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Sleep Is for Forgetting 464 • The Journal of Neuroscience, January 18, 2017 • 37(3):464–473 Dual Perspectives Dual Perspectives Companion Paper: Sleep to Remember, by Susan J. Sara Sleep Is for Forgetting Gina R. Poe Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, California 90095-7246 It is possible that one of the essential functions of sleep is to take out the garbage, as it were, erasing and “forgetting” information built up throughout the day that would clutter the synaptic network that defines us. It may also be that this cleanup function of sleep is a general principle of neuroscience, applicable to every creature with a nervous system. Key words: depotentiation; development; mental health; noradrenaline; REM sleep; spindles; theta; TR sleep Introduction was for forgetting useless tidbits of information learned through- In this article, I discuss and illustrate the importance of forgetting out the day that, if not eliminated, would soon saturate the mem- for development, for memory integration and updating, and for ory synaptic network with junk. Therefore, the type of forgetting resetting sensory-motor synapses after intense use. I then intro- we will discuss here is also not the global synaptic weight down- duce the mechanisms whereby sleep states and traits could serve scaling of the synaptic homeostasis hypothesis (SHY) (Tononi this unique forgetting function separately for memory circuits and Cirelli, 2003), although evidence from excellent experiments within reach of the locus coeruleus (LC) and those formed and used to support the idea of sleep for synaptic homeostasis will be governed outside its noradrenergic net. Specifically, I talk about used to make points here. Instead, this article will present lines of the role of rapid eye movement (REM) and transition-to-REM evidence supporting the idea that, whereas synaptic strengthen- (TR) sleep for hippocampal and somatosensory memories and ing underlying learning (long term potentiation, or LTP) can be the role of slow-wave sleep (SWS) for memories guided by the accomplished either in waking or sleep (Bramham and Srebro, dorsal striatum (e.g., motor and procedural learning). Finally, I 1989), (1) it is the targeted erasure of synapses that is unique to talk about mental health disorders, such as schizophrenia, post- sleep, (2) this targeted forgetting is necessary for efficient learn- traumatic stress disorder (PTSD), and autism, memory disorders ing, and (3) deficits in this process may underlie various kinds of like Alzheimer’s disease, and movement disorders, such as Par- intellectual disabilities and mental health problems. kinson’s disease, in light of these important sleep-dependent for- At a time when most studies regarding sleep and learning were getting functions and in light of treatment considerations. supporting the function of REM sleep for remembering, Nobel laureate Francis Crick and his colleague Graham Mitchison pub- Forgetting to avoid saturation lished a speculative article (Crick and Mitchison, 1983) postulat- As pointed out in the article titled “Sleep to Remember” by Susan ing that REM sleep might be for forgetting. They proposed that Sara in this issue, Jenkins and Dallenbach (1924) were the first to REM sleep is for forgetting all those extraneous things one learns demonstrate experimentally that sleep preserved memory from during the day that, if not disposed of, would cloud and confuse gradual degradation over time. They called this gradual rate of cognitive access to the important knowledge we must use to sur- forgetting “obliviscence.” However, the type of forgetting we will vive. They argued that all the experiences of the day need not be discuss in this article is not passive obliviscence, but rather the remembered and that, indeed, if all were retained, they would active, targeted erasure of synapses. It is what Crick and Mitchi- create a white noise problem wherein all modifiable synapses son (1983) had in mind when they hypothesized that REM sleep would eventually saturate with LTP and any incoming input would cause excitation that would spread like wildfire from cir- Received March 13, 2016; revised Sept. 16, 2016; accepted Oct. 5, 2016. cuit to circuit without distinction. Their hypothesis was purely The research cited and ideas developed at the Sleep and Memory laboratory were supported by National Insti- theoretical. Evidence will be presented here, from my own and tutes of Health Grant MH60670, Collaborative Research in Computational Neuroscience, and the Department of other studies, that the ideas of Crick and Mitcheson were pre- Anesthesiology at the University of Michigan. We thank past and present contributors to the research efforts in the scient and have been amply born out and expanded