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Dreaming with hippocampal damage

  1. Goffredina Spanò
  2. Gloria Pizzamiglio
  3. Cornelia McCormick
  4. Ian A Clark
  5. Sara De Felice
  6. Thomas D Miller
  7. Jamie O Edgin
  8. Clive R Rosenthal
  9. Eleanor A Maguire  Is a corresponding author
  1. Wellcome Centre for Human Neuroimaging, UCL Queen Square Institute of Neurology, University College London, United Kingdom
  2. Department of Neurodegenerative Diseases and Geriatric Psychiatry, University Hospital Bonn, Germany
  3. Department of Neurology, Royal Free Hospital, United Kingdom
  