Neurogenesis and Song Learning
The involvement of neurogenesis in learning was first shown in the avian brain by Fernando Nottebohm and colleagues (Nottebohm, 1989). His papers throughout the 1970’s and 1980’s built a body of work that effectively overturned the notion that no new neurons are born into the adult brain, and led to a general acceptance of adult neurogenesis. The reason he was so successful was because he was able to show that these new neurons are involved in learning, and functionally integrate into existing circuitry. In his 1989 review of his findings, the subtitle states: “Such neurogenesis could hold the key to brain self-repair in humans.” The study of neurogenesis and neuronal replacement in birds paved the way for modern neurogenesis research in humans, and the connection between neurogenesis and learning.
Figure 1. Song-Learning Circuitry of the Canary Brain
(adapted from Alvarez-Buylla, Theelen, and Nottebohm, 1988)
Research By Fernando Nottebohm and Colleagues
Fernando Nottebohm describes canary song learning as having analogies to the acquisition of language in humans. Song birds, like humans, have a strict window of time before sexual maturity during which they must learn by imitating models (parents). Once they go through the babbling infant, or subsong stage, male birds acquire a more structured plastic song, followed by a stable song, which is developed around the same time as sexual maturity. There is also the analogous critical period before adulthood when a bird (like a human) must learn how to produce the proper song. Dr. Nottebohm’s work with canaries was, in part, inspired by the observation that the volumes of the “song” areas of the brain (see Figure 1) were greater in males (who sang complex songs) than in females (who sang simpler songs). He found that severe song deficits occurred when the HVc and RA were lesioned (Nottebohm et al., 1976). This study also traced the pathways (shown in Figure 1) between some of these key brain areas. Later studies were able to show neurogenesis in adult canaries, and mapped the migration and circuit integration of the new neurons (Alvarez-Buylla et al., 1988; Nottebohm, 1989; Barkan et al., 2006). His and other work showed that the volumes of the male canary RA and HVc depend on the seasonal fluctuations in testosterone (T) associated with plastic song (late fall to early spring), and stable song (spring-early fall/mating season) (Nottebohm, 1989; Brainard & Doupe, 2002). See Figure 2.
Figure 2. Seasonal Fluctuation in Song
Dr. Nottebohm also concluded that the volume changes in the RA were due to a change in the number of synaptic connections, whereas the volume of the HVc changed due to death and subsequent renewal of neurons – this suggests that newly generated neurons replace dying ones (neuronal replacement) in the avian brain (Notebohm, 1989).
The work of Nottebohm and colleagues continues to lead this field. Recent research as shown that neurons in the auditory cortex (AC) are specialized for specific sounds, and can even be shaped by experience (Brainard & Doupe, 2002). A study by Barkan et al. (2006) showed that a brain area called the nidopallium caudale (NC) is also involved in sound processing. The amount neurogenesis in the NC was proportional to the number of offspring fledged, which suggests that these new neurons play a role in the parent learning to recognize fledglings by their vocalizations. Although this field has made progress, much remains to be understood about the acquisition of song. Different bird species have different learning patterns and criteria, which makes it difficult to generalize neural circuitry for song production (Brainard & Doupe, 2002). More work still needs to be done in order to determine the functional role of neurogenesis in song learning.
Neurogenesis and Food Storage/Retrieval
Besides song learning, hippocampal neurogenesis is also evaluated through the examination of spatial learning. This type of learning is evaluated by behavioral aspects of food storage and retrieval in bird species such as the black-capped chickadee (Parus Atricapilus), mountain chickadees (Poecile gambeli), and hand-raised marsh tits (Parus palustris). Such experiments evaluated the amount of new born cells and their survival rate based upon necessity by seasonal changes and complexity of the surrounding environment (enrichment). Investigations into the relationship between spatial learning and hippocampal neurogenesis utilized techniques such as thymidine labeling. Initial studies, such as the one performed by Barnea and Nottebohm in 1994, have demonstrated that a large number of hippocampal neurons are constantly born in the adult chickadee brain in response to seasonal changes, i.e. the fall when food storage is most important.
Figure 3: Seasonal Fluctuation in Neuronal Survival
This study also put forth results that demonstrated both free-ranging birds and those kept in captivity exhibited proliferation of new cells, however, captives demonstrated approximately half of the neuronal growth of those in the wild (Barnea, 1994). Finally, this initial study by Nottebohm also showed that the rostral hippocampal complex had the most neuronal addition and neuonal turnover in comparison to the mid section and caudal part of the hippocampus
Figure 4: Neurogenesis in the Avian Hippocampal Complex (Adapted from Barnea, 1994)
Despite these initial results, the relationship between spatial learning and hippocampal growth has been up for debate. A more recent study performed by LaDage in 2009 examined different conditions of surrounding environment and the effects on spatial memory. The LaDage study utilized certain neurological markers (i.e. doublecortin) in order to quantify the amount of proliferating cells within 3 experimental groups: free ranging subjects, subjects kept in enriched captivity, & subjects in captivity where memory experiences were restricted. The results demonstrated that the highest amount of proliferating cells were found in the free ranging experimental group, followed by subjects contained in enriched captivity. Subjects kept in memory restricted captivity demonstrated the lowest amount of hippocampal neurogenesis. (Fig. 5) The results from this study were also consistent with the results found by Barnea & Nottebohm in 1994 in that free ranging subjects showed a marked increase in neurogenesis than those kept in captive (LaDage, 2009).
Figure 5: Number of New Neurons and Experience Condition (LaDage, 2009)
These studies not only spurred further research into the occurrence of neurogenesis in bird species, but also laid the groundwork for further investigation into neurogenesis within other higher functioning animals as well.
Thank you to Fernando Nottebohm and Rudi Bellani at The Rockefeller University for providing the sound examlpes of canary song.
Page By: Alyssa Wheeler and Loretta Cacace