Abstract
Schizophrenia is a disorder characterized by a variety of symptoms, which among others include hallucinations, delusions and passivity experiences. It has been found that individuals with schizophrenia misattribute their own thoughts and actions to an outside agency (source monitoring deficits), which could account for psychotic experiences such as that of hearing voices. In order to explain the source-monitoring deficits as well as psychosis, it has been proposed that mechanisms that enable anticipation and recognition of sensory consequences of one’s own actions are impaired in schizophrenia. Importantly, such mechanisms may require accurate cortical sensory representations such as in the primary somatosensory cortex (S1). The establishment and maintenance of cortical sensory representations has been found to utilize a sleep-related brain rhythm known as spindling. Namely, in the perinatal period in humans and animals, and possibly also thereafter, spontaneous activity in the sensory periphery drives spindle activity in the developing cortical sensory areas, which then contributes to the formation of sensory representations that match bodily features. For example, muscle twitch-spindle sequences during sleep facilitate the formation and maintenance of S1 in accordance with the layout of musculature. This process has been proposed to continue throughout the lifespan and may be particularly important during periods of bodily changes (adolescence, menopause). In schizophrenia, the amount of sleep spindle activity is markedly reduced, which would be expected to result in insufficient cortical sensory representations and have relevance for the relative inability of individuals with schizophrenia to accurately recognize self-initiated actions.
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References
American Psychiatric Association, Diagnostic and statistical manual of mental disorders, 4th ed. text revision, American Psychiatric Association, 2000
Arad M., Weiner I., Disruption of latent inhibition induced by ovariectomy can be reversed by estradiol and clozapine as well as by co-administration of haloperidol with estradiol but not by haloperidol alone, Psychopharmacology, 2009, 206, 731–740
Oades R. D., Schepker R., Serum gonadal steroid hormones in young schizophrenic patients, Psychoneuroendocrinology, 1994, 19, 373–385
Cohen R. Z., Seeman M. V., Gotowiec A., Kopala L., Earlier puberty as a predictor of later onset of schizophrenia in women, Am. J. Psychiatry, 1999, 156, 1059–1064
Cohen B. M., Yurgelun-Todd D., Alterations of thalamic activity in schizophrenia and in response to antipsychotic drugs, Neuropsychopharmacology, 2001, 25, 305–312
Feinberg I., Corollary discharge, hallucinations and dreaming, Schizophr. Bull., 2011, 37, 1–3
Guller Y., Ferrarelli F., Shackman A.J., Sarasso S., Peterson M. J., Langheim F. J., et al., Probing thalamic integrity in schizophrenia using concurrent transcranial magnetic stimulation and functional magnetic resonance imaging, Arch. Gen. Psychiatry, 69, 662–671
Vukadinovic Z., Sleep abnormalities in schizophrenia may suggest impaired trans-thalamic cortico-cortical communication: towards a dynamic model of the illness, Eur. J. Neurosci., 2011, 34, 1031–1039
Vukadinovic Z., Rosenzweig I., Abnormalities in thalamic neurophysiology in schizophrenia: could psychosis be a result of potassium channel dysfunction?, Neurosci. Biobehav. Rev., 2012, 36, 960–968
Vukadinovic Z., Similarities between cortical “up” states during slow wave sleep and wakefulness: the implications for schizophrenia, Transl. Neurosci., 2012, 3, 51–55
Steriade M., Grouping of brain rhythms in corticothalamic systems, Neuroscience, 2006, 137, 1087–1106
Sherman S. M., Guillery R. W., Exploring the thalamus and its role in cortical function, 2nd ed., MIT Press, Cambridge, MA, 2006
