Motor circuits are required to encode a sensory model for imitative learning


This article is based off a paper whose title it shares, written by Todd F Roberts, Sharon M H Gobes, Malavika Murugan, Bence P Ölveczky, and Richard Mooney.  It was published in the October 2012 addition of Nature Neuroscience, volume 15 number 10.


Behaviors can be passed though a population by an individual observing the actions of another then imitating the aforementioned behavior.  Though behaviors have been observed and documented to be passed along in this manner, commonly noticed in song birds like the Zebra Finch (Taeniopygia guttata), the mechanism in which the brain encodes and replays the received messages is not fully understood.  However, it is known that songbirds learn their songs through trial-and-error experimentation and practice.  Through continually practicing and comparing to that of the original tutor’s song, young adult songbirds can produce remarkably similar copies (2).  In recent years, premotor circuits have been suggested to play a role in imitative behaviors, such as birdsongs.

Premotor Circuits

The role of premotor circuits in sensory learning was tested in juvenile male zebra finches.  Results from these experiments suggest a sensory motor phase, in which the pupil finch memorizes the song from the tutor finch, and a sensorimotor learning, during which the pupil practices and matches the original tones (Figure 1a).  To supplement these two stages of learning, the zebra finch’s brain is equipped with developed auditory and song motor pathways (Figure 1b).  The directionality of these pathways were determined by pharmacologically manipulating secondary regions throughout the brain of juvenile zebra finches to observe the effect on the birds ability to imitate the original song (Figure 1c), though it remains unclear if the song which is encoded in one region is originally reliant on downstream structures to originally encode the message.

Figure 1.

Figure 1. Song learning pathways in songbirds. (a) Temporeal outline of song learning. (b) Dorsal view of zebra finch brain (left), and side view through medial forebrain (right). Song premotor circuitry is shown in red, with the HVC (high vocal center) and auditory circuitry in blue. A1 primary auditory regions (field L); CM, caudal mesopallium; Area X, striatal component of the song system; RA, robust nucleus of the arcopallium; VMNs, vocal motor neurons. (c) Schemmatic of tutor-song-contingent disruption of neural activity in pupil's brain. (Roberts 2012)

To further test the high vocal center’s role in sensory learning, viral mediated expression of humanized channelrhodopsin-2 (hChR2 expressed using scAAV2/9-hChR2–yellow fluorescent protein (YFP) or herpes simplex virus 1 (HSV1-hChR2)) could be used with light pulse to alter the HVC’s neural activity.  The effect of pulsing the lazer (473 nm) in short intervals, aimed at the dorsal area of the HVC, gave rise to the same result described by Figure 1c.

Role of the HVC

Once the HVC was determined to play a leading role in the imitation of the tutor’s song, the next question was why does it.  The notes in a songbird’s song are controlled within milliseconds.  By timing the lazer pulses through an optic cable targeting the HVC, it was theorized possible to interfere with the encoding of a single syllable of the tutor’s song by the pupil (Figure 2a).  This manipulation of the syllable of the tutor’s song was quantified and shown in the graph depicted in Figure 2b and sonogram printout shown in Figure 2c.

Figure 2. Interference of a single syllable of the tutor's song. (a) Visual representation of the effect a pulse (~100 ms) of laser light (473 nm) has on the encoding of a syllable of the tutor's song has on the pupil's encoding. (b) Similarities of notes, showing a clear decrease in the c syllable affected by the pulse. (c) Sonogram of the notes of the two finches' songs. (Roberts 2012)

With the questions of which areas affected the sensory learning involved in the acquiring of the finch’s song and the role it had in the process, the question of how the HVC network plays a role in encoding the tutor’s song remained.  In vivo images were obtained using multiphoton imaging experiments on juvenile finches following tutoring sessions with their tutors.  These images showed that the tutoring had triggered the rapid enlargement of previously stable dendritic spines in HVC, which has been shown to depend on the activation of postsynaptic NMDA receptors (3).  To test if the enlargement in this case was due to NMDA receptors, the receptors were blocked pharmacologically (Figure 3a).  HVC neurons were then tagged with GFP to aid in the imaging of the tested neurons.  To establish baseline leves for the spine size, images of dendritic spines were taken for the juvenile finches prior to tutoring.  The juveniles were then injected with the NMDA antagonist (D-AP5) into the HVC of the birds, directly before tutoring.  The size of the HVC dendritic spines were then examined to determine if the tutoring had an effect on the size of the spines (Figure 3b).  The findings were supportive of the tutoring-induced growth of dendritic spines in the HVC is dependent on the NMDA receptors.  This means that blocking NMDA receptors during tutoring sessions would prevent accurate song imitation.  A study conducted using D-AP5 injected finches supported this claim, by the song comparison of the injected adult birds to the birds that were not injected with the antagonist (Figures 3d,e).

