How songbirds sing birdsongs?

Transcription

1 How songbirds sing birdsongs? Liora Las Michale Fee (MIT) Veit et al. (J Neurophysiol, 2011)

2 Outline: 1) Introduction to songbirds as a model. 2) Neuronal circuits underlying mature song production (motor system). 3) Neuronal circuits underlying early stages of singing (learning system).

3 Vocal learning Mammals: Humans Bats Dolphins/Whales Elephants Sealions Birds: Parrots Hummingbirds Songbirds

4 What do songbirds and humans have in common? Both humans and songbirds learn their motor behavior (e.g. vocal) early in life. Both learn to communicate by listening to their parents. They must be able to hear their own vocalization in order to learn to sing/speak. Both humans and songbirds have evolved a complex hierarchy of specialized brain areas essential for vocal control.

5 Birds sing for two main reasons: 1. To attract a mate. 2. To establish and hold a territory. Singing is mostly a male activity. Male s brains are specialized in singing, female s brains are specialized in evaluating the song

6 Frequency Songbirds sing! Adult song is highly stereotyped Zebra finch motif syllables time ~1sec Ofer Tchernichovski s Lab (CUNY)

7 Song Variability Songbirds learn to sing by imitating their tutor 40d 60d 90d Subsong Plastic Song Crystallized Similarity to Tutor Tutor Song Age (days)

8 Reinforcement learning model for song acquisition Auditory feedback Song evaluation Auditory Memory -- Reinforcement signal Song Song motor system Exploratory variability Konishi 1965; Marler 1970

9 Brain of Songbirds Cortex Thalamus Basal Ganglia

10 Motor pathway HVC: high vocal center RA: primary motor cortex HVC Motor pathway brainstem motor areas Muscles of the syranx respiratory muscles nxiits RA Uva DM Nottebohm et al., (J Comp Neurol, 1976)

11 Question: How do these circuits work to produce a song? Record from brain areas and see what are the firing patterns of these neurons during singing.

12 The song Recordings from RA neuron during the song HVC RA nxii

13 RA activity during singing Leonardo & Fee (J Neurosci, 2005) HVC RA nxii

14 HVC Motor pathway RA Learning Pathway (AFP) nxiits Area X

15 Recording electrode antidromic stimulation Stimulating electrode HVC RA

16 Stimulating electrode Stimulating electrode

17 Recording electrode Collision test Stimulating electrode HVC RA

18 Recording electrode Collision test Stimulating electrode HVC RA

19 Using antidromic stimulation to identify cell types within HVC HVC Motor pathway RA nxiits Hahnloser et al. (Nature, 2002)

20 Activity of HVC-RA neurons during singing Hahnloser et al. (Nature, 2002)

21 Hahnloser et al. (Nature, 2002)

22 Simple sequence generation circuit Sparse representation of time Output Leonardo and Fee, 2005

23 Simple sequence generation circuit Sparse representation of time Output Leonardo and Fee, 2005

24 Part 1: Summary HVC exhibits sparse bursts during singing. RA transforms the sparse code into multiple bursts which then drive motoneurons. BUT: Where are these patterns of activity coming from? What is driving HVC to fire at a particular moment?

25 Are the dynamics generated within HVC? Fee & Long (Curr Opin Neurobiol, 2011)

26 Local manipulation of brain temperature Long & Fee (Nature, 2008)

27 Cooling of HVC- 3% per 1 degree Long & Fee (Nature, 2008)

28 Part 1: Summary HVC: HVC exhibits sparse bursts during singing. Song timing is controlled within HVC. RA: RA transforms the sparse code into multiple bursts which then drive motoneurons.

29 Subsong ( babbling ) i.e., the highly variable song in very young juveniles Fee & Scharff (ILAR, 2010)

30 Question: What are the mechanisms that produce subsong ( babbling ) i.e., the highly variable song in very young juveniles?

