The zebra finch is a small (10 cm long) song bird that are known for their complex song learning behaviors. Song learning in zebra finch has been extensively studied for its applications in the neural bases of human learning, memory and sensorimotor integration. When the zebra finch became the second bird to have its genome sequenced in 2008, it was determined that much of the genetic code devoted to brain circuitry are similar to the sequences encoding vocal learning in humans. These similarities suggest that gaining an understanding of the zebra finch brain could lead to a greater understanding of human speech and communication disorders such as autism and stuttering.
Stages of Song Learning in Zebra Finch
The zebra finch song is a series of notes made in a distinct order. The learning of the zebra finch song occurs in several distinct stages (Soderstrom and Tian, 2006).
Auditory Learning Stage
- Prefledglings memorize the notes and the order in which they are produced while being raised and sung to in the nest.
- The auditory learning stage usually lasts to 35 days of age.
- In the sensory-motor stage of song development, the zebra finch memorizes the order of the production of notes and begins to vocalize the notes.
- Vocal production and auditory feedback are necessary in order to learn during this stage
- In the sensory-motor stage, the zebra finch first enters a “subsong” period. During the subsong period, birds learn how to produce distinct notes by controlling their syrinx, the avian vocal organ.
- Following the successful production of notes, the bird enters the “plastic song” period of sensory motor learning.
- Periadolescent birds begin to mimic the song learned in the auditory learning stage.
By 90 days of age the bird is capable of consistently reproducing the song presented during auditory learning, and this song will not change for the rest of the lifetime of the bird.
Brain Structures Associated with Song Learning in Zebra Finches
Zebra finches possess an unusually enlarged telencephalon. Other studies have indicated that enlargement of the telencephalon in passerine birds, including zebra finches, is positively correlated with higher levels of behavioral complexity (Lefebvre et al., 2002, Lefebvre et al., 1997). Because most of the neurons involved in song learning and production are located within the telencephalon, it has been speculated that an enlarged telencephalon is responsible for the complexity observed in zebra finch song learning (Konishi, 1985 as cited by Charvet and Striedter, 2009).
There are several regions of the zebra finch telencephalon included in song learning and production. Song regions in the rostral (located towards the beak of the bird) forebrain play a role in song learning but are not necessary for adult vocal behavior (Soderstrom and Tian, 2008). On the other hand, two regions in the caudal telencephalon are important during song learning and recitation of an already learned song as an adult.
Song regions necessary for song learning:
- lateral magnocellular nucleus of the anterior neostriatum (IMAN)
- medial portion of the dorsolateral nucleus of the thalamus (DLM)
- area X of striatum (Area X)
Regions necessary for song learning and vocalization of an already learned song as an adult:
- higher vocal center (HVC)
- robust nucleus of the archistriatum (RA)
Cannabinoid Receptor Expression in Zebra Finch Telencephalon
The expression of cannabinoid receptors in the telecephalon of zebra finches was initially investigated due to the high CB1 cannabinoid receptor expression on mammalian telencephalon. Results of behavioral studies in rats suggest that cannabinoids play an important role in cognitive function, learning and memory (Hampson and Deadwyler, 1998). Because the zebra finch telencephalon controls song learning, it was proposed that endocannabinoid signaling may play a key role in vocal development (Soderstrom and Johnson, 2000).
The expression of cannabinoid receptor (CB1) in zebra finch telencephalon was measured using Northern blotting and RT-PCR in a study conducted by Soderstrom and Johnson (2000). The Northern blots revealed presence of CB1 mRNA of a similar size to that reported in the rat. The levels of CB1 mRNA in zebra finch also differed over the course of song development.
- Levels of CB1 mRNA levels were lowest in RNA taken form caudal telencephalon during the auditory learning stage.
- Increased levels of CB1 mRNA were observed in RNA isolated from the telencephalon during the sensory-motor learning stage of vocal development.
- RNA isolated from adult telencephalon expressed higher CB1 mRNA levels than RNA isolated during the auditory learning stage, but they were lower than in RNA isolated during the sensory-motor learning stage.
These findings were confirmed by RT-PCR. The results of both of these assays can be seen in the figure below.
