Timothy P. Brawn

Consolidating the Effects of Waking and Sleep on Motor-Sequence Learning

Sleep is widely believed to play a critical role in memory consolidation. Sleep-dependent consolidation has been studied extensively in humans using an explicit motor-sequence learning paradigm. In this task, performance has been reported to remain stable across wakefulness and improve significantly after sleep, making motor-sequence learning the definitive example of sleep-dependent enhancement. Recent work, however, has shown that enhancement disappears when the task is modified to reduce task-related inhibition that develops over a training session, thus questioning whether sleep actively consolidates motor learning. Here we use the same motor-sequence task to demonstrate sleep-dependent consolidation for motor-sequence learning and explain the discrepancies in results across studies. We show that when training begins in the morning, motor-sequence performance deteriorates across wakefulness and recovers after sleep, whereas performance remains stable across both sleep and subsequent waking with evening training. This pattern of results challenges an influential model of memory consolidation defined by a time-dependent stabilization phase and a sleep-dependent enhancement phase. Moreover, the present results support a new account of the behavioral effects of waking and sleep on explicit motor-sequence learning that is consistent across a wide range of tasks. These observations indicate that current theories of memory consolidation that have been formulated to explain sleep-dependent performance enhancements are insufficient to explain the range of behavioral changes associated with sleep.

Sleep-Dependent Consolidation of Auditory Discrimination Learning in Adult Starlings

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.

Consolidation of sensorimotor learning during sleep

Consolidation of nondeclarative memory is widely believed to benefit from sleep. However, evidence is mainly limited to tasks involving rote learning of the same stimulus or behavior, and recent findings have questioned the extent of sleep-dependent consolidation. We demonstrate consolidation during sleep for a multimodal sensorimotor skill that was trained and tested in different visual-spatial virtual environments. Participants performed a task requiring the production of novel motor responses in coordination with continuously changing audio-visual stimuli. Performance improved with training, decreased following waking retention, but recovered and stabilized following sleep. These results extend the domain of sleep-dependent consolidation to more complex, adaptive behaviors.

Sleep Consolidation of Interfering Auditory Memories in Starlings

Memory consolidation has been described as a process to strengthen newly formed memories and to stabilize them against interference from similar learning experiences. Sleep facilitates memory consolidation in humans, improving memory performance and protecting against interference encountered after sleep. The European starling, a songbird, has also manifested sleep-dependent memory consolidation when trained on an auditory-classification task. Here, we examined how memory for two similar classification tasks is consolidated across waking and sleep in starlings. We demonstrated for the first time that the learning of each classification reliably interferes with the retention of the other classification across waking retention but that sleep enhances and stabilizes the memory of both classifications even after performance is impaired by interference. These observations demonstrate that sleep consolidation enhances retention of interfering experiences, facilitating opportunistic daytime learning and the subsequent formation of stable long-term memories.

In vitro and in vivo charge capacity of AIROF microelectrodes.

Activated Iridium Oxide Film (AIROF) microelectrodes are thought to be well-suited for neural stimulation of the cortex because they can sustain high charge capacity (about ten times higher than Pt microelectrodes) when characterized in phosphate-buffered saline (PBS) or other high ionic strength electrolytes. However, it is known that their capacity diminishes after they are implanted in vivo. It has been suggested that tissue encapsulation is an underlying cause. In this paper, we report electrochemical measurements of AIROF microelectrodes that were performed acutely in the brain of the zebra finch. The experiment showed that the interstitial fluid environment in the birds brain did not maintain the high charge delivery capacity of the AIROF microelectrodes. A simple compensation for access resistance may create hazards to sustained electrode integrity

Differential development of retroactive and proactive interference during post-learning wakefulness

Newly encoded, labile memories are prone to disruption during post-learning wakefulness. Here we examine the contributions of retroactive and proactive interference to daytime forgetting on an auditory classification task in a songbird. While both types of interference impair performance, they do not develop concurrently. The retroactive interference of task-B on task-A developed during the learning of task-B, whereas the proactive interference of task-A on task-B emerged during subsequent waking retention. These different time courses indicate an asymmetry in the emergence of retroactive and proactive interference and suggest a mechanistic framework for how different types of interference between new memories develop.

Chapter 6 – Sleep and Learning in Birds: Rats! There’s More to Sleep

The role of sleep in learning has often been viewed in terms of memory consolidation in mammalian systems, but understanding the functions of sleep and learning can be informed by a broader evolutionary and ethological perspective. Here we advocate the value of combining behavioral and neuronal observations to study sleep mechanisms of learning by developing examples in two songbird species. In European starlings ( Sturnus vulgaris ), we describe an auditory classification learning paradigm that was modeled after the design of sleep-memory studies in humans and that replicates the pattern of performance changes commonly observed in humans across waking and sleeping retention. In zebra finches ( Taeniopygia guttata ), we describe how neural processing during sleep is involved in song maintenance in adult birds and in the developmental learning of song in juvenile birds. Throughout, we discuss the results in relation to work in mammals and suggest future directions to more closely connect the behavioral effects of sleep with the neural mechanisms underlying sleep-dependent memory consolidation.

Sleep and Learning in Birds

The role of sleep in learning has often been viewed in terms of memory consolidation in mammalian systems, but understanding the functions of sleep and learning can be informed by a broader evolutionary and ethological perspective. Here we advocate the value of combining behavioral and neuronal observations to study sleep mechanisms of learning by developing examples in two songbird species. In European starlings ( Sturnus vulgaris ), we describe an auditory classification learning paradigm that was modeled after the design of sleep-memory studies in humans and that replicates the pattern of performance changes commonly observed in humans across waking and sleeping retention. In zebra finches ( Taeniopygia guttata ), we describe how neural processing during sleep is involved in song maintenance in adult birds and in the developmental learning of song in juvenile birds. Throughout, we discuss the results in relation to work in mammals and suggest future directions to more closely connect the behavioral effects of sleep with the neural mechanisms underlying sleep-dependent memory consolidation.

Sleep and Learning in Birds: Rats! There’s More to Sleep

The role of sleep in learning has often been viewed in terms of memory consolidation in mammalian systems, but understanding the functions of sleep and learning can be informed by a broader evolutionary and ethological perspective. Here we advocate the value of combining behavioral and neuronal observations to study sleep mechanisms of learning by developing examples in two songbird species. In European starlings ( Sturnus vulgaris ), we describe an auditory classification learning paradigm that was modeled after the design of sleep-memory studies in humans and that replicates the pattern of performance changes commonly observed in humans across waking and sleeping retention. In zebra finches ( Taeniopygia guttata ), we describe how neural processing during sleep is involved in song maintenance in adult birds and in the developmental learning of song in juvenile birds. Throughout, we discuss the results in relation to work in mammals and suggest future directions to more closely connect the behavioral effects of sleep with the neural mechanisms underlying sleep-dependent memory consolidation.