Waking memory consolidation

One of the proposed purposes of sleep is that the brain requires time to consolidate new learning, and requires an inactive consciousness to do it. But so far it has been difficult to figure out exactly what the brain has to do to accomplish this and over what time span it happens, both desiderata for studying the phenomenon with brain imaging.

This week, two papers address what happens to memories associated with new learning between the exposure to the activities and when a subject finally gets to sleep. A paper by Philippe Peigneux and colleagues in PLoS Biology examines the neural correlates of learning in wakeful human subjects after learning a new task, and Forster and Wilson do the same for rats, focusing on "sequential replay" in the hippocampus.

A Nature commentary by Colgin and Moser helps to make sense of the problem:

Memories develop in several stages. After the initial encoding of new information during learning, memories are consolidated 'off-line', seemingly while not being actively thought about, through a cascade of events that is not well understood. In humans and other mammals, such an enhancement of recent memories may occur during sleep.... Although reactivation during sleep may provide a mechanism for consolidation of recent memories, the mystery remains as to how memories can be maintained as distinct entities for hours or days in sleep-deprived subjects, considering that the participating neurons are probably involved in myriad events before the subject is finally allowed to take a nap.

Peigneux and colleagues' study was the more relevant to learning in humans:

Neuroimaging studies have usually assessed the temporal and spatial evolution of the neuronal correlates of recent memories by scanning participants during the practice of a learning task, i.e. online, repeatedly after variable resting intervals. Here we characterized the offline evolution of the cerebral correlates of these recent memories, without the confounding effect of any concurrent practice of the learned material. Hence this paradigm reveals the neuronal activity underlying the maintenance of latent memories. Furthermore, we show that post-learning persistence and early reorganization of neuronal activity during wakefulness is a common feature both for hippocampus-independent (motor procedural) and hippocampus-dependent (spatial) memories, but with different time courses.

They made the people play Duke Nukem, exploring and learning a level of the game, and then they did fMRI to find out what their brains were doing while learning and for a long period of time afterward.

The results in a nutshell are given in the final paragraph:

Finally, the present study demonstrates learning-dependent changes in spontaneous regional brain activity during post-training wakefulness, similar to learning-dependent changes during post-training sleep [1-4], both for hippocampus-dependent and hippocampus-independent memories. Though these spontaneous offline activities may appear phenomenally similar, it is worth remembering that sleep and wakefulness are strikingly different vigilance states characterized by specific neuronal firing patterns, neuromodulatory context and gene expression [58]. The question remains unanswered as to how these parameters affect the functional status of the offline persistence of post-training cerebral activity for the processing and consolidation of recent memories during sleep and wakefulness. The present results suggest that post-training changes in regional cerebral activity during the first hours of post-training wakefulness are an integral part of the processing and maintenance of recent memories in the human brain, even when it is currently coping with unrelated cognitive demands.

In other words, the brain goes on building its new learned elements while awake, even though attention is directed to other activities.

Forster and Wilson found something interesting about those hippocampus-localized spatial learning tasks:

They studied rats running back and forth on a narrow track, and they recorded neural activity from so-called place cells10. These hippocampal cells have spatial receptive fields, so each cell responds when the animal is in a particular location. Food was placed at the ends of the track, and the animals stopped after every lap to eat. When the rat paused, sharp waves emerged in its hippocampus. During these sharp waves, the place cells from the running period were reactivated, but their order of firing was reversed with respect to their earlier order of activation on the track (Colgin and Moser 2006:616).

In other words, the cells do a "rewind" of the action, reinforcing it in reverse order. Forster and Wilson suggest that this sets wakeful response apart from sleep consolidation:

Reverse replay during the awake state can be contrasted with replay in sharp waves during slow-wave sleep, in which episodes of spatial experience are replayed in the same temporal order as that in which they were experienced. This re-expression of events while the animal occupies an entirely different physical and temporal context, as well as a different behavioural state, may have a role in memory consolidation during sleep. When awake, reverse replay occurs in situ, allowing immediately preceding events to be evaluated in precise temporal relation to a current, anchoring event, and so may be an integral mechanism for learning about recent events. Moreover, by converting single experiences into multiple reverse events, even after the first encounter in a new environment, awake replay represents efficient use of hard-won experience. Understanding this replay is likely to be critical to understanding how animals learn from experience.

I would guess this is may not be relevant to types of learning that aren't spatial, and in particular social and linguistic learning. But other mechanisms may be at play in similar pathways.

References:

Peigneux P, Orban P, Balteau E, Degueldre C, Luxen A, Laureys S, Maquet P. 2006. Offline persistence of memory-related cerebral activity during active wakefulness. PLoS Biol 4:e100. Full text

Colgin LL, Moser EI. Neuroscience: rewinding the memory record. Nature 440:615-617. DOI link