Sara Carletto
Thomas Borsato
Marco Pagani- 1Department of Clinical and Biological Sciences, University of Turin, Turin, Italy
- 2Department of Psychology, University of Milano-Bicocca, Milan, Italy
- 3Institute of Cognitive Sciences and Technologies, National Research Council, Rome, Italy
Post-traumatic stress disorder (PTSD) is a clinical condition that may develop after a person experienced a traumatic event. PTSD can be considered as a disorder in which a fear conditioned response fails to extinguish, leading to several symptoms such as re-experiencing of the traumatic moment with intrusive thoughts, flashbacks, and nightmares, avoidance of situations related to the trauma, negative alterations in cognitions and mood, and hyper-arousal.
One important feature of PTSD is the re-experiencing of specific aspects of the traumatic memory. This aspect is related to the fact that, as originally suggested by Van Der Kolk et al. (1997); Van Der Kolk (1998), traumatic memories are encoded differently than memories of ordinary events, including several multisensory fragments that cannot be integrated in a structured meaningful narrative.
At a neurobiological level, memories recorded during extreme stressful situations cause a maximal potentiation of amygdalar synapses, assumed to temporarily store the events. This causes the saturation of all amygdalar alpha-amino-3-hydroxy-5-methyl-4-isoxazole (AMPA) receptors-bindings sites, preventing the recorded emotional memory trace to be merged with the cognitive memory trace from the hippocampus (Corrigan, 2002; Harper et al., 2009). Therefore, the fragments of emotionally charged memories remain trapped in the limbic system and cannot be transfered to the cortical areas, where a further processing and integration into already existing networks should take place.
Eye Movement Desensitization and Reprocessing (EMDR) was initially proposed in the late 80's by Francine Shapiro (Shapiro, 1989) and it's now a well-established psychological treatment for PTSD (Bradley et al., 2005; Chen et al., 2014). EMDR is a complex therapeutic approach that integrates elements of many traditional psychological orientations, but one of the key aspects is the use of Alternate Bilateral Stimulations (ABS) such as eye movements (EMs). Over recent years a large debate has developed whether EMs are an active treatment component and if the mechanisms responsible for EMDR efficacy differ substantially from those operating in trauma-focused cognitive behavioral therapy and standard exposure therapy. The original theory of Adaptive Information Processing (AIP), which is the basis of EMDR (Shapiro, 2001), posits that humans have an innate information processing system that assimilates new experiences into already existing memory networks. Pathology arises when new information is inadequately processed and then stored in a maladaptive mode in the memory networks, along with associated distorted thoughts, sensations and emotions. When memories are adequately processed, symptoms can be alleviated and memories integrated. EMDR seems to facilitate the access to and processing of the components of traumatic memories bringing them to an adaptive resolution (Shapiro, 2001). EMDR therefore aims at re-elaborating non-integrated memories and consolidating new memories into already existing semantic links, promoting the insertion of traumatic but no longer disturbing memory in a coherent and adaptive autobiography.
In recent years, the crucial role of sleep in memory consolidation has been highlighted (Stickgold and Walker, 2007; Rasch and Born, 2013). Physiological normal sleep presents a cyclic alternated pattern of Rapid Eye Movement (REM) and non-REM Slow Wave Sleep (SWS). EEG recordings show synchronous delta wave activity (0.5–4 cycles/sec, i.e., 0.5–4 Hz) during SWS, and synchronous theta waves (4–8 Hz) during REM sleep. The non-REM SWS appears to play a key role in memory consolidation, as edited memories are transferred from the hippocampus to the neocortex, and then integrated into neocortical neuronal networks upon this phase.
During the waking state, new memories are encoded in a temporarily form in the hippocampal network. Over SWS, such hippocampal memories are reactivated by slow oscillations (< 1 Hz) originating from the cortical networks in which the encoding originally took place (Born et al., 2006).
The combined activation of hippocampal memories and cortical synapses favors the transfer back to the neo-cortex, and during REM sleep the memories might be further consolidated and integrated in already existing associative links, therefore promoting a meaningful narrative of the event.