Sherman S. M., Guillery R. W., Distinct functions for direct and transthalamic corticocortical connections, J. Neurophysiol., 2011, 106, 1068–1077
Yang J. W., An S., Sun J. J., Reyes-Puerta V., Kindler J., Berger T., et al., Thalamic network oscillations synchronize ontogenic columns in the newborn rat barrel cortex, Cereb. Cortex, in press, doi: 10.1093/cercor/bhs103
Khazipov R., Sirota A., Leinekugel X., Holmes G. L., Ben-Ari Y., Buzsáki G., Early motor activity drives spindle bursts in the developing somatosensory cortex, Nature, 2004, 432, 758–761
Milh M., Kaminska A., Huon C., Lapillonne A., Ben-Ari Y., Khazipov R., Rapid cortical oscillations and early motor activity in premature human neonate, Cereb. Cortex, 2007, 17, 1582–1594
Huffaker S. J., Chan J., Nicodemus K. K., Sambataro F., Yang F., Mattay V., et al., Primate-specific, brain isoform of KCNH2 affects cortical physiology, cognition, neuronal repolarization and risk of schizophrenia, Nat. Med., 2009, 15, 509–518
Arseneault L., Cannon M., Witton J., Murray R. M., Causal association between cannabis and psychosis: examination of the evidence, Br. J. Psychiatry, 2004, 184, 110–117
Semple D. M., McIntosh A. M., Lawrie S. M., Cannabis as a risk factor for psychosis: systematic review, J. Psychopharmacol., 2005, 19, 187–194
Byne W., Hazlett E. A., Buchsbaum M. S., Kemether E., The thalamus and schizophrenia: current status of research. Acta Neuropathol., 2009, 117, 347–368
Fuster J. M., The prefrontal cortex, 4th ed., Elsevier, 2008
Guillery R. W., Sherman S. M., Branched thalamic afferents: what are the messages that they relay to the cortex? Brain Res. Rev., 2011, 66, 205–219
Buzsáki G., Rhythms of the brain, Oxford University Press, New York, 2006
Frith C. D., Blackemore S. J., Wolpert D. M., Explaining the symptoms of schizophrenia: abnormalities in the awareness of action, Brain Res. Rev., 2000, 31, 357–363
Schneider K., Klinische Psychopathologie, Georg Thieme Verlag, 1950
Kumari V., Fannon D., Ffytuche D. H., Raveenrdran V., Antonova E., Premkumar P., et al., Functional MRI of verbal self-monitoring in schizophrenia: performance and illness-specific effects, Schizophr. Bull., 2010, 36, 740–755
Anselmetti S., Cavallaro R., Bechi M., Angelone S. M., Ermoli E., Cocchi F., et al., Psychopathological and neuropsychological correlates of source monitoring impairment in schizophrenia, Psychiatry Res., 2007, 150, 51–59
Brebion G., Amador X., David A., Malaspina D., Sharif Z., Gorman J. M., Positive symptomatology and source-monitoring failure in schizophrenia-an analysis of symptom-specific effects, Psychiatry Res., 2000, 95, 119–131
Ford J. M., Mathalon D. H., Whitfield S., Faustman W. O., Roth W. T., Reduced communication between frontal and temporal lobes during talking in schizophrenia, Biol. Psychiatry, 2002, 52, 485–492
Ford J. M., Gray M., Faustman W. O., Roach B. J., Mathalon D. H., Dissecting corollary discharge dysfunction in schizophrenia, Psychophysiology, 2007, 44, 522–529
Franck N., Farrer C., Georgieff N., Marie-Cardine M., Dalery J., d’Amato T., et al., Defective recognition of one’s own actions in schizophrenic patients, Am. J. Psych., 2001, 158, 454–459
Johns L. C., Rossell S., Frith C., Agmad F., Hemsley D., Kuipers E., et al., Verbal self-monitoring and auditory verbal hallucinations in patients with schizophrenia, Psychol. Med., 2001, 31, 705–715
Keefe R. S., Arnold M. C., Bayen U. K., Harvey P. D., Source-monitoring deficits in patients with schizophrenia: a multinomial modeling analysis, Psychol. Med., 1999, 29, 903–914
Keefe R. S., Arnold M. C., Bayen U. K., McEvoy J. P., Wilson W. H., Source monitoring deficits for self-generated stimuli in schizophrenia: multinomial modeling of data from three sources, Schizophr. Res., 2002, 57, 51–67
