Skip to main content
SpringerLink
Log in

The “ways” we look at dreams: evidence from unilateral spatial neglect (with an evolutionary account of dream bizarreness)

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Despite decades of research, the question of whether the rapid eye movements (REMs) of paradoxical sleep (PS) are equivalent to waking saccades and whether their direction is congruent with visual spatial events in the dream scene is still very controversial. We gained an insight into these questions through the study of a right brain damaged patient suffering attentional neglect for the left side of space and drop of the optokinetic nystagmus (OKN) with alternating rightward slow/leftward fast phases evoked by rightward optic flow. During PS the patient had frequent Nystagmoid REMs with alternating leftward slow/rightward fast phases and reported dreams with visual events evoking corresponding OKN such as a train running leftward. By contrast, just as in waking OKN, Nystagmoid REMs with alternating rightward slow/leftward fast phases were virtually absent. REMs followed by staring eye position or by consecutive REMs were also observed: these showed no asymmetry comparable to that of Nystagmoid ones. The selective disappearance of Nystagmoid REMs in one horizontal direction proves, for the first time, that in humans different types of REMs exists and that these are driven by different premotor mechanisms. Concomitant drop of OKN and Nystagmoid REMs toward the same horizontal direction demonstrates that phylogenetically ancient oculomotor mechanisms, such as the OKN, are shared by waking and PS. On this evidence and converging findings from animal, neuropsychological and brain imaging studies, a new evolutionary account of dream bizarreness is proposed. Classification and labelling of the different types of REMs are also provided.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aboitz F, Morales D, Montiel J (2003) The evolutionary origin of the mammalian isocortex: towards an integrated developmental approach. Behav Brain Sci 26:535–586

    Article  Google Scholar 

  • Appenzeller O, Fischer AP (1968) Disturbances of rapid eye movements during sleep in patients with lesions of the nervous system. Electroenceph Clin Neurophysiol 25:29–35

    Article  PubMed  CAS  Google Scholar 

  • Aserinsky E, Lynch JA, Mack ME, Tzankoff SP, Hurn E (1985) Comparison of eye motion in wakefulness and REM sleep. Psychophysiology 22:1–10

    Article  PubMed  CAS  Google Scholar 

  • Baloh RW, Yee RD, Honrubia V (1980) Optokinetic nystagmus and parietal lobe lesions. Ann Neurol 7:269–276

    Article  PubMed  CAS  Google Scholar 

  • Barton JJS, Sharpe JA, Raymond JE (1996) Directional defects in pursuit and motion perception in humans with unilateral cerebral lesions. Brain 119:1535–1550

    Article  PubMed  Google Scholar 

  • Bischof M, Bassetti CL (2004) Total dream loss: a distinct neuropsychological dysfunction after bilateral PCA stroke. Ann Neurol 56:583–586

    Article  PubMed  Google Scholar 

  • Bisiach E, Luzzatti C (1978) Unilateral neglect of representational space. Cortex 14:129–133

    PubMed  CAS  Google Scholar 

  • Bowker RM, Morrison AR (1976) The startle reflex and PGO spikes. Brain Res 102:185–190

    Article  PubMed  CAS  Google Scholar 

  • Braun AR, Balkin TJ, Wesensten NJ, Carson RE, Varga M, Baldwin P, Selbie G, Belenky G, Herscovitch P (1997) Regional blood flow throughout the sleep-wake cycle. An H 152 O PET study. Brain 120:1173–1197

    Article  PubMed  Google Scholar 

  • Braun AR, Balkin TJ, Wesensten NJ, Gwadry F, Carson RE, Varga M, Baldwin P, Belenky E, Herscovitch P (1998) Dissociated pattern of activity in visual cortices and their projections during human rapid eye movement sleep. Science 279:91–95

    Article  PubMed  CAS  Google Scholar 

  • Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35:625–641

    Article  PubMed  CAS  Google Scholar 

  • Datta S (1997) Cellular basis of pontine ponto-geniculo-occipital wave generation and modulation. Cell Mol Neurobiol 17:341–365

    Article  PubMed  CAS  Google Scholar 

  • De Gennaro L, Ferrara M (2000) Effect of a presleep optokinetic stimulation on rapid eye movements during REM sleep. Physiol Behav 69:471–475