As mentioned above, traumatic memories may cause over-potentiation of amygdalar synapses, while the recording of the episodic aspect of the memory in the hippocampus results in a normal potentiation of hippocampal synapses. This difference in potentiation between amygdalar and hippocampal synapses makes impossible to merge the emotional and cognitive aspects of the traumatic memory, which normally takes place via the anterior cingulated cortex, then preventing the subsequent transfer to neocortex (Harper et al., 2009). Therefore, non-processed emotional memories remain trapped and unchanged at subcortical level without contextual integration, causing in some cases PTSD symptoms.
The first who proposed a similarity between EMDR physiological effects and sleep processes was Stickgold (2002), focusing mainly on REM sleep. Moving a step forward, one of the hypothesized mechanism of action of EMDR posits a parallel between synaptic depotentiation occurring during SWS and EMDR bilateral stimulation (Harper et al., 2009; Pagani et al., 2017). During EMDR the client is asked to hold into attention the fragmented traumatic materials while the therapist performs the ABS, favoring the reactivation of the traumatic memory in amygdalar and hippocampal networks. Recent findings have shown that ABS elicits delta waves in a range (1.5 Hz) very similar to the one registered during SWS (Rétey et al., 2005; Harper et al., 2009; Pagani et al., 2011, 2012). It is then conceivable that EMDR bilateral stimulation mimics the low-frequency stimulations naturally occurring during SWS, causing a depotentation of AMPA receptors of amygdalar synapses, which in turn facilitates the merging of the amygdalar emotional and the hippocampal episodic memories thus creating an associative memory that can be further transferred and processed by neocortical areas, leading to the cessation of symptoms.
This hypothesis on EMDR mechanism of action is also supported by previous neuroimaging findings. Pagani et al. (2012) showed a shift of cortical activation elicited by traumatic memories after successful EMDR treatment from an implicit subcortical to an explicit cortical state suggesting their integration into existing semantic memory. Herkt et al. (2014) observed an increased activation in the right amygdala during auditory ABS upon processing of negative emotional stimuli, suggesting that an initial enhancement of emotional processing is a prerequisite for the effective reintegration of traumatic material.
Other neurobiological findings frequently reported by neuroimaging studies in PTSD are supporting this hypothesis. Three main brain areas have been identify to be altered in PTSD: amygdala, involved in emotional interpretation of incoming information (Etkin and Wager, 2007; Francati et al., 2007; Patel et al., 2012), medial prefrontal cortex (mPFC), implicated in the processing of emotional materials and in emotion regulation (Shin et al., 2006; Patel et al., 2012; Nicholson et al., 2017) and hippocampus, involved in contextual learning and spatial and episodic memory (Burgess et al., 2002; Liberzon and Sripada, 2008; Liberzon and Abelson, 2016). The most recurrent finding is a relative decreased mPFC activity and a parallel increased amygdalar activation. In light of the SWS hypothesis such hyperactivation could be considered as the macroscopic expression of the molecular-level alteration, i.e., the above described over-potentiation of amygdalar synapses. At the same time mPFC, despite its tight connection with the limbic system, doesn't exert its role of normalizing amygdalar hyperactivity, probably as a consequence of the remarkable hyper-activation of the latter. The insufficiency of top-down prefrontal cortex functioning, coupled with dysregulated bottom-up activity of limbic structures accounts as well for the impaired autonomic response and concomitant inadequate emotional regulation peculiar of PTSD.
Recently, a pathologic bottom up mechanism involving cerebellum in PTSD has also been proposed (Carletto and Borsato, 2017). This structure has a key role in associative learning, fear regulation, attention, and in motor control (Wolf et al., 2009; Schmahmann, 2010) and it is strongly interconnected to cerebral cortex (Bergmann, 2008). Growing evidence shows altered functions of cerebellum in PTSD patients (Osuch et al., 2001; Anderson et al., 2002; Pissiota et al., 2002), with traumatic reminders ehnancing its activation (Fernandez et al., 2001; Driessen et al., 2004). Furthermore, cerebellar volume is smaller in adults with PTSD than in healthy controls (De Bellis and Kuchibhatla, 2006; Carrion et al., 2009; Baldaçara et al., 2011), and this reduction is associated with the magnitude of PTSD symptoms.