Woodward T. S., Weinstein S., Cairo T. A., Metzak P., Ngan E. T. C., Kumar D., Hallucinations are associated with aberrant activation in inner speech regions during source monitoring, Schizophr. Res., 2008, 102,Suppl. 2, 96
Tausk V., On the origin of the “influencing machine” in schizophrenia, Psychoanal. Quart., 1933, 2, 519–556
Ferrarelli F., Huber R., Peterson M. J., Massimini M., Murphy M., Riedner B. A., et al., Reduced sleep spindle activity in schizophrenia patients, Am. J. Psych., 2007, 164, 483–492
Destexhe A., Hughes S. W., Rudolph M., Crunelli V., Are corticothalamic ‘up’ states fragments of wakefulness?, Trends Neurosci., 2007, 30, 334–342
Ferrarelli F., Peterson M. J., Sarasso S., Riedner B. A., Murphy M. J., Benca R. M., et al., Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles, Am. J. Psych., 2010, 167, 1339–1348
Seeck-Hirschner M., Baier P. C., Sever S., Buschbacher A., Aldenhoff J. B., Göder R., Effects of daytime naps on procedural and declarative memory in patients with schizophrenia, J. Psychiatr. Res., 2009, 44, 42–47
Manoach D. S., Thakkar K. N., Stroynowski E., Ely A., McKinley S. K., Wamsley E., et al., Reduced overnight consolidation of procedural learning in chronic medicated schizophrenia is related to specific sleep stages, J. Psychiatr. Res., 2010, 44, 122–120
Wamsley E. J., Tucker M. A., Schinn A. K., Ono K. E., McKinley S. K., Ely A. V., et al., Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation?, Biol. Psychiatry, 2012, 71, 154–161
Ferrarelli F., Tononi G., The thalamic reticular nucleus and schizophrenia, Schizophr. Bull., 2011, 37, 306–315
Keshavan M. S., Reynolds C. F. 3rd, Miewald M. J., Montrose D. M., Sweeney J. A., Vasko R. C. Jr., et al., Delta sleep deficits in schizophrenia: evidence from automated analyses of sleep data, Arch. Gen. Psychiatry, 1998, 55, 443–448
Buzsáki G., The thalamic clock: emergent network properties, Neuroscience, 1991, 41, 351–364
Mölle M., Marshall L., Gais S., Born J., Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep, J. Neurosci., 2002, 22, 10941–10947
Steriade M., Neuronal substrates of sleep and epilepsy, Cambridge University Press, 2003
Bazhenov M., Timofeev I., Steriade M., Sejnowski T., Spiking-bursting activity in the thalamic reticular nucleus initiates sequences of spindle oscillations in thalamic networks, J. Neurophysiol., 2000, 84, 1076–1087
Swadlow H. A., Gusev A. G., The impact of’ bursting’ thalamic impulses at a neocortical synapse, Nat. Neurosci., 2001, 4, 402–408
Kim U., Sanchez-Vives M. V., McCormick D. A., Functional dynamics of GABAergic inhibition in the thalamus, Science, 1997, 278, 130–134
Owen M. J., O’Donovan M. C., Thapar A., Craddock N., Neurodevelopmental hypothesis of schizophrenia, Br. J. Psychiatry, 2011, 198, 173–175
Parnas J., Bovet P., Zahavi D., Schizophrenic autism: clinical phenomenology and pathogenic implications, World Psychiatry, 2002, 1, 131–136
Laumonnier F., Roger S., Guerin P., Molinari F., M’Rad R., Cahard D., et. al., Association of a functional deficit of the BKCa channel, a synaptic regulator of neuronal excitability, with autism and mental retardation, Am. J. Psychiatry, 2006, 163, 1622–1629
Limoges E., Mottron L., Bolduc C., Berthiaume C., Godbout R., Atypical sleep architecture and the autism phenotype, Brain, 2005, 128, 1049–1061
Khazipov R., Luhmann H. J., Early patterns of elecrtical activity in the developing cerebral cortex of humans and rodents, Trends Neurosci., 2006, 29, 414–418
Minlebaev M., Ben-Ari Y., Khazipov R., Network mechanisms of spindle-burst oscillations in the neonatal rat barrel cortex in vivo, J. Neurophysiol., 2007, 97, 692–700
Mohns E. J., Blumberg M. S., Neocortical activation of the hippocampus during sleep in infant rats, J. Neurosci., 2010, 30, 3438–3449
Hanganu I. L., Ben-Ari Y., Khazipov R., Retinal waves trigger spindle bursts in the neonatal rat visual cortex, J. Neurosci., 2006, 26, 6728–6736