31 HVC-lesioned birds could still produce subsong! Control no HVC Subsong stage (37 dph) Plastic song stage (50 dph) Adult Aronov et.al. (2008) Science 250 ms

32 RA HVC Cortex LMAN X Motor Pathway Learning Pathway (Anterior forebrain pathway- AFP) nxii Thalamus DLM Area X Basal Ganglia The learning pathway is not necessary for adult song production, but is required for learning (Bottjer, 1984, Scharff and Nottebohm, 1991)

33 Frequency of vocalizations (sec/day) subsong plastic song What drives subsong production? crystallized song RA HVC X X LMAN X Age (days) nxiits Muscles 2500 N=57/57 N=26/27 N=0/5 N=0/12 N=0/6 N=6/ Control no HVC no RA nohvc nolman no LMAN (38-44 dph) no LMAN (45-67 dph) Aronov et.al. (2008) Science

34 AFP (anterior forebrain pathway) is necessary for producing subsong, suggesting that this circuit is important for vocal variability. Which part of AFP is necessary? Lesion of area X does not lead to elimination of subsong. DLM is necessary for the production of subsong. LMAN RA pathway cannot generate subsong like vocalizations independent of DLM. Motor pathway HVC Learning pathway (AFP) RA LMAN nxiits DLM (Thalamus) X Area X (Basal ganglia)

35 Separate premotor pathways for stereotyped song and babbling Sequence Stereotypy Precision Uva DLM Randomness Variability Exploration Adult song HVC LMAN Subsong RA Motor Output

36 Question: What is the role of LMAN in older juveniles?

37 Role of LMAN in older juveniles TTX or Muscimol HVC RA Motor Pathway Learning Pathway (AFP) LMAN nxii DLM Area X Andalman & Fee (2009)

38 subsong plastic song Role of LMAN in older juveniles LMAN is a generator of variability Ölveczky et al. (PLoS Biology, 2005) Age (days)

39 Reduced variability in pitch after LMAN inactivation during crystalized song Control LMAN inactivated

40 Conditional auditory feedback Andalman & Fee (PNAS, 2009)

41 LMAN is a generator of variability LMAN is the essential premotor nucleus for the earliest babbling vocalizations (Aronov and Fee, 2008). LMAN adds variability to enable exploration. LMAN may serve an essential role in song learning by driving variability: in subsong, plastic song, and even in adult song (Kao et al, 2005).

42 Separate premotor pathways for stereotyped song and babbling Sequence Stereotypy Precision Uva DLM Randomness Variability Exploration HVC LMAN RA Motor Output

43 Summary Activity of the motor pathway is stereotyped. Activity of the learning pathway is variable. These two signals are combined at RA. Motor pathway HVC Learning pathway (AFP) RA LMAN nxiits DLM (Thalamus) Area X (Basal ganglia)

44 Chomsky: Universal grammar constraints syntactic diversity in humans. In other words: genes constrain language diversity. Ofer Tchernichovski: Do genes constrain song diversity?

45 Song culture in birds Some songbirds provide biologically tractable models of culture: some members of species show individual variation in singing, and geographically separated groups have local song dialects. But the variety is not infinite: different species exhibit distinct song cultures, suggesting genetic constraints.

46 What happens when you isolate a bird from his father before the sensory period? Age (days)

47 What happens when you isolate a bird from his father before the sensory period? Birds are establishing the song template very early, during the sensory period. The experiment: to determine whether wildtype song culture might emerge over multiple generations in an isolated colony founded by isolates. Konishi 1965; Marler 1970 Fehe r et al. Nature 2009 The lab of Ofer Tchernichovski

48 Culture in the lab: development of song culture in the zebra finch Fehe r et al. Nature 2009 The lab of Ofer Tchernichovski

49 Fehe r et al. Nature 2009 The lab of Ofer Tchernichovski Song evolved towards the wild-type in three to four generations. Thus, species-typical song culture can appear de novo.