Cerebellum has also an indirect link to PTSD since it is a key structure in associative learning. In fact, PTSD can be described as the result of a fear conditioned response where extinction fails (Milad et al., 2009; VanElzakker et al., 2014). More specifically it is a conditioning to the context rather than to a specific stimulus (Davis et al., 2010) and it is well-documented how cerebellum appears to be involved in both conditioning and extinction process (Sacchetti et al., 2005; Kim and Jung, 2006). In a rodent study, Sacchetti et al. (2007) showed how cerebellum could be as crucial as amygdala in long term fear memories: when amygdala is inactivated the fear-conditioning response is carried out by cerebellum.
Zhu et al. (2006) analyzed the extensive connectivity between cerebellum and whole brain suggesting that this area is an essential modulator and coordinator of visceral and behavioral response through cerebellar-hypothalamic circuit.
Cerebellum has also a central role in the sleep-wake cycle (Cunchillos and De Andrés, 1982; de Andrés et al., 2011; DelRosso and Hoque, 2014). There seem to be a bidirectional interaction between cerebellum and sleep: malfunction of cerebellum affects quality of sleep but also quality of sleep affects cerebellum dependent memory formation and memory consolidation (Canto et al., 2017). Patients with spinocerebellar ataxia, a degenerating pathology of cerebellum and its connections, show alterations in sleep stages as well in non-wakefullness. In this way cerebellum tunes neocortical forms of sleep related activity (Pedroso et al., 2011; Canto et al., 2017). On the other hand, sleep improves cerebellar learning as learning-dependent timing, procedural memory formation, and spatiotemporal predictions of motor actions (Verweij et al., 2016).
Fogel et al. (2015) reported that sleep after a procedural task showed an increment in SWS density, highlighting a putative cerebellar involvement.
Typically, cerebellar activity decreases during the transition from pre-sleep wakefulness to SWS (Braun et al., 1997; Hofle et al., 1997; Kajimura et al., 1999; Hiroki, 2005). During SWS cerebellar fMRI signals co-occurred with slow waves in neo cortex, and the level of density of those waves in cerebellum was correlated with gray matter volume (Dang-Vu et al., 2008; Saletin et al., 2013).
According to Born et al. (2006) since the synchronization caused by slow oscillations during SWS is not restricted to neocortex but spreads to hippocampus, thalamus, and brainstem, it can be speculated that also cerebellum is involved in such synchronous activation which in turn might favor its involvement in processing the procedural aspect of the psychological trauma, an essential component of therapy successful outcome.
The role of cerebellum in such process needs further investigations: cerebellar transcranial Direct Current Stimulation (tDCS), a form of brain polarization that influences motor functions and learning processes (Gandiga et al., 2006) could be a promising tool in understanding this complex relation. Previous findings have shown that tDCS applied to frontocortical regions induced an increase in SWS and enhanced consolidation of hippocampal-dependent declarative memories (Marshall et al., 2004, 2006). Moreover, a recent study (Ferrucci et al., 2013) indicated that cerebellar tDCS improves implicit procedural learning. This technique could be potentially coupled with Electroencephalography, assessing brain frequencies evoked by this manipulation, in particular testing if cerebellar electrical field modulation could lead to a “SWS-like” brain activity.
In conclusion, this opinion article aims at underlining the role of SWS in the physiological storage of memories and its participation in putative mechanisms of recover from conditions in which memory remains pathologically unprocessed, as in PTSD. This will also stimulate further research, both at theoretical and experimental levels, on the role of various structures in formation, consolidation, and reprocessing of traumatic memories.
In our opinion, there is a need of deepening the current model of PTSD going beyond the role of top-down processes. Investigating other brain regions such as cerebellum in bottom-up processes involved in PTSD will allow to better understand the underlying mechanisms of this disorder and to promote effective and neurobiologically-grounded therapies for trauma treatment.
Author Contributions
MP and TB were responsible for the conception of the hypothesis outlined. SC wrote the article, that was integrated and critically revised by MP and TB. All authors have approved the final manuscript.