Effects of Cannabinoid Exposure on Vocal Learning in Zebra Finches
The endocannabinoid system in zebra finch (and mammals) is a neurochemical signaling system composed of two G-protein coupled receptors, CB1 and CB2 (Soderstrom et al., 2011). CB1 is expressed at higher levels in the zebra finch CNS. The endocannabinoid system also employs an array of fatty acid ligands including anandamide and 2-arachidonyl glycerol (2-AG). These fatty acid ligands are capable of activating CB1.
G-protein-coupled receptors are often regulated by agonist-induced internalization and metabolism in which the duration of agonist effects are limited by receptor expression. Therefore, exogenous cannabinoid-induced alteration of normal vocal development may depend on regulation of endocannabinoids and receptor expression.
When treated with cannabinoid agonist WIN55212-2 (WIN) zebra finches during the sensory-motor learning, a noteable decrease in notes learned and stereotypy score (presence of a distinct pattern) was observed (Soderstrom and Johnson, 2003). It should be noted that mean duration of notes produced did not change.
In order to further elucidate the role of endocannabinoid signaling in vocal development, Soderstrom et al. studied the effects of the cannabinoid receptor agonist WIN55212-2 (WIN) on levels of AG-2 and density of CB1 immunostaining in the zebra finch brain (Soderstrom et al., 2011). It was determined that when repeatedly exposed to cannabinoid agonist WIN during the sensory-motor stage of vocal development, levels of AG-2 were increased and CB1 immunostaining intensities decreased within the rostral telencephalon. This trend was not observed following repeated WIN treatment of adult zebra finches. This disparity suggests that susceptibility to disregulation caused by prolonged exposure to cannabinoids is limited to the developing zebra finch CNS.
The Current Status of Zebra Finch Research
While the papers referenced above have studied the role of cannabinoids in great detail, much remains unknown about the signaling pathways that play a role in song learning. Because only male zebra finches sing, an investigation of the causes of this sexual dimorphism may be particularly informative. It has recently been observed that the developmental stressors that impair song learning in males do not affect the female preferences for song complexity (Woodgate et al., 2011). It has also been determined that exposure to oxytocin may result in an inability to properly vocalize the learned note patterns, similar to autism in humans (Riffle, 2010).
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Konishi M. 1985. Birdsong: from behavior to neuron. Annu Rev Neurosci 8:125–170.
Soderstrom K, Johnson F: Cannabinoid exposure alters learning of zebra finch vocal patterns. Brain Res Dev Brain Res 2003, 142(2):215-7.
Charvet, J.C., Striedter, G.F. (2009). Developmental Origins of Mosaic Brain Evolution: Morphometric Analysis of the Developing Zebra Finch Brain. Journal of Comparative Neurology, 514: 203-213.
Riffle, B.W. (under the guidance of Dr. Ken Soderstrom). Oxytocin Modulation of Zebra Finch Vocal Development. Department of Pharmacology and Toxicology, Brody School of Medicine, East Carolina University. August 2010.
Soderstrom K, Johnson F. 2000. CB1 cannabinoid receptor expression in brain regions associated with zebra ﬁnch song control. Brain Res 857: 151–157.
Soderstrom K., Tian, Q. (2006). Developmental pattern of CB1 cannabinoid receptor immunoreactivity in brain regions important to zebra finch (Taeniopygia guttata) song learning and control. J Comp Neurol, 496(5):739-58.
Soderstrom K, Tian Q: CB(1) cannabinoid receptor activation dose dependently modulates neuronal activity within caudal but not rostral song control regions of adult zebra finch telencephalon. Psychopharmacology (Berl) 2008, 199(2):265-73
Hampson, R.E., Deadwyler S.A. (1998) Role of cannabinoid receptors in memory storage, Neurobiol. Dis. 5 1998 474–482.
Woodgate, J.L., Leitner, S., Catchpole, C. K., Berg, M.L., Bennett, A. T. D., Buchanan, K. L.. (2011). Developmental stressors that impair song learning in males do not appear to affect female preferences for song complexity in the zebra finch. Behavioral Ecology. 21 (3).