Society for Neuroscience Abstracts, 23:796 (311.8)
A Comparison of the Effects of Deafening and Vocal Denervation on the
Stability of Crystallized Song.
H.Williams*, F.M. Mullins, J.E. Danforth. Williams College, Williamstown,
MA 01267
Introduction
Some species of song birds, such as the canary, are able to relearn portions
of their song each year, while others, such as zebra finches, complete song
learning early in life and do not change their songs thereafter. Deafening
studies by Konishi and Nottebohm have shown that song learning requires
auditory input both for the acquisition of a song model and for the process
of matching the bird's vocal output to the model. However, the role of vocal-auditory
comparisons for the maintenance of adult song is not clear, especially for
species that do not relearn their songs annually. Price (1979) found little
change in zebra finch song six months after deafening, while Nordeen and
Nordeen (1990) described dramatic changes six months after deafening adult
males of the same species. Williams and McKibben (1990) described alterations
in the motor pattern for learned song after injuring the nerve that innervates
the vocal organ, and similar results have been seen after other manipulations
that alter vocal output without affecting hearing (Pytte and Suthers, 1996;
Hough and Volman, 1996).
The effects of deafening and vocal disruption on adult zebra finch song
may be due to interference with one process, that of comparing vocal output
to auditory feedback. To test this possibility, we compared the long-term
effects upon adult zebra finch song of a) deafening, b) altering vocal output,
and c) the combination of the two disruptions.
Methods
Fifteen adult male zebra finches aged at least 16 months (22 ±
2.1 months) were divided into three groups matched for songs. Five birds
were deafened using Konishi's method of bilateral cochlear removal, five
birds received right tracheo-syringeal nerve section and distal stump removal
(to prevent regeneration), and five birds received both treatments. All
birds' songs were recorded after surgery and then biweekly for 6 months.
They were re-recorded at 1 year after surgery, and the right HVC was then
lesioned (3 minutes of 50 µA anodal current passed through an insulated
insect pin placed by means of stereotaxic coordinates and visual determination
of the outline of HVC). Birds' songs were recorded after surgery and 1 and
2 months later. The birds were then euthanized, perfused (10% formol saline)
and the brains sectioned and stained with cresyl violet to verify the extent
of lesions.
At least 20 seconds of song were obtained from most birds at each recording
(some deafened birds sang sparingly). All songs were examined and compared
with the song of the intact bird, and the number of bouts, songs, and syllables
and syllable sequence present in each song were noted, and the number of
syllables that were dropped from the song, added to the song, or substantially
altered in phonology were scored. To provide a measure of constancy of song
structure, each song was expressed as a string of syllables, and each distinct
string was considered to be a song type; the number of songs for each song
type was noted. For example, a bird that sang a bout:
iiiiiABCDEFGCDEFGCDEFGCDEFGCDE
where i is an introductory note and A,B,C,D,E,F, and G are syllables
would be scored as:
1 song of type ABCDEFG
1 song of type CDE
3 songs of type CDEFG
The proportion of song types identical to those given in the original,
intact recordings was calculated for each song recording after deafening
and nerve injury; after HVC lesion, the proportion of song types that were
identical to those sung at the recording immediately prior to lesioning
was calculated.
Results
Figure 1. Birds in all three groups changed their songs in a manner
similar to that described previously for birds with disrupted vocalizations.
Syllables were dropped from songs, new syllables were added, and, relatively
rarely, alterations to syllable phonology occurred.
Examples of songs sung after by adult male zebra finches after
- A) deafening (114K file),
-
- B) tracheosyringeal nerve (NXIIts) injury
(69K file),
-
- C) both deafening and NXIIts injury
(85K file).
Songs are shown for intact birds, within two weeks after surgery, three,
six and twelve months after surgery, and two months after right side HVC
lesion (the right side is dominant for song control in the zebra finch).
Song syllables maintained from the original song are shown in blue; syllables
that occur for the last time in this recording are shown in red; and syllables
that did not occur in the original song are shown in black.