Figure 3.

Figure 3. Blocking of NMDA receptors in HVC to prevent spine enlargement and inhibit learning of tutor's song. (a) Image depicting the in vivo multiphone imaging of the dendritic spines in the HVC and pharmacological blocking of NMDA receptors with D-AP5 immediately prior to tutoring. (b) Stable spines before and after tutoring an injection of D-AP5. (c) Steps for reversibly blocking the NMDA receptors during tutoring. (d) Addition of D-AP5 in the HVC during tutoring but not during practice sessions. (e) Sonogram of tutor's song and songs of test birds. (Roberts 2012)

Beyond the HVC

Though it was shown that the HVC receives information from several sources, the nucleus interface (NIf) was shown to be major source of auditory input to the HVC.  To test if NIf had a role in sensory learning, a permanent bilateral lesion was made in the NIf of juvenile finches before the initiation of song tutoring (Figure 4a).  After time with the tutor to learn the song, the variance of the pupil’s song from the original was shown to be correlated to the size of the lesion (Figure 4b).  This correlation was sought to be proven true by reverse inactivating the NIf lesion to show that reversing improved the song quality of the imitation, though, even after reverse inactivating these legions, the ability to copy the tutor’s song was still hindered (Figure 4c,d,e,f).  However, when the solutions from the reverse inactivating was reversed the pupil’s songs had a strong resemblance to the tutor’s song (Figure 4c,d,e,f).  The resulting conclusion of these two finding is that NIf plays a role in the processing of the encoded signal in the HVC by impairing the signaling during tutoring.

To further investigate this pathway, tutor song-triggered microstimulations to the NIf or the Field L1 region were applied to juvenile zebra finches (Figure 4d).  Following the tutelage stage, all the NIf impaired finches produced poor quality songs, while the stimulation of the adjacent Field L1 auditory region had no observable effect on the song quality of the copy (Figure 4e,f,g).  These findings suggested that NIf plays a critical role in the conveying of the auditory signaling to the HVC while the tutor is singing.

Figure 4.

Figure 4. Tutor's song is processed by the HVC from the NIf. (a) Timeline of NIf lesion experiment. (b) Effect of lesioning NIf before tutoring. Results in dramatically different songs. (c) How NIf lesion experiment was conducted. (d) Sketch of experiment in which pupil's NIf was microstimulated. (e) Inactivating the NIf during the experiment changes the pupil's song. (f) Sonograms of a tutor's song and adult songs of two pupils in which NIF was inactivated with TTX during or after tutoring session. (g) Sonograms of a tutor's song and adult songs of two pupils in which tutor triggered microstimulation of NIf was occurring. (Roberts 2012)

Conclusion

The process by which a zebra finch learns its birdsong is a complicated and time sensitive multistep process.  Regions of songbirds’ brains involved in this learning process were isolated using a series of techniques that altered how the pupil finch encoded the tutor’s song.  By observing changes between the tutor’s and pupil’s songs, it became possible to deduce the area’s function in encoding and recalling the song.  The paper gave strong data to support the authors’ claims of which areas of the songbird’s brain were communicating to pass along and encode the message into the birds memory.  While the paper seemed successful in deducing a large portion of how the song was encoded into the bird’s memory and what role motor circuits played in the priming of these systems, there was some ambiguity as to the functions of some of the supporting structors surrounding the active area.  It is possible that the paper was published before all of these areas could be completely analyzed or some areas that presently seem irrelevant or inactive in the pathway could later be proven to serve a function in the overall signal transduction pathway.

Using this information learned, it could be possible to target and treat learning disabilities within our own population.  If the signal pathway can be completely understood, recognizing miscommunications during the encoding process could lead improved recalling of stored information with a high rate of matching the originally produced message.  Treatment of this nature could increase the success rates in primary school systems and result in the treated individual to be able to function at a higher level then would originally be possible (4).

References

1) Robers, Todd F; Gobes, Sharon M H; Murugan, Malavika; Olveczky, Bence P; Mooney, Richard (2012).  Motor circuits are required to encode a sensory model for imitative learning.  Nature Neuroscience; Volume 15, number 10.  1454-1461

2) Ölveczky, B.P., Andalman, A.S. & Fee, M.S. Vocal experimentation in the juvenil songbird requires a basal ganglia circuit. PLoS Biol. 3, e153 (2005).

3) Engert, F. & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66–70 (1999).

4) Naritoku et al. (2003).  Methods for improving learning or memory by vagus nerve stimulation.  United States Patent.  Patent # 6,556,868 B2.  April 29, 2003.

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