in multiple Sleep and Memory laboratory over the past 18 years; Esmeralda Montes and the two anonymous reviewers for readingthemanuscriptandprovidinghelpfulsuggestionstobetterclarifythepoints;andSusanSarafortheyearsof experiments. excellent experimentation and reporting that inspired this feature Dual Perspectives article. The author declares no competing financial interests. Hippocampal activity for forgetting during REM sleep Correspondence should be addressed to Dr. Gina R. Poe, Department of Integrative Biology and Physiology, One way to test whether Crick and Mitcheson were right that University of California, Los Angeles, 612 Charles E. Young Drive East, Box 957246, Los Angeles, CA 90095-7246. E-mail: [email protected]. sleep was for forgetting, or whether instead, sleep was for remem- DOI:10.1523/JNEUROSCI.0820-16.2017 bering is to test the activity of hippocampal neurons during sleep. Copyright © 2017 the authors 0270-6474/17/370464-10$15.00/0 The hippocampus is a temporary rapid assembly area for mem- Poe • Sleep Is for Forgetting J. Neurosci., January 18, 2017 • 37(3):464–473 • 465 Figure 1. Graphic depiction of the importance of weakening synapses to incorporate new information into old schemas. A, A simplified Christmas schema as might be presented to a small child. B, When that child first learns that Santa is a myth and therefore cannot bring the toys, the new information is laid upon the schema during waking. C, During sleep, the old schema is updated with thenewinformationtyingthegiftstothefamilymembersandinsertinga“no”tothe“SantaToys”iteminformationforanalteredbutsingularschemaofChristmas.DepotentiationoftheoldSanta belief is necessary to form this coherent new schema and make it accessible without confusion. ory. Hippocampal synapse numbers are limited compared with solidation from the hippocampus to storage places outside the those contained in the entire neocortical mantle, where long- hippocampus as described by Kim and Fanselow (1992). Such term memories are thought to be stored in a parallel, distributed theta trough firing could accomplish the refreshing of synapses fashion (Lashley, 1950). The hippocampus forms initial associa- that had encoded already-consolidated memories. However, not tive memories and temporarily stores them until they are consol- yet consolidated memories remain reactivated at theta peaks idated to the neocortex. It is logical, therefore, that the hipp- (Poe et al., 2000), consistent with a synaptic strengthening and ocampal network of weighted synapses involved with already remembering function of REM sleep for these memories that consolidated memories should be recycled for future differential have not been “downloaded” to the neocortex. Thus, REM weighting, such that it is free to form new associative links during sleep would serve to maintain or strengthen memories until future learning involving other sets of hippocampal functional they are transferred outside the hippocampus whereupon they assemblies. should be erased from that space-limited short-term memory Hippocampal place cells form a functional assembly to map factory, allowing those synapses to be used to encode new an animal’s environment. Place cells are most active at the peaks associative memories. of theta frequency (5–10 Hz) local field potential patterns during active waking. Such theta peak activity is consistent with Forgetting necessary to incorporate novel information into strengthening synapses (LTP) during the learning process. Theta established schema peaks correspond to the maximum depolarization phase of the Depotentiation, the reverse of LTP, is also induced by learning, cell membrane during the theta cycle, and such subthreshold such as during novel spatial exploration (Xu et al., 1998), and membrane depolarization allows neuron to respond robustly to seems to be necessary to encode the introduction of new stimuli inputs, e.g., as the neuron discharges through the place field in a familiar contextual schema (Kemp and Manahan-Vaughan, (Buzsa´ki et al., 1983; Fox et al., 1986). Pavlides et al. (1988) found 2004). The updating of schema, a term used here to represent that stimulation on the positive phase of the hippocampal theta related memory sets, such as the set of place memories associated rhythm induced LTP whereas stimulation at the opposite phase, with the concept of “home,” is a function important for cognition the theta trough, induced a decrease in synaptic efficacy (depo- (Manahan-Vaughan and Braunewell, 1999; Braunewell and tentiation). Huerta and Lisman (1995) and others have replicated Manahan-Vaughan, 2001; Nakao et al., 2002). The hypothesis this robust finding. I hypothesized that, if REM sleep is for learn- that REM sleep is a unique time for forgetting would
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