    Article  PubMed  Google Scholar 

  • Dement WC (1964) Eye movements during sleep. In: Bender MB (ed) The oculomotor system. Hoeber, New York, pp 366–416

    Google Scholar 

  • Dement WC, Kleitman N (1957) The relationship of eye movements during sleep to dream activity. An objective method for the study of dreaming. J Exp Psychol 53:339–346

    Article  PubMed  CAS  Google Scholar 

  • Doricchi F, Tomaiuolo F (2003) The anatomy of neglect without hemianopia: a key role for parietal–frontal disconnection? NeuroReport 14:2239–2243

    Article  PubMed  Google Scholar 

  • Doricchi F, Violani C (1992) Dream recall in brain damaged patients: an introduction to the neuropsychology of dreaming through a review of the literature. In: Antrobus J, Bertini M (eds) The neuropsychology of sleep and dreaming. Lawrence Erlbaum Associates, Hillsdale, pp 99–140

    Google Scholar 

  • Doricchi F, Guariglia C, Paolucci S, Pizzamiglio L (1993) Disturbances of the rapid eye movements (REMs) of the REM sleep in patients with unilateral attentional neglect: clue for the understanding of the functional meaning of REMs. Electroenceph Clin Neurophysiol 87:105–116

    Article  PubMed  CAS  Google Scholar 

  • Doricchi F, Guariglia C, Paolucci S, Pizzamiglio L (1996) REMs asymmetry in chronic unilateral neglect does not change with behavioral improvement induced by rehabilitation treatment. Electroenceph Clin Neurophysiol 98:51–58

    Article  PubMed  CAS  Google Scholar 

  • Doricchi F, Siegler I, Iaria G, Berthoz A (2002) Vestibulo-ocular and optokinetic impairments in left unilateral neglect. Neuropsychologia 40:2084–2099

    Article  PubMed  Google Scholar 

  • Eisensehr I, Noachtar S, Strupp M, v Lindeiner H, Brandt T, Buttner U (2001) Absence of nystagmus during REM sleep in patients with vestibular neuritis. J Neurol Neurosurg Psychiatr 71:386–389

    Article  PubMed  CAS  Google Scholar 

  • Freud S (1990) The interpretation of dreams. Basic Books, New York

    Google Scholar 

  • Fuchs A, Ron S (1968) An analysis of rapid eye movements of sleep in the monkey. Electroenceph Clin Neurophysiol 25:244–251

    Article  PubMed  CAS  Google Scholar 

  • Gabersek V, Scherrer J (1969) L’analyse des mouvements oculaires pendant la phase paradoxale du sommeil. J Physiologie 61:294

    Google Scholar 

  • Gordon CR, Oksenberg A (1993) Spontaneous nystagmus across the sleep-wake cycle in vegetative state patients. Electroencephal Clin Neurophysiol 86:132–137

    Article  CAS  Google Scholar 

  • Herman JH, Barker DR, Roffwarg H (1983) Similarity of eye movements characteristics in REM sleep and the awake state. Psychophysiology 20:537–543

    Article  PubMed  CAS  Google Scholar 

  • Herman JH, Herman M, Boys R, Perser L, Taylor M, Roffwarg H (1984) Evidence for a directional correspondence between eye movements and dream imagery in REM sleep. Sleep 7:52–63

    PubMed  CAS  Google Scholar 

  • Hobson JA (1988) The dreaming brain. Basic Books, New York

    Google Scholar 

  • Hobson JA, McCarley RW (1977) The brain as a dream state generator: an activation-synthesis hypothesis of the dream process. Am J Psychiatr 134:1335–1348

    PubMed  CAS  Google Scholar 

  • Hong CCH, Potkin SG, Antrobus JS, Dow BM, Callaghan GM, Gillin JC (1997) Rem sleep eye movements counts correlate with visual imagery in dreaming: a pilot study. Psychophysiology 34:377–381

    Article  PubMed  CAS  Google Scholar 

  • Hornak J (1992) Ocular exploration in the dark by patients with visual neglect. Neuropsychologia 30:547–552