Conflict of Interest Statement
All authors have been invited as speakers in national and international EMDR conferences.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
Anderson, C. M., Teicher, M. H., Polcari, A., and Renshaw, P. F. (2002). Abnormal T2 relaxation time in the cerebellar vermis of adults sexually abused in childhood: potential role of the vermis in stress-enhanced risk for drug abuse. Psychoneuroendocrinology 27, 231–244. doi: 10.1016/S0306-4530(01)00047-6
Baldaçara, L., Jackowski, A. P., Schoedl, A., Pupo, M., Andreoli, S. B., Mello, M. F., et al. (2011). Reduced cerebellar left hemisphere and vermal volume in adults with PTSD from a community sample. J. Psychiatr. Res. 45, 1627–1633. doi: 10.1016/j.jpsychires.2011.07.013
Bergmann, U. (2008). The neurobiology of EMDR: exploring the thalamus and neural integration. J. EMDR Pract. Res. 2, 300–314. doi: 10.1891/1933-3196.2.4.300
Born, J., Rasch, B., and Gais, S. (2006). Sleep to remember. Neurosci. Rev. J. Bringing Neurobiol. Neurol. Psychiatry 12, 410–424. doi: 10.1177/1073858406292647
Bradley, R., Greene, J., Russ, E., Dutra, L., and Westen, D. (2005). A multidimensional meta-analysis of psychotherapy for PTSD. Am. J. Psychiatry 162, 214–227. doi: 10.1176/appi.ajp.162.2.214
Braun, A. R., Balkin, T. J., Wesenten, N. J., Carson, R. E., Varga, M., Baldwin, P., et al. (1997). Regional cerebral blood flow throughout the sleep-wake cycle. An H2(15)O PET study. Brain J. Neurol. 120 (Pt 7), 1173–1197. doi: 10.1093/brain/120.7.1173
Burgess, N., Maguire, E. A., and O'Keefe, J. (2002). The human hippocampus and spatial and episodic memory. Neuron 35, 625–641. doi: 10.1016/S0896-6273(02)00830-9
Canto, C. B., Onuki, Y., Bruinsma, B., van der Werf, Y. D., and De Zeeuw, C. I. (2017). The sleeping cerebellum. Trends Neurosci. 40, 309–323. doi: 10.1016/j.tins.2017.03.001
Carletto, S., and Borsato, T. (2017). Neurobiological correlates of post-traumatic stress disorder: a focus on cerebellum role. Eur. J. Trauma Dissociation 1, 153–157. doi: 10.1016/j.ejtd.2017.03.012
Carrion, V. G., Weems, C. F., Watson, C., Eliez, S., Menon, V., and Reiss, A. L. (2009). Converging evidence for abnormalities of the prefrontal cortex and evaluation of midsagittal structures in pediatric posttraumatic stress disorder: an MRI study. Psychiatry Res. 172, 226–234. doi: 10.1016/j.pscychresns.2008.07.008
Chen, Y. R., Hung, K. W., Tsai, J. C., Chu, H., Chung, M. H., Chen, S. R., et al. (2014). Efficacy of eye-movement desensitization and reprocessing for patients with posttraumatic-stress disorder: a meta-analysis of randomized controlled trials. PLoS ONE 9:e103676. doi: 10.1371/journal.pone.0103676
Corrigan, F. M. (2002). Mindfulness, dissociation, emdr and the anterior cingulate cortex: a hypothesis. Contemp. Hypn. 19, 8–17. doi: 10.1002/ch.235
Cunchillos, J. D., and De Andrés, I. (1982). Participation of the cerebellum in the regulation of the sleep-wakefulness cycle. Results in cerebellectomized cats. Electroencephalogr. Clin. Neurophysiol. 53, 549–558. doi: 10.1016/0013-4694(82)90067-0
Dang-Vu, T. T., Schabus, M., Desseilles, M., Albouy, G., Boly, M., Darsaud, A., et al. (2008). Spontaneous neural activity during human slow wave sleep. Proc. Natl. Acad. Sci. U.S.A. 105, 15160–15165. doi: 10.1073/pnas.0801819105
