1. A BRIEF OVERVIEW FOR CRITICAL PERIODS OF VOCAL LEARNING
A Comparative View
of Language Acquisition
Stuart D. Washington, PhD
Bio-Imaging Lab
University of Antwerp

2. GENIE “Genie” was the victim of severe abuse and neglect.
Her father kept her alone in a room, forbade others from talking with her, left her strapped to a toilet or bound in a crib.
Genie was only discovered by social workers when she was almost 14 years of age.

3. GENIE
With the help of mental health professionals, “Genie” made tremendous strides in her social skills and non-verbal communication.
However, “Genie” failed to acquire a first language.
“Genie’s” case is noteworthy in the annals of psychology and linguistics, as evidence for a “critical period” for language acquisition.

4. CRITICAL PERIOD FOR LANGUAGE ACQUISITION
A hypothesis forwarded by Penfield and Roberts (1959) and popularized by Lenneberg (1967), Newport (1990), and Pinker (1994).
Language develops more easily and successfully early in life (generally before age 5 but possibly extending into puberty) than later in life.

5. So what’s the problem here?
Could “Genie” have been intellectually challenged as well as abused?
How much can “Genie” and other tragic children tell us about language acquisition in general when they are such exceptional cases?
How well can we understand the mechanisms underlying language acquisition without performing behavioral, physiological, and molecular experiments that are unethical to perform on humans?

6. Comparative Studies of Language Acquisition
Comparative studies of language acquisition would address many of the problems raised earlier by allowing researchers to take multiple, healthy animals, deprive them of social contact, and to observe whether the animals develop language.
Problem: Only humans are acknowledged to actually use language.
Solution: Though animals have not been shown to use “language” (a complex and controversial concept firmly rooted in symbolic reasoning), it is indisputable that some animals use acoustic signals to communicate; perhaps studying “auditory communication” (and “vocal learning in particular”) in animals will shed light on speech, the auditory domain of language.

7. SONGBIRD: A MODEL FOR CRITICAL PERIOD OF VOCAL LEARNING
Male songbirds attract mates using acoustically complex songs.
There are three aspects of songbird vocal learning that make it a strong model for critical periods in humans:
Dependence on auditory experience and feedback for vocal learning.
A complex hierarchy of neural circuits in which motor and auditory areas closely interact.
Parallels with humans at the genetic level.

8. SONGBIRD: A MODEL FOR CRITICAL PERIOD OF VOCAL LEARNING
During a critical ( or “sensitive”) period, young male zebra finches (Taeniopygia guttata) memorize the song of a tutor.
Next, these pupils go through a phase of sensorimotor practice, during which they try to match their verbal output to the songs they previously memorized.
During this sensorimotor phase, the birds generate a “subsong” before their song finally crystalizes into the song they will sing their entire lives.
Zebra finches are good model for critical period of vocal learning
Similarities in process of vocal learning
- Learning of complex vocalizations during sensitive period (sensory-learning phase/sensory-motor learning phase + babbling = subsong etc)
- Strong dependence on auditory experience and feedback for learning
Well defined brain circuitry in control of song/speech: Complex hierarchy of specialized forebrain areas in which motor and auditory centers interact closely
Parallels at genetic level: Human language disorders in humans have been linked to mutations in FOXP2 and one of its neural targets, the contactin-associated protein-like 2 gene (CNTNAP2). By analyzing the expression patterns of these genes in songbirds, enticing parallels between songbirds and humans were observed. In addition, FOXP2 was shown to be involved in song learning and the sensitive period for song learning.
Research at genetic level possible (Recently the complete genome of this bird was unraveled + availability of commercial micro array)
Figures
Brainard & Doupe (2002); timeline critical period etc.
Petkov & Jarvis (2012): bird vs human brain organization & pathways