    Article  PubMed  CAS  Google Scholar 

  • Ilg UJ (1997) Slow eye movements. Prog Neurobiol 53:293–329

    Article  PubMed  CAS  Google Scholar 

  • Incoccia C, Doricchi F, Galati G, Pizzamiglio L (1995) Amplitude and speed change of the optokinetic response in patients with and without neglect. Neuroreport 6:2137–2140

    Article  PubMed  CAS  Google Scholar 

  • Jacobs L, Feldman M, Bender MB (1972) Are the eye movements of dreaming sleep related to the visual images of the dreams? Psychophysiology 9:393–401

    Article  PubMed  CAS  Google Scholar 

  • Jeannerod M, Mouret J (1962) Etude des mouvements oculaires observè chez l’Homme au cours de la veille et du sommeil. C R Seances Soc Biol Fil (Paris) 156:1407–1410

    Google Scholar 

  • Kawahara R, Hazama H, Fukuhara T (1980) Nystagmus and REM density during sleep in patients with brainstem lesions. Waking Sleeping 4:205–210

    PubMed  CAS  Google Scholar 

  • King WM, Zhou W (2000) New ideas about binocular coordination of eye movements: is there a chamaleon in the primate family tree? Anatom Rec 261:153–161

    Article  CAS  Google Scholar 

  • Louie K, Wilson MA (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29:145–156

    Article  PubMed  CAS  Google Scholar 

  • Maquet P, Peters JM, Aerts J, Delfiore G, Degueldre C, Luxen A, Franck G (1996) Functional neuroanatomy of human rapid eye movement sleep and dreaming. Nature 383:163–166

    Article  PubMed  CAS  Google Scholar 

  • Nofzinger EA, Mintun MA, Wiseman M, Kupfer DJ, Moore RY (1997) Forebrain activation in REM sleep: an FDG PET study. Brain Res 770:192–201

    Article  PubMed  CAS  Google Scholar 

  • Pace-Schott EF, Hobson J (2002) The neurobiology of sleep: genetics, cellular physiology and subcortical networks. Nat Rev Neurosci 3:591–605

    PubMed  CAS  Google Scholar 

  • Pavlides C, Winson J (1989) Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci 9:2907–2918

    PubMed  CAS  Google Scholar 

  • Peigneux P, Laureys S, Fuchs S, Delbeuck X, Degueldre C, Aerts J, Delfiore G, Luxen A, Maquet P (2001) Generation of rapid eye movements during paradoxical sleep in humans. Neuroimage 14:701–708

    Article  PubMed  CAS  Google Scholar 

  • Perenin MT, Maeda T, Jeannerod M (1972) Are vestibular nuclei responsible for rapid eye movements of paradoxical sleep. Brain Res 43:617–621

    Article  PubMed  CAS  Google Scholar 

  • Pizzamiglio L, Frasca R, Guariglia C, Incoccia C, Antonucci G (1990). Effect of optokinetic stimulation in patients with visuospatial neglect. Cortex 26:535–540

    PubMed  CAS  Google Scholar 

  • Porte HS, Hobson A (1996) Physical motion in dreams: one measure of three theories. J Abnorm Psychol 105:329–335

    Article  PubMed  CAS  Google Scholar 

  • Rafal R, Henik A, Smith J (1991). Extrageniculate contributions to reflex visual orienting in normal humans: a temporal hemifield advantage. J Cogn Neurosci 3:323–328

    Article  Google Scholar 

  • Rechtschaffen A, Kales AE (1968) A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. Government Printing Office, Washington DC

    Google Scholar 

  • Reding GR, Fernandez C (1968) Effects of vestibular stimulation during sleep. Electroenceph Clin Neurophysiol 24:75–79

    Article  PubMed  CAS  Google Scholar 

  • Robinson DA, Zee DS (1981) Theoretical considerations on the function and circuitry of various rapid eye movements. In: Fuchs AF, Becker W (eds) Progress in oculomotor research. Elsevier/North-Holland, New York, pp 3–9

    Google Scholar 

  • Salzarulo P, Pecheux MG, Lairy GC (1973) A vecto-oculographic approach to fast sleep eye movements in man. Electroenceph Clin Neurophysiol 34:539–542