Davis, M., Walker, D. L., Miles, L., and Grillon, C. (2010). Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 35, 105–135. doi: 10.1038/npp.2009.109
de Andrés, I., Garzón, M., and Reinoso-Suárez, F. (2011). Functional Anatomy of Non-REM Sleep. Front. Neurol. 2:70. doi: 10.3389/fneur.2011.00070
De Bellis, M. D., and Kuchibhatla, M. (2006). Cerebellar volumes in pediatric maltreatment-related posttraumatic stress disorder. Biol. Psychiatry 60, 697–703. doi: 10.1016/j.biopsych.2006.04.035
DelRosso, L. M., and Hoque, R. (2014). The cerebellum and sleep. Neurol. Clin. 32, 893–900. doi: 10.1016/j.ncl.2014.07.003
Driessen, M., Beblo, T., Mertens, M., Piefke, M., Rullkoetter, N., Silva-Saavedra, A., et al. (2004). Posttraumatic stress disorder and fMRI activation patterns of traumatic memory in patients with borderline personality disorder. Biol. Psychiatry 55, 603–611. doi: 10.1016/j.biopsych.2003.08.018
Etkin, A., and Wager, T. D. (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am. J. Psychiatry 164, 1476–1488. doi: 10.1176/appi.ajp.2007.07030504
Fernandez, M., Pissiota, A., Frans, O., von Knorring, L., Fischer, H., and Fredrikson, M. (2001). Brain function in a patient with torture related post-traumatic stress disorder before and after fluoxetine treatment: a positron emission tomography provocation study. Neurosci. Lett. 297, 101–104. doi: 10.1016/S0304-3940(00)01674-8
Ferrucci, R., Brunoni, A. R., Parazzini, M., Vergari, M., Rossi, E., Fumagalli, M., et al. (2013). Modulating human procedural learning by cerebellar transcranial direct current stimulation. Cerebellum 12, 485–492. doi: 10.1007/s12311-012-0436-9
Fogel, S. M., Ray, L. B., Binnie, L., and Owen, A. M. (2015). How to become an expert: a new perspective on the role of sleep in the mastery of procedural skills. Neurobiol. Learn. Mem. 125, 236–248. doi: 10.1016/j.nlm.2015.10.004
Francati, V., Vermetten, E., and Bremner, J. D. (2007). Functional neuroimaging studies in posttraumatic stress disorder: review of current methods and findings. Depress. Anxiety 24, 202–218. doi: 10.1002/da.20208
Gandiga, P. C., Hummel, F. C., and Cohen, L. G. (2006). Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin. Neurophysiol. Off. J. Int. Fed. Clin. Neurophysiol. 117, 845–850. doi: 10.1016/j.clinph.2005.12.003
Harper, M. L., Rasolkhani-Kalhorn, T., and Drozd, J. F. (2009). On the neural basis of EMDR therapy: insights from qEEG studies. Traumatology 15, 81–95. doi: 10.1177/1534765609338498
Herkt, D., Tumani, V., Grön, G., Kammer, T., Hofmann, A., and Abler, B. (2014). Facilitating access to emotions: neural signature of EMDR stimulation. PLoS ONE 9:106350. doi: 10.1371/journal.pone.0106350
Hiroki, M. (2005). Cerebral white matter blood flow is constant during human non-rapid eye movement sleep: a positron emission tomographic study. J. Appl. Physiol. 98, 1846–1854. doi: 10.1152/japplphysiol.00653.2004
Hofle, N., Paus, T., Reutens, D., Fiset, P., Gotman, J., Evans, A. C., et al. (1997). Regional cerebral blood flow changes as a function of delta and spindle activity during slow wave sleep in humans. J. Neurosci. Off. J. Soc. Neurosci. 17, 4800–4808.
Kajimura, N., Uchiyama, M., Takayama, Y., Uchida, S., Uema, T., Kato, M., et al. (1999). Activity of midbrain reticular formation and neocortex during the progression of human non-rapid eye movement sleep. J. Neurosci. Off. J. Soc. Neurosci. 19, 10065–10073.
