Sleep-dependent consolidation of auditory discrimination learning in adult starlings

Abstract

Memory consolidation is widely believed to benefit from sleep. Sleep-dependent memory consolidation has been established broadly in humans, appearing in declarative and procedural tasks. Animal studies have indicated a variety of mechanisms that could potentially serve as the neural basis of sleep-dependent consolidation, such as the offline replay of waking neural activity and the modulation of specific sleep parameters or synaptic strength during sleep. Memory consolidation, however, cannot be inferred from neuronal events alone, and the behavioral demonstration of sleep-dependent consolidation has been limited in animals. Here we investigated whether adult animals undergo sleep-dependent memory consolidation comparable to that of humans. European starlings (Sturnus vulgaris) were trained to discriminate between segments of novel starling song and retested after retention periods that included a regular night of sleep or consisted only of wakefulness. Auditory discrimination performance improved significantly after retention periods that included sleep but not after time spent awake, and the performance changes following sleep were significantly greater than after comparable periods of wakefulness. Thus, sleep produces a pattern of memory benefits in adult starlings that is fundamentally similar to the patterns of sleep-dependent consolidation observed in humans, suggesting a common sleep-dependent mechanism works across many vertebrate species to consolidate memories and establishing a robust animal model for this phenomenon.

Figure 1.

Performance accuracy. A, Performance was measured as the percentage of correct trials. For each pair of bars, the left/black bar denotes posttraining performance, and the right/gray bar denotes postretention performance. The leftmost four pairs of bars represent performance during the test sessions; the rightmost four pairs of bars represent the corresponding performance on the first 100 baseline trials after each test session. The three lowest significance bars show significant within-condition performance improvements. The significance bars at the three upper levels show that the performance improvement in the 24 h-AM, sleep, and 24 h-PM conditions were each significantly greater than the performance change in the wake condition. B, For each set of three bars, the left/black bar denotes posttraining performance, the middle/light-gray bar denotes the first postretention test performance, and the right/dark-gray bar denotes the second postretention test performance. The leftmost two sets of bars represent performance during the test sessions, and the rightmost two sets of bars represent the corresponding performance on the first 100 baseline trials after each test session. The lower significance bars show significant performance improvements across the given retention interval. The upper significance bars show that the performance change across the sleep retention interval was significantly greater than the performance change across the wake retention interval in both conditions. Data are the means ± SEM (*p < 0.05; **p < 0.01; ***p < 0.001).