    Article  PubMed  CAS  Google Scholar 

  • Schneider D (1978) Spatio-temporal properties of rapid eye movements in human rem sleep. Waking Sleeping 2:63–67

    Google Scholar 

  • Schwartz S (2003) Are life episodes replayed during dreaming? Trends Cogn Sci 7:325–327

    Article  PubMed  Google Scholar 

  • Schwartz S, Maquet P (2002) Sleep imaging and the neuropsychological assessment of dreams. Trends Cogn Sci 6:23–30

    Article  PubMed  Google Scholar 

  • Siegel JM (2005) Clues to the functions of mammalian sleep. Nature 437:1264–1271

    Article  PubMed  CAS  Google Scholar 

  • Soh K, Morita Y, Sei H (1992) Relationship between eye movements and oneiric behavior in cats. Physiol Behav 52:553–558

    Article  PubMed  CAS  Google Scholar 

  • Solms M (1997) The neuropsychology of dreams. Erlbaum, New Jersey

    Google Scholar 

  • Solms M, Turnbull O (2002) The brain and the inner world. Other Press, New York

    Google Scholar 

  • Tauber ES, Weitzman ED, Herman J (1973) Absence of nystagmus during REM sleep in a patient with waking nystagmus and oscillopsia. J Neurol Neurosurg Psychiatr 36:833–888

    Article  PubMed  CAS  Google Scholar 

  • Thiebaut de Schotten M, Urbanski M, Duffau H, Volle E, Lévy R, Dubois B, Bartolomeo P (2005) Direct evidence for a parietal–frontal pathway subserving spatial awareness in humans. Science 309:2226–2228

    Article  CAS  Google Scholar 

  • Vanni-Mercier G, Pelisson D, Goffart L, Sakay K, Jouvet M (1994) Eye saccades dynamics during paradoxical sleep in the cat. Eur J Neurosci 6:1298–1306

    Article  PubMed  CAS  Google Scholar 

  • Vertes RP (1984) Brainstem control of the events of REM sleep. Prog Neurobiol 22:241–288

    Article  PubMed  CAS  Google Scholar 

  • Zhou W, King WM (1997) Binocular eye movements not coordinated during REM sleep. Exp Brain Res 117:153–160

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Fabrizio Doricchi wishes to dedicate the manuscript to the loving memory of Patrizia Sirianni Doricchi, Renato Grasso, Greta Schmidt Scola, Caterina Laicardi and Renato Fabietti. Support by Andrea Doricchi and Domenica Bueti was precious. We thank many colleagues and the referees for suggestions and Hugo Bowles for text revision. U. Cellini, P. Fermani and D. Moretti provided skilful technical assistance. This study was supported by grants from the “Fondazione Santa Lucia” and from the “Ministero della Universita’ e della Ricerca Scientifica”.

Author information

Authors and Affiliations

  1. LENA (Laboratoire Europeen des Neurosciences de l’Action), Centro Ricerche di Neuropsicologia Fondazione Santa Lucia, Fondazione Santa Lucia IRCCS, Via Ardeatina 306, Rome, 00179, Italy

    Fabrizio Doricchi, Giuseppe Iaria, Massimo Silvetti & Francesca Figliozzi

  2. Dipartimento di Psicologia, Università degli Studi di Roma “La Sapienza”, 39, Via dei Marsi 78, Rome, 00185, Italy

    Fabrizio Doricchi, Giuseppe Iaria, Massimo Silvetti & Francesca Figliozzi

  3. Centre de Recherches en Sciences du Sport, Université Paris-Sud 11, Paris, France

    Isabelle Siegler

Authors
  1. Fabrizio Doricchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Giuseppe Iaria
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Massimo Silvetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francesca Figliozzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Isabelle Siegler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fabrizio Doricchi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Doricchi, F., Iaria, G., Silvetti, M. et al. The “ways” we look at dreams: evidence from unilateral spatial neglect (with an evolutionary account of dream bizarreness). Exp Brain Res 178, 450–461 (2007). https://doi.org/10.1007/s00221-006-0750-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-006-0750-x

Keywords

Search

Navigation