Kim, J. J., and Jung, M. W. (2006). Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review. Neurosci. Biobehav. Rev. 30, 188–202. doi: 10.1016/j.neubiorev.2005.06.005
Liberzon, I., and Abelson, J. L. (2016). Context processing and the neurobiology of post-traumatic stress disorder. Neuron 92, 14–30. doi: 10.1016/j.neuron.2016.09.039
Liberzon, I., and Sripada, C. S. (2008). The functional neuroanatomy of PTSD: a critical review. Prog. Brain Res. 167, 151–169. doi: 10.1016/S0079-6123(07)67011-3
Marshall, L., Helgadóttir, H., Mölle, M., and Born, J. (2006). Boosting slow oscillations during sleep potentiates memory. Nature 444, 610–613. doi: 10.1038/nature05278
Marshall, L., Mölle, M., Hallschmid, M., and Born, J. (2004). Transcranial direct current stimulation during sleep improves declarative memory. J. Neurosci. 24, 9985–9992. doi: 10.1523/JNEUROSCI.2725-04.2004
Milad, M. R., Pitman, R. K., Ellis, C. B., Gold, A. L., Shin, L. M., Lasko, N. B., et al. (2009). Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol. Psychiatry 66, 1075–1082. doi: 10.1016/j.biopsych.2009.06.026
Nicholson, A. A., Rabellino, D., Densmore, M., Frewen, P. A., Paret, C., Kluetsch, R., et al. (2017). The neurobiology of emotion regulation in posttraumatic stress disorder: amygdala downregulation via real-time fMRI neurofeedback. Hum. Brain Mapp. 38, 541–560. doi: 10.1002/hbm.23402
Osuch, E. A., Benson, B., Geraci, M., Podell, D., Herscovitch, P., McCann, U. D., et al. (2001). Regional cerebral blood flow correlated with flashback intensity in patients with posttraumatic stress disorder. Biol. Psychiatry 50, 246–253. doi: 10.1016/S0006-3223(01)01107-6
Pagani, M., Amann, B. L., Landin-Romero, R., and Carletto, S. (2017). Eye movement desentisization and reprocessing and slow wave sleep: a putative mechanism of action. Front. Psychol. 8:1935. doi: 10.3389/fpsyg.2017.01935
Pagani, M., Di Lorenzo, G., Monaco, L., Niolu, C., Siracusano, A., Verardo, A. R., et al. (2011). Pretreatment, intratreatment, and posttreatment EEG imaging of EMDR: methodology and preliminary results from a single case. J. EMDR Pract. Res. 5, 42–56. doi: 10.1891/1933-3196.5.2.42
Pagani, M., Di Lorenzo, G., Verardo, A. R., Nicolais, G., Monaco, L., Lauretti, G., et al. (2012). Neurobiological correlates of EMDR monitoring - an EEG study. PLoS ONE 7:e45753. doi: 10.1371/journal.pone.0045753
Patel, R., Spreng, R. N., Shin, L. M., and Girard, T. A. (2012). Neurocircuitry models of posttraumatic stress disorder and beyond: a meta-analysis of functional neuroimaging studies. Neurosci. Biobehav. Rev. 36, 2130–2142. doi: 10.1016/j.neubiorev.2012.06.003
Pedroso, J. L., Braga-Neto, P., Felício, A. C., Aquino, C. C., Prado, L. B., Prado, G. F., et al. (2011). Sleep disorders in cerebellar ataxias. Arq. Neuropsiquiatr. 69, 253–257. doi: 10.1590/S0004-282X2011000200021
Pissiota, A., Frans, O., Fernandez, M., von Knorring, L., Fischer, H., and Fredrikson, M. (2002). Neurofunctional correlates of posttraumatic stress disorder: a PET symptom provocation study. Eur. Arch. Psychiatry Clin. Neurosci. 252, 68–75. doi: 10.1007/s004060200014
Rasch, B., and Born, J. (2013). About sleep's role in memory. Physiol. Rev. 93, 681–766. doi: 10.1152/physrev.00032.2012
Rétey, J. V., Adam, M., Honegger, E., Khatami, R., Luhmann, U. F., Jung, H. H., et al. (2005). A functional genetic variation of adenosine deaminase affects the duration and intensity of deep sleep in humans. Proc. Natl. Acad. Sci. U.S.A. 102, 15676–15681. doi: 10.1073/pnas.0505414102