Colonnese M. T., Kaminska A., Minlebaev M., Milh M., Bloem B., Lescure S., et al., A conserved switch in sensory processing prepares developing neocortex for vision, Neuron, 2010, 67, 480–498
Tritsch N. X., Bergles D. E., Developmental regulation of spontaneous activity in the mammalian cochlea, J. Neurosci., 2010, 30, 1539–1550
Halasz P., Terzano M., Parrino L., Bodizs R., The nature of arousal in sleep, J. Sleep Res., 2004, 13, 1–23
Pinault D., Dysfunctional thalamus-related networks in schizophrenia, Schizophr. Bull., 2011, 37, 238–243
Sato Y., Fukuoka Y., Minamitani H., Honda K., Sensory stimulation triggers spindles during sleep stage 2, Sleep, 2007, 30, 511–518
Andrillon T., Nir Y., Staba R. J., Ferrarelli F., Cirelli C., Tononi G., Sleep spindles in humans: insights from intracranial EEG and unit recordings, J. Neurosci., 2011, 31, 17821–17834
Pivik R. T., Joncas S., Busby K. A., Sleep spindles and arousal: the effects of age and sensory stimulation, Sleep Res. Online, 1999, 2, 89–100
Marcell A. V., Adolescence, In: Kliegman R. M., Behrman R. E., Jenson H. B., Stanton B. F. (eds.), Nelson textbook of pediatrics, 18th ed., Saunders Elsevier, Philadelphia, PA, 2007
Cohrs S., Sleep disturbances in patients with schizophrenia: impact and effect of antipsychotics, CNS Drugs, 2008, 22, 939–962
Benson K. L., Sleep in schizophrenia, Sleep Med. Clin., 2008, 3, 251–260
Monti J. M., Monti D., Sleep in schizophrenia patients and the effects of antipsychotic drugs, Sleep Med. Rev., 2004, 8, 133–148
Shepard P. D., Canavier C. C., Levitan E. S., Ether-a-go-go-related gene potassium channels: what’s all the buzz about?, Schizophr. Bull., 2007, 33, 1263–1269
Papa M., Boscea F., Canitano A., Castaldo P., Selletti S., Annunziato L., et al., Expression pattern of the ether-a-gogo-related (ERG) K+ channel-encoding genes ERG1, ERG2, and ERG3 in the adult rat central nervous system, J. Comp. Neurol., 2003, 466, 119–135
Saganich M. J., Machado E., Rudy B., Differential expression of genes encoding subthreshold-operating voltage-gated K+ channels in brain, J. Neurosci., 2001, 21, 4609–4624
Welch K.A., Stanfield A.C., McIntosh A.M., Whalley H.C., Job D.E., Moorhead T.W., Impact of cannabis use on thalamic volume in people at familial high risk of schizophrenia, Br. J. Psychiatry, 2011, 199, 386–390
Di Forti M., Henquet C., Verdoux H., Murray R. M., van Os J., Which cannabis users develop psychosis? In: Castle D., Murray R. M., D’souza D. C. (eds), Marijuana and madness, Cambridge University Press, Cambridge, UK, 2012
Snutch T. P., David L. S., T-type calcium channels: an emerging therapeutic target for the treatment of pain, Drug Develop. Res., 2006, 67, 404–415
Ross H. R., Napier I., Connor M., Inhibition of recombinant human T-type calcium channels by delta 9-tetrahydrocannabinol and cannabidiol, J. Biol. Chem., 2008, 283, 16124–16134
Spinoza, B., The ethics, treatise on the emendation of the intellect, and selected letters, 2nd ed., Hackett, Indianapolis, IN, 1991
Freud S., The standard edition of the complete psychological works of Sigmund Freud, Hogarth Press, London, 1953–74
Christensen M. S., Lundbye-Jensen J., Geertsen S. S., Peterson T. H., Paulson O. B., Nielsen J. B., Premotor cortex modulates somatosensory cortex during voluntary movements without proprioceptive feedback, Nat. Neurosci., 2007, 10, 417–419
Buzsáki G., Petit mal epilepsy and parkinsonian tremor: hypothesis of a common pacemaker, Neuroscience, 1990, 36, 1–14
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Vukadinovic, Z. Schizophrenia as a disturbance of cortical sensory maps. Translat.Neurosci. 3, 388–398 (2012). https://doi.org/10.2478/s13380-012-0043-8
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DOI: https://doi.org/10.2478/s13380-012-0043-8