (version 19.0, SPSS Inc., Chicago, IL). To assess partner or song preferences, we compared the proportion of time spent nearest one choice compared to the other choice within each treatment group using repeated measures ANOVAs on arc sine transformed proportions to achieve normality (the second presentation of the stimuli was analyzed, since the first and second presentations did not significantly differ from each other). To assess differences in affiliation with the male during saline and lidocaine treatments in the partner preference experiment, we analyzed differences in the amount of time or

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Proportion of time spent near each male

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0.9

SHAM

0.8

TS

0.7 0.6 0.5 0.4

*

0.3 0.2 0.1 0 Control

Lidocaine

Fig. 2. The effects of temporary inactivation of NCM on female song preferences. Females were exposed to live SHAM males singing normal song or males who had their tracheosyringeal nerve transected (TS). *Significance at the p < 0.05 level.

frequency in behaviors on day 1 using Wilcoxon Signed Ranks tests.

3. Results

Fig. 3. The amount of time spent in direct physical contact (clumping) with a male on day 1 of testing after receiving an intra-NCM infusion of either saline or lidocaine in female zebra finches. N = 8. *Significance at the p < 0.05 level. Table 2 Means ± standard errors for behaviors observed in a study of the effects of temporary inactivation of NCM on female partner preferences.

3.1. Song perception We hypothesized that lidocaine would impair female preferences for SHAM males over TS males. When females were treated with saline, they spent a significantly greater proportion of time near SHAM males than TS males, F(1,7) = 5.62, p = 0.049 (see Fig. 2). In contrast, when these same females were treated with lidocaine, they spent a similar proportion of time near SHAM males and TS males, F(1,7) = 0.03, p = 0.87 (see Fig. 2).

3.2. Sexual partner preferences Due to the presence of visual cues (males and females differ greatly in plumage coloration), we predicted that temporary inactivation of NCM would not affect sexual partner preferences. Surprisingly, when females were treated with either saline or lidocaine, the proportion of time they spent near the male (saline: 0.68 ± 0.11; lidocaine: 0.66 ± 0.12) or the female (saline: 0.32 ± 0.11; lidocaine: 0.34 ± 0.12) did not significantly differ [saline: F(1,7) = 3.00, p = 0.13; lidocaine: F(1,7) = 1.71, p = 0.23].

Beak wiping (female behavior) Directed singing (male behavior) Dancing (male behavior)

Saline (mean ± SE)

Lidocaine (mean ± SE)

1.33 ± 0.51 18.88 ± 10.53 0.13 ± 0.13

2.93 ± 0.71 36.06 ± 11.16 0.88 ± 0.50

3.3. Partner preferences We hypothesized that lidocaine would increase interactions with the male. Indeed, when females were infused with lidocaine, they spent significantly more time clumping, or time spent in direct contact, with the male, than when they were infused with saline, Z(16) = −2.20, p = 0.03 (see Fig. 3). Females did not differ according to treatment group in the amount of time spent beak wiping, Z(16) = −1.16, p = 0.11 (see Table 2). Male behavior toward females did not differ by treatment. Although males were slightly more likely to engage in dancing bouts when females were treated with lidocaine than when they were treated with saline, this difference was not statistically significant, Z(16) = −1.73, p = 0.08 (see Table 2). Male directed singing did not differ according to female treatment, Z(16) = −1.16, p = 0.25 (see Table 2). Allopreening, tail quivers and copulations occurred

Fig. 4. The amount of time spent near familiar and unfamiliar males 24 h after receiving an intra-NCM infusion of either saline or lidocaine in female zebra finches. N = 8.

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too infrequently to permit analysis. Thus, the effects of treatment were more attributable to female choice (clumping) and not to male behavior (directed singing and dancing). Regardless of treatment, females did not form a partner preference for the familiar male on day 2, as measured by the proportion of time spent nearest to the familiar male relative to the unfamiliar male [saline: F(1,7) = 0.02, p = 0.89; lidocaine: F(1,7) = 2.24, p = 0.18; see Fig. 4].

4. Discussion The present study demonstrates that temporary inactivation of NCM affects female song discrimination and increases interaction with a male in a forced-choice paradigm. Thus, the NCM, like the CMM (MacDougall-Shackleton et al., 1998), is necessary for female processing of male song, and our results extend these findings to conspecific songs that differed in quality (TS or normal song). Given the role of the NCM in song memories (Bolhuis et al., 2000; Phan et al., 2006; Woolley and Doupe, 2008; Gobes and Bolhuis, 2007) and song maintenance in males (Canopoli et al., 2014), these findings are perhaps unsurprising. However, given that the differences between songs are attributable to a specific syllable type (i.e. the absence of tonal syllables in TS male song and the presence of these syllables in SHAM song), these findings underscore the complexity of female song discrimination. We predicted that the sexual partner preference test would not require the NCM and therefore lidocaine treatments would not affect this preference. However, in both the lidocaine and the saline conditions, although females showed opposite-sex preferences, this preference was not statistically significant. Studies that have compared sexual partner preferences have often found that females show strong opposite-sex preferences (Adkins-Regan, 2002; Adkins-Regan and Krakauer, 2000; Laplante et al., 2014). Our inability to detect differences may have been due to extended same-sex housing prior to testing, which can shift sexual partner preferences (Adkins-Regan, 2002). As we predicted, when females were allowed to interact with a single male, females showed more affiliation when they were treated with lidocaine than when they were treated with saline. This suggests that temporary inactivation of NCM may have led to a decrease in selectivity based on song. These effects were not attributable to behavior by the male, as singing and dancing by males did not differ significantly according to treatment. We further predicted that saline-treated females would form a partner preference, whereas lidocaine-treated females would not. However, neither treatment resulted in a significant preference for either the familiar or unfamiliar male. This lack of a preference for the familiar male in either the lidocaine or saline conditions is likely due to our use of a forced-choice paradigm. For example, a previous study using a forced-choice paradigm found no significant preference for the familiar partner when zebra finches were treated with an oxytocin antagonist or saline (Goodson et al., 2004). However, when zebra finches were given a choice of partners, animals treated with saline formed a pair (i.e. partner preference), but those treated with the oxytocin antagonist were less likely to do so (Klatt and Goodson, 2013; Pedersen and Tomaszycki, 2012). Since zebra finches normally live in social groups, it appears that a forced choice paradigm (in which a single female and a single male are housed together) is not the ideal means of testing partner preferences. Thus, our future work will focus on testing the role of NCM in partner preference formation using more naturalistic paradigms. Nonetheless, our results extend the role of NCM to regulating affiliation with males, likely on the basis of song quality. Indeed, females choose male mates on the basis of song quality (Tomaszycki and Adkins-Regan, 2005), and the present results