Sacchetti, B., Sacco, T., and Strata, P. (2007). Reversible inactivation of amygdala and cerebellum but not perirhinal cortex impairs reactivated fear memories. Eur. J. Neurosci. 25, 2875–2884. doi: 10.1111/j.1460-9568.2007.05508.x
Sacchetti, B., Scelfo, B., and Strata, P. (2005). The cerebellum: synaptic changes and fear conditioning. Neurosci. Rev. J. Bringing Neurobiol. Neurol. Psychiatry 11, 217–227. doi: 10.1177/1073858405276428
Saletin, J. M., van der Helm, E., and Walker, M. P. (2013). Structural brain correlates of human sleep oscillations. Neuroimage 83, 658–668. doi: 10.1016/j.neuroimage.2013.06.021
Schmahmann, J. D. (2010). The role of the cerebellum in cognition and emotion: personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychol. Rev. 20, 236–260. doi: 10.1007/s11065-010-9142-x
Shapiro, F. (1989). Eye movement desensitization: a new treatment for post-traumatic stress disorder. J. Behav. Ther. Exp. Psychiatry 20, 211–217. doi: 10.1016/0005-7916(89)90025-6
Shapiro, F. (2001). Eye Movement Desensitization and Reprocessing (EMDR): Basic Principles, Protocols, and Procedures, 2nd Edn. New York, NY: Guilford Press.
Shin, L. M., Rauch, S. L., and Pitman, R. K. (2006). Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Ann. N.Y. Acad. Sci. 1071, 67–79. doi: 10.1196/annals.1364.007
Stickgold, R. (2002). EMDR: a putative neurobiological mechanism of action. J. Clin. Psychol. 58, 61–75. doi: 10.1002/jclp.1129
Stickgold, R., and Walker, M. P. (2007). Sleep-dependent memory consolidation and reconsolidation. Sleep Med. 8, 331–343. doi: 10.1016/j.sleep.2007.03.011
Van Der Kolk, B. A. (1998). Trauma and memory. Psychiatry Clin. Neurosci. 52, S57–S69. doi: 10.1046/j.1440-1819.1998.0520s5S97.x
Van Der Kolk, B. A., Burbridge, J. A., and Suzuki, J. (1997). The psychobiology of traumatic memory. Clinical implications of neuroimaging studies. Ann. N.Y. Acad. Sci. 821, 99–113. doi: 10.1111/j.1749-6632.1997.tb48272.x
VanElzakker, M. B., Dahlgren, M. K., Davis, F. C., Dubois, S., and Shin, L. M. (2014). From Pavlov to PTSD: the extinction of conditioned fear in rodents, humans, and anxiety disorders. Neurobiol. Learn. Mem. 113, 3–18. doi: 10.1016/j.nlm.2013.11.014
Verweij, I. M., Onuki, Y., Van Someren, E. J., and Van der Werf, Y. D. (2016). Sleep to the beat: a nap favours consolidation of timing. Behav. Neurosci. 130, 298–304. doi: 10.1037/bne0000146
Wolf, U., Rapoport, M. J., and Schweizer, T. A. (2009). Evaluating the affective component of the cerebellar cognitive affective syndrome. J. Neuropsychiatry Clin. Neurosci. 21, 245–253. doi: 10.1176/jnp.2009.21.3.245
Keywords: slow wave sleep, memory, EMDR, PTSD, cerebellum
Citation: Carletto S, Borsato T and Pagani M (2017) The Role of Slow Wave Sleep in Memory Pathophysiology: Focus on Post-traumatic Stress Disorder and Eye Movement Desensitization and Reprocessing. Front. Psychol. 8:2050. doi: 10.3389/fpsyg.2017.02050
Received: 07 September 2017; Accepted: 10 November 2017;
Published: 22 November 2017.
Edited by:
Rossella Guerini, Università degli Studi Roma Tre, ItalyReviewed by:
Michael Hase, Lüneburger Zentrum für Stressmedizin, GermanyCaroline L. Horton, Bishop Grosseteste University, United Kingdom
Copyright © 2017 Carletto, Borsato and Pagani. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Sara Carletto, sara.carletto@unito.it