Influence of early-life nutritional stress on songbird memory formation

Abstract

In birds, vocal learning enables the production of sexually selected complex songs, dialects and song copy matching. But stressful conditions during development have been shown to affect song production and complexity, mediated by changes in neural development. However, to date, no studies have tested whether early-life stress affects the neural processes underlying vocal learning, in contrast to song production. Here, we hypothesized that developmental stress alters auditory memory formation and neural processing of song stimuli. We experimentally stressed male nestling zebra finches and, in two separate experiments, tested their neural responses to song playbacks as adults, using either immediate early gene (IEG) expression or electrophysiological response. Once adult, nutritionally stressed males exhibited a reduced response to tutor song playback, as demonstrated by reduced expressions of two IEGs (Arc and ZENK) and reduced neuronal response, in both the caudomedial nidopallium (NCM) and mesopallium (CMM). Furthermore, nutritionally stressed males also showed impaired neuronal memory for novel songs heard in adulthood. These findings demonstrate, for the first time, that developmental conditions affect auditory memories that subserve vocal learning. Although the fitness consequences of such memory impairments remain to be determined, this study highlights the lasting impact early-life experiences can have on cognitive abilities.

Keywords: IEG; auditory; developmental stress; electrophysiology; vocal learning; zebra finch.

Figure 1.

Relationship between body mass (mean ± s.e.) and age for nestling zebra finches reared on a control (ad libitum) or stressed (restricted) diet, in experiment 1 (a) and experiment 2 (b). Control and stressed subjects began and ended the nutritional stress paradigm at similar weights. However, during early-life deprivation, stressed nestlings weighed significantly less than controls (table 1 and text for details). An asterisk * indicates days when stressed nestlings were significantly lighter than controls. (Online version in colour).

Figure 2.

IEG expression levels (mean ± s.e.) for Arc (a) and ZENK (b) in the NCM and CMM in response to playback of tutor or novel songs in adult males raised under either control or stressed conditions. (a) n = 5 for all treatment groups, (b) n = 6 for control/tutor song, n = 5 for control/novel song, n = 5 for stressed/tutor song and n = 8 for stressed/novel song. Significant differences between treatment groups are symbolized: *p < 0.05, **p < 0.01. IEG expression after tutor song playback was higher in controls than stressed subjects (see text for details). (Online version in colour).

Figure 3.

Mean (±s.e.) tutor RRS (a), familiar RRS (b) and familiar FI (c) in the NCM and CMM of adult males raised under either control or stressed conditions. Significant difference between control and stressed birds are symbolized: *p < 0.05, **p < 0.01. Male subjects showed impaired neuronal memory for tutor song (a) and recently heard songs (b,c). (a) Tutor RRS scores were significantly lower in control than stressed subjects (scale reversed, mixed-effects model: p = 0.005), and only control birds had RRS < 0 (indicating response selectivity for tutor song). (b,c) Familiar RRS and FI indices were significantly higher in control than stressed subjects (RRS: p = 0.006, FI: p = 0.022) and only control birds had FI > 1 (indicating memory of the recently heard song). (Online version in colour).