Individual variation in neuron number predicts differences in the propensity for avian vocal imitation

Abstract

Avian song learning involves memorizing and reproducing song material produced by conspecifics. In several species song repertoire size correlates with the overall volume of two song-related brain regions, the HVc (acronym used as the proper name) and the robust nucleus of the archistriatum (RA). We raised male zebra finches with two adult tutors and found that individual differences in HVc volume and neuron number correlated positively with differences in the number of tutor syllables accurately copied. These results were replicated in a second study. The relationship between RA volume and song learning was similar, but less robust. Importantly, total repertoire size (number of song syllables) did not correlate significantly with anatomical measures of either the HVc or RA. Because previous work suggests that the volume and neuron number of these regions are not regulated by song learning, it is possible that naturally occurring variation in neuron number constrains how much song material can be copied or reproduced.Comparative analyses of neuroanatomical organization imply that an expansion of neural network space permits the development of more complex behavior. However, within species there is little evidence that individual differences in learning capacity relate to differences in brain space. Perhaps such relationships are elusive because the neural circuitry involved in learning a specific skill often participates in many different behaviors. However, in oscine songbirds a network of brain regions appears to be dedicated to the learning, production, and perception of song, and there are several indications that the sizes of these regions correlate with the capacity for song learning and production. Song is a male-typical behavior, and across species, sexual dimorphisms in the anatomy of songrelated brain nuclei relate to the degree of sex difference in vocal behavior (1-3). Also, the volume of one song region, the HVc, tends to be larger in males of those species with larger song repertoires than in those that produce simpler songs (4-6). This relationship seems not to reflect species differences in perceptual demands because population differences in repertoire size of marsh wrens correlate significantly with the size of the HVc in males (who produce the songs) but not in females (7). Finally, in at least two species individual differences in HVc size correlate with individual differences in song complexity. Male canaries that produce a large number of song syllables have a larger HVc than do those that have a smaller repertoire (8), and a similar relationship is evident within two different populations of marsh wrens (4). Despite these strong brain-behavior relationships, a causal relationship between the size of individual song regions and song learning has not been established.If such correlations between brain space and song complexity reflect a causal relationship, it could be that HVc growth is influenced by how much song material is learned. Song learning is tightly coupled with the additi...

Deafening-Induced Vocal Deterioration in Adult Songbirds Is Reversed by Disrupting a Basal Ganglia-Forebrain Circuit

“…For instance, individual differences in the rate of vocal deterioration reported here and previously (Nordeen and Nordeen, 1992;Brainard and Doupe, 2000b;Horita et al, 2008) may reflect natural variability in the degree to which HVC versus LMAN control RA output. The size of these structures (especially HVC) differs tremendously among individual adult zebra finches (Ward et al, 1998;Airey et al, 2000). Also, the diminishing effects of deafening with age (Lombardino and Nottebohm, 2000) could reflect a decline in the overall level of variability in LMAN activity (Kao and Brainard, 2006), and/or a greater influence of HVC-RA connections over behavior.…”

Social inhibition of song imitation among sibling male zebra finches

“…Another study (20) noted, anecdotally, that in a group of three male siblings, the youngest one produced the best song imitation and also had the greatest number of neurons in the high vocal center. High vocal center is a key nucleus in the pathway for song learning (21).…”

Sexually dimorphic expression of trkB, a Z-linked gene, in early posthatch zebra finch brain

“…In mice, haploinsufficiency of the trkB gene has a significant impact, lowering the number and density of neurons in the hippocampal dentate gyrus (29). Like the hippocampus of mammals, the songbird HVC receives a continuous supply of new neurons in adulthood (64,65), is important for song learning and memory, and is impacted strongly by the action of BDNF (38,(66)(67)(68). If trkB plays a similar role in these tissues, the effects of a haploinsufficiency in the HVC of zebra finches may be similar.…”