Figure 2. One year after deafening/NXIIts injury, the average number
of changes to songs varied with treatment.
Birds with NXIIts injury alone had significantly fewer changes
to their songs than did birds that were deafened or that received both treatments.
The effects of deafening and and NXIIts injury were not additive; the number
of changes in the songs of birds that were deafened did not differ statistically
from the number of changes in the songs of birds that were both deafened
and NXIIts-injured.
One-way ANOVA: F(2,11) = 7.42; p = 0.01; Fisher's PLSD: NXIItsX <
deafened, p < 0.01; NXIItsX < both treatments, p < 0.05 |
 |
Figure 3. The time course of song changes was the same for all treatment
groups.
The absolute value of the change in proportion of songs that contained
each syllable was summed for all syllables in each bird's song and averaged
for the birds in each treatment group. Most song changes occurred by three
months after surgery.
Figure 4. Two months after HVC lesion, the average number of additional
changes to songs did not vary with treatment.
There were substantial changes to the songs of all birds after
HVC lesion, with an average of 2 syllables dropped, 1 syllable altered,
and 1.5 syllables added (syllables scored as "added" may have
been syllables that were altered beyond recognition; only the songs of birds
that had at least 2 recognizable syllables were scored). One-way ANOVA:
F(2,8) = 2.23; p = 0.17
More changes to the songs occurred within the two months after HVC lesion
than had occurred in the year since the birds were deafened and/or NXIIts
injured, but this difference was not statistically significant. One-way
ANOVA: F(1,20) = 1.17; p = 0.29 |
 |
Figure 5. One year after the initial surgery, birds with tracheosyringeal
nerve injury alone retained more of the song types sung in the intact recording
than did birds that were deafened.
Although the birds in the NXIIts injury treatment group retained
an average of fewer than half of the song types they had sung when intact,
this was substantially and significantly higher than the proportion of song
types retained by birds in the other treatment groups. One-way ANOVA: F(2,9)
= 7.12; p = 0.01;
Fisher's PLSD: NXIItsX > deafened, p < 0.05; NXIItsX > both
treatments, p < 0.05).
This result is most probably directly related to the finding that the
NXIIts-injured birds also retained more unaltered syllables (see Figure
2). |
 |
Figure 6. After HVC lesion, birds with tracheosyringeal nerve injury
alone retained fewer of the song types sung in the intact recording than
did birds that were deafened.
| Despite the fact that birds in all treatment groups had the same number
of changes to song syllables after HVC lesion (see Figure 4), the birds
with NXIIts nerve injuries retained fewer than 5% of the song types they
had at 1 year after the original surgery, while birds in the other two groups
retained over 30% of the song types present at 1 year after the original
surgery. However, this trend did not reach significance. |
 |
Discussion
Since deafening and NXIIts injury effect song in similar ways, although
the degree of the effect is greater for deafening. Birds in all treatment
groups lost substantial numbers of song syllables. They also added syllables
to their songs and made changes to existing syllables, though these changes
were less frequent. In general, song patterns and song syllables were identifiable
one year after the original surgery. The discrepancy between our results
and those of Nordeen and Nordeen may be due to the fact that the birds in
our study were older, averaging 21 months of age; it is possible that, as
was suggested by Nottebohm, the amount of song sung as an adult is directly
related to the song's "permanence" after disrupting the ability
of birds to perform vocal-auditory comparisons.
The syllables of birds in all treatment groups were similarly and severely
affected by HVC lesions made more than 1 year after the original surgery.
The song structure of birds with NXIIts injury alone tended to be more severely
affected than that of birds that had previously been deafened. If this trend
is confirmed, it could have interesting implications about the role of HVC
in song maintenance in adult zebra finches.
These results indicate that the effects of deafening and vocal disruption
in adult zebra finches differ in degree but not in kind, and that both may
be due to a mismatch of auditory feedback and motor activity.
Acknowledgements
This study was supported by grants from the Essel Foundation and the
Howard Hughes Medical Institute.
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