Zebra finch mates use their forebrain song system in unlearned call communication

Abstract

Unlearned calls are produced by all birds whereas learned songs are only found in three avian taxa, most notably in songbirds. The neural basis for song learning and production is formed by interconnected song nuclei: the song control system. In addition to song, zebra finches produce large numbers of soft, unlearned calls, among which "stack" calls are uttered frequently. To determine unequivocally the calls produced by each member of a group, we mounted miniature wireless microphones on each zebra finch. We find that group living paired males and females communicate using bilateral stack calling. To investigate the role of the song control system in call-based male female communication, we recorded the electrical activity in a premotor nucleus of the song control system in freely behaving male birds. The unique combination of acoustic monitoring together with wireless brain recording of individual zebra finches in groups shows that the neuronal activity of the song system correlates with the production of unlearned stack calls. The results suggest that the song system evolved from a brain circuit controlling simple unlearned calls to a system capable of producing acoustically rich, learned vocalizations.

Figure 1. Duration and FM of tet and stack calls in 6 pairs (10 randomly selected measurements per animal).

A. Examples of tets and stacks. Clearly, tets are much stronger frequency-modulated than stacks. Note that our wireless microphones show more power in the lower frequencies as compared with external microphones since they record the near field. B. Tet calls had shorter durations than stacks (P = 1.90e–19). In females, duration was slightly longer than in males (P = 0.0025). C. Tets had higher FM-scores than stacks (P = 0.0001) whereas FM-scores were generally lowest in females (P = 0.0003). All tests: REML in JMP10 with pairs as random factor. Pitch was not different between tets and stacks (not shown).

Figure 2. The detailed relationships between stack calls produced by pairs of zebra finches.

A. The temporal relationship is shown as a peristimulus-time-histogram (PSTH; upper graph), where the onset times of the male calls are aligned to the onset times of the female calls. The horizontal lines in the PSTH are the 1% confidence intervals. In the raster diagram (lower panel) the female calls are shown as red dots. Each male call is represented by a black dot. The probability of male stack calls occurring within half a second before or after the female stack is clearly and significantly increased. Data from one pair kept in a soundbox: 8472 male stacks and 11047 female stacks were recorded in a 35 h period (5 days with 7 h of recording each, starting at 8∶00 AM). Binwidth is 100 msec. B. Relative contributions of calls that were answered, were an answer, or were not connected to any stack call of the partner. Data from 5 established pairs.

Figure 3. Charting calling relationships in a group.

Four pairs of zebra finches. Based on the PSTH, metrics were calculated to describe the strength of the correlation between stack calls. The calls were recorded with carry-on microphones. Indicated in the upper matrix (A) are the PSTH’s from which the metrics were calculated. The animals to whose calls the PSTH’s were aligned are indicated along the left vertical side of the matrix. The animals whose calls were counted in the histograms are indicated along the bottom of the matrix. The lower matrix (B) shows the strength of the relationship regardless of symmetry. The matrix shows different possible calling relationships. For instance, pair 4 and pair 2 do not call with any other animal in the aviary. In contrast, the male of pair 1 is answered not only by the female of pair 1, but also by the female of pair 3. The partners of pair 3 are the only pair that did not interact at all in our experiments with groups. The associations of the callers with themselves are grayed out because they represent autocorrelations, whereas all the others are cross-correlations. Two sonograms of stack calls are shown in panel B. Duration in msec is shown underneath the sonograms.

Figure 4. Activity of RA neurons associated with calling and singing.

All data from one representative example where the same RA unit fired during song as well as before stack call production. The recording was 4 h. A. Properties of the recorded unit and the stack calling exchange of the recorded male with his partner. Left: Interspike interval (ISI) histogram of the unit that was isolated after sorting. The histogram describes a neuron that has a modal ISI of 30.4 msec, which is typical for RA neurons recorded in free moving finches. Center: PSTH of male and female stacks aligned on the 137 male calls. Right: 196642 superimposed waveforms of the unit. B. RA activity associated with different stack call categories. RA unit firings aligned to the onset of the stack call. The call is amplified x10 as compared with the song shown in C. Stack calls categorized as “answered” (green, N = 44), “answer” (red, N = 28), or “no connection” (dark grey, N = 65) are associated with elevated RA firing before the call is produced. The RA activity patterns are very similar and seem independent of the stack call category. The call has an average FM value of 24.3 which is well within the range for stacks. The stack does not resemble any song syllable C. Binned activity of an RA neuron, aligned to 33 songs produced by this animal. The pattern is aligned to the first of the three repeated syllables (arrow). Binwidth: 5 msec. During song production, the firing rate of the unit corresponds with specific syllables.