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suggest that this choice may be mediated by the NCM. To the best of our knowledge, this is the first study to investigate the role of NCM in female affiliative behavior. Further research should focus on tests conducted over longer time courses with multiple choices of mates to test the role of NCM in pair formation. Lesions to NCM or a drug with a longer timecourse, such as muscimol, a GABA-A agonist, would allow one to test females over extended periods. Research should also focus on the neurochemical basis of this partner preference. Our research shows that females treated with a noradrenergic neurotoxin, DSP4, do not distinguish between songs of differing quality, whereas intact females do (Vahaba et al., 2013). Therefore, research focused on determining the extent to which activity at noradrenergic receptors within the NCM is responsible for these findings is definitely warranted. Furthermore, since estradiol increases in NCM in song processing (Remage-Healey and Joshi, 2012; Remage-Healey et al., 2008; Jeong et al., 2011), future studies should investigate the link between electrical (as affected by lidocaine) and hormonal (estradiol) signaling in NCM. Our results suggest that the NCM, an auditory storage site, is important for the song discrimination and affiliation, the first step in the pairing process. These findings differ from those in rodents, in which regions linked to olfaction are important for partner preference formation. Thus, our findings highlight the importance of studying multiple species to understand mechanisms of complex social interactions. Acknowledgements We thank Elizabeth Adkins-Regan and Timothy DeVoogd for assistance with the conceptualization of this research. We also thank Bernard Tarr, Peter Baxter, and Leora Ramiro for assistance with the cannulation surgeries. We thank Timothy Van Deusen for assistance with animal care. We would also like to thank two anonymous reviewers for comments on an earlier version of this manuscript. This research was supported by NRSA F32 MH06740902 (MLT) and start-up funds (MLT). References Adkins-Regan, E., 2002. Development of sexual partner preference in the zebra finch: a socially monogamous, pair-bonding animal. Arch. Sex. Behav. 31, 27–33. Adkins-Regan, E., Krakauer, A., 2000. Removal of adult males from the rearing environment increases preference for same-sex partners in the zebra finch. Anim. Behav. 60, 47–53. Bailey, D.J., Rosebush, J.C., Wade, J., 2002. The hippocampus and caudomedial neostriatum show selective responsiveness to conspecific song in the female zebra finch. J. Neurobiol. 52, 43–51. Bailey, D.J., Wade, J., 2003. Differential expression of the immediate early genes FOS and ZENK following auditory stimulation in the juvenile male and female zebra finch. Brain Res. Mol. Brain Res. 116, 147–154. Bauer, E.E., Coleman, M.J., Roberts, T.F., Roy, A., Prather, J.F., Mooney, R., 2008. A synaptic basis for auditory–vocal integration in the songbird. J. Neurosci. 28, 1509–1522. Bolhuis, J.J., Gahr, M., 2006. Neural mechanisms of birdsong memory. Nat. Rev. Neurosci. 7, 347–357. Bolhuis, J.J., Hetebrij, E., Den Boer-Visser, A.M., De Groot, J.H., Zijlstra, G.G.O., 2001. Localized immediate early gene expression related to the strength of song learning in socially reared zebra finches. Eur. J. Neurosci. 13, 2165–2170. Bolhuis, J.J., Zijlstra, G.G., den Boer-Visser, A.M., Van Der Zee, E.A., 2000. Localized neuronal activation in the zebra finch brain is related to the strength of song learning. Proc. Natl. Acad. Sci. U. S. A. 97, 2282–2285. Braaten, R.F., Petzoldt, M., Colbath, A., 2006. Song perception during the sensitive period of song learning in zebra finches (Taeniopygia guttata). J. Comp. Psychol. 120, 79–88. Brenowitz, E.A., 1991. Altered perception of species-specific song by female birds after lesions of a forebrain nucleus. Science 251, 303–305. Canopoli, A., Herbst, J.A., Hahnloser, R.H.R., 2014. A higher sensory brain region is involved in reversing reinforcement-induced vocal changes in a songbird. J. Neurosci. 34, 7018–7026. Clayton, N.S., 1988. Song discrimination learning in zebra finches. Anim. Behav. 36, 1016–1024. Coleman, M.J., Roy, A., Wild, J.M., Mooney, R., 2007. Thalamic gating of auditory responses in telencephalic song control nuclei. J. Neurosci. 27, 10024–10036.

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