9. SONGBIRD: A MODEL FOR CRITICAL PERIOD OF VOCAL LEARNING
Other songbirds have different, often more complex critical periods.
The subsong generated during the critical period (i.e., before song crystallization) has been compared to the “babbling” phase in human infants.
Like “Genie,” when deprived of the kind of social contact that offers auditory experience and feedback from conspecifics, zebra finches and other songbirds fail to learn communication sounds vital to successful social interactions.
Zebra finches are good model for critical period of vocal learning
Similarities in process of vocal learning
- Learning of complex vocalizations during sensitive period (sensory-learning phase/sensory-motor learning phase + babbling = subsong etc)
- Strong dependence on auditory experience and feedback for learning
Well defined brain circuitry in control of song/speech: Complex hierarchy of specialized forebrain areas in which motor and auditory centers interact closely
Parallels at genetic level: Human language disorders in humans have been linked to mutations in FOXP2 and one of its neural targets, the contactin-associated protein-like 2 gene (CNTNAP2). By analyzing the expression patterns of these genes in songbirds, enticing parallels between songbirds and humans were observed. In addition, FOXP2 was shown to be involved in song learning and the sensitive period for song learning.
Research at genetic level possible (Recently the complete genome of this bird was unraveled + availability of commercial micro array)
Figures
Brainard & Doupe (2002); timeline critical period etc.
Petkov & Jarvis (2012): bird vs human brain organization & pathways

10. SONGBIRD: A MODEL FOR CRITICAL PERIOD OF VOCAL LEARNING
Like in humans, there are vocal motor circuits and auditory perceptual circuits that interact with one another to support vocal learning.
Unlike in humans, songbird brains are nucleated, making these circuits easier to pinpoint and study than the amorphous cortical functional areas of humans (e.g., Broca’s and Wernicke’s areas).
The Anterior Forebrain Pathway (AFP) underlies much of the song learning phase. The Motor Pathway underlies vocalization.
Lesions to AFP nuclei lead to abnormal song production even in normally tutored pupils.
Testosterone is known trigger the end of a critical period by reducing the number of synapses in AFP nuclei (specifically in LMAN).
The AFP and motor pathways converge upon Area RA, which may underlie the practice and crystallization phase of vocal learning

11. SONGBIRD: A MODEL FOR CRITICAL PERIOD OF VOCAL LEARNING
Language disorders (e.g., specific language impairment and autism spectrum disorder) have been linked to mutations in FOXP2 and one of its neural targets, the contactin-associated protein-like 2 gene (CNTNAP2).
The songbird genome contains these same two genes, and by analyzing the pattern of their expression in songbirds, enticing parallels between songbird and human communication have been observed. For example, FOXP2 was shown to be involved in song learning and the sensitive period for song learning.
FOX P2
Now that the complete genome of the zebra finch has been sequenced, a great deal of genetic research is now possible.

13. AUDITORY COMMUNICATION IN BATS
Bats comprise 20% of mammalian species.
Bats are highly vocal and social.
They are mammals and thus have a laminar brain with all the same neuroanatomical structures as humans.
Microchiroptera (unlike the Flying Fox pictured at left) depend on audition for spatial guidance (echolocation) and for communication.
One would expect that, like zebra finches, they would display some sort of critical period, but we don’t know conclusively.

14. AUDITORY COMMUNICATION IN BATS
There is evidence for “developmentally sensitive periods” in which neural selectivity to certain portions of echolocation signals develop earlier than selectivity to other components of those same signals (Razak and Fuzessery, 2015).
Further, there is evidence for vocal learning in bats (Vernes, 2016; Knörnschild, 2014).

15. AUDITORY COMMUNICATION IN BATS
Hand-reared bat pups adapt to the FM properties of digital directive calls, demonstrating an ability to learn from a conspecific template (Esser, 1994).
Other bats show turn-taking (Yoshida & Okanoya, 2005).
Despite these leads, it will be up to future experiments to determine whether bats display “critical periods” similar to those of humans and birds.