The relationship of neurogenesis and growth of brain regions to song learning - PubMed (original) (raw)
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The relationship of neurogenesis and growth of brain regions to song learning
John R Kirn. Brain Lang. 2010 Oct.
Abstract
Song learning, maintenance and production require coordinated activity across multiple auditory, sensory-motor, and neuromuscular structures. Telencephalic components of the sensory-motor circuitry are unique to avian species that engage in song learning. The song system shows protracted development that begins prior to hatching but continues well into adulthood. The staggered developmental timetable for construction of the song system provides clues of subsystems involved in specific stages of song learning and maintenance. Progressive events, including neurogenesis and song system growth, as well as regressive events such as apoptosis and synapse elimination, occur during periods of song learning and the transitions between variable and stereotyped song during both development and adulthood. There is clear evidence that gonadal steroids influence the development of song attributes and shape the underlying neural circuitry. Some aspects of song system development are influenced by sensory, motor and social experience, while other aspects of neural development appear to be experience-independent. Although there are species differences in the extent to which song learning continues into adulthood, growing evidence suggests that despite differences in learning trajectories, adult refinement of song motor control and song maintenance can require remarkable behavioral and neural flexibility reminiscent of sensory-motor learning.
Copyright © 2009 Elsevier Inc. All rights reserved.
Figures
Figure 1
Sagittal views of the major brain regions involved in song learning and production. While there is considerable overlap in the structures depicted in each schematic, the one on the left is designed to emphasize key structures involved in song vocal control whereas the diagram on the right illustrates important auditory structures. Left schematic: The pathway necessary for the production of learned song is demarcated by solid black lines. The anterior forebrain pathway, necessary for song learning, is shown with dashed lines, and dashed lines illustrate sites of convergence between the two pathways. Right Schematic: Key ascending auditory pathways are shown. Abbreviations: AV-nucleus avalanche; CLM-caudal lateral mesopallium; CMM-caudal medial mesopallium; CN-cochlear nucleus; CStcaudal striatum; DM-dorsal medial nucleus; DLM-medial portion of the dorsolateral nucleus of the thalamus; E-entopallium; B-basorostralis; HVC-high vocal center; LLD-lateral lemniscus, dorsal nucleus; LLI-lateral lemniscus, intermediate nucleus; LLV-lateral lemniscus, ventral nucleus; MLd-dorsal lateral nucleus of the mesencephalon; LMAN-lateral subdivision of the magnocellular nucleus of the anterior nidopallium; mMan-medial subdivision of the magnocellular nucleus of the anterior nidopallium; AreaX-Area X of the medial striatum; MO-oval nucleus of the mesopallium; NCM-caudal medial nidopallium; NIF-interfacial nucleus of the nidopallium; nXIIts-XII, tracheosyringeal part; OV-ovoidalis; PAm-paraambiguus; Ram- retroambigualis; RA-robust nucleus of the arcopallium; SO-superior olive; Uva-nucleus uvaeformis;. Nomenclature based on Reiner et al., in press. nAM-nucleus ambiguous. Adapted from (Reiner et al., 2004).
Figure 2
The distribution of [3H]-labelled neurons in sagittal brain sections from 1-year old canaries following [3H]-thymidine injections at the embryonic (E) ages indicated. The lower map is from a 1-year old adult that received [3H]-thymidine injections in October and was then killed 125 days later. Although there is an overall decrease in neurogenesis (cell production + survival) as development proceeds, the absolute magnitude of the decrease cannot be ascertained from these figures due to several methodological factors, including variation in the amount of time [3H]-thymidine was available for cell labeling (see Alvarez-Buylla et al., 1994). However, developmental shifts in the regional distribution of new neurons are significant. Between E5 and E9, sub-telencephalic neuron addition is virtually over with the notable exception of DLM (medial portion of the dorsolateral nucleus of the thalamus), part of the vocal control system. Injections on E10 labelled cells restricted to the telencephalon, yet few such cells were found in HVC. As with DLM, HVC neurogenesis is delayed relative to surrounding regions. Post-hatching (P6-P10), large numbers of neurons are added to the striatum, including song system nucleus Area X (not shown). The most notable difference between birds injected as juveniles and adults is a greater decline in striatal, relative to extra-striatal, neuron addition in older birds. Nevertheless, neuron addition is widespread even in adults. Dorsal = up and Rostral = left, Modified from (Alvarez-Buylla et al., 1994).
Figure 3
Much of the development of the efferent, HVC⇒RA pathway occurs over the time course of song learning. At the ages indicated, the HVC⇒RA pathway was retrogradely labeled (white) by injecting Fluoro-Gold into RA in male canaries. By 7-12 months, canary song has become fully stereotyped for the first time (Nottebohm and Nottebohm, 1978; Nottebohm et al., 1986). Dorsal = up, Rostral = right. Scale bar = 200μm.
Figure 4
Neuronal replacement in adult canaries. Upper left: A [3H]-labeled neuron (black dots overlying the nucleus) retrogradely labeled from RA with Fluoro-Gold (white deposits in cytoplasm) indicating an adult-formed HVC⇒RA neuron. Modified from (Kirn et al., 1999). Upper right: A pyknotic, degenerating neuron, also backfilled from RA with Fluoro-Gold. Transfer from long- to short day lengths resulted in a significant increase in the number of degenerating HVC⇒RA neurons in adult canaries and a decrease in the total number of HVC⇒RA neurons. Modified from (Kirn and Schwabl, 1997). Lower panels: HVC⇒RA neurons were labeled with latex microspheres and sacrificed after 20 days in late April (Lower left) or 6 months in October (lower right). This experiment was designed to determine how many HVC⇒RA neurons present in April, when canaries are singing stereotyped song, are still present the following October, when song becomes unstable and new song elements are added. The results suggest that between one-third and one-half of all such neurons are lost and replaced over this interval. Modified from (Kirn and Nottebohm, 1993). Scale bars in upper two panels = 10 μm. Scale bars in lower two panels = 200 μm.
Figure 5
A relationship between neuronal replacement and song modification in adult canaries. Upper graph: Twelve groups of adult male canaries (one group for each month) were injected with [3H]-thymidine and sacrificed one month later. The mean numbers of [3H]-labeled neurons (solid line) and pyknotic, degenerating cells (dashed line) per 1000 HVC neurons are shown. There were two peaks in new neuron addition, preceded by 2 peaks in cell death. The precise temporal relationship between peaks in addition and loss may not be accurately reflected by these data. Values are plotted by month of sacrifice, rather than month of [3H]-thymidine treatment. Other work indicates that there is a culling of new neurons when they are roughly two weeks old (Kirn et al., 1999). If this culling is responsible for seasonal changes in new neuron number seen at 1-month survivals, then the solid line for [3H]-labeled cell number should be left-shifted by two weeks, revealing greater overlap between death and replacement. Modified from Kirn et al., 1994). Lower graph: In a separate group of adult canaries, song modification was measured between one and two years of age by monthly counts of the mean number of new syllables added per month. Modified from (Nottebohm et al., 1986). Periods of high song modification correlate with periods of high neuronal replacement.
Figure 6
Adult behavioral and neural plasticity in a close-ended learner. Upper graph: Mean (+SEM) song stereotypy scores-the acoustical similarity across repeated deliveries of the same syllable, as a function of age. Data are for two groups of zebra finch males, “Young Adults” (recorded at 123-140 days, and again at 9-9.5 months and 15-15.5 months) and “Old Adults” (recorded at 3-3 years and 9 months at first recording and then two more times at the same intervals as the younger adults. There was a significant increase in song stereotypy across the recordings for the young, but not older adults. Modified from (Pytte et al., 2007). Middle graph: Adult song maintenance appears to be an active process guided by reference to auditory memories. However, an age-related decline in the reliance on auditory feedback for song maintenance was also found. The data show changes in syllable morphology between songs recorded before and 1-month after deafening performed at various ages (filled circles). For comparison, song similarity scores for age-matched controls are shown (open circles). Deafening at ages between 100-200 days after hatching has a much more dramatic effect on song structure compared to when birds are deafened at older ages (from Brainard and Doupe, 2001). Had longer intervals after deafening been examined, even old adults would eventually show modest song degradation (Lombardino and Nottebohm, 2000). Lower Graph: The number of new neurons (identified using [3H]-thymidine and retrograde labeling from RA (not shown) or Nissl stain) added to HVC declines with increasing age. Each triangle represents the mean number of [3H]-labeled neurons per day of [3H]-thymidine injections for a single bird (modified from Wang et al, 2002). Although precisely comparable ages across data sets are not available, collectively, the results suggest that change occurs at both behavioral and neural levels well beyond song crystallization. Moreover, the data suggest that as song stereotypy increases, the stability of the song motor program as well as the population of HVC⇒RA neurons increases.
Figure 7
Potential constraints on adult neuron addition. Nest mate similarities in HVC neuron addition persist even when one member of a nest mate pair is deafened in adulthood. Upper graph: Deafening in adulthood resulted in a significant increase in neuron addition (mean + SEM). Lower graph: However, the mean percentage of [3H]-labeled HVC neurons in nest mate pairs where one member was deafened in adulthood still showed a significant positive correlation. From Hurley et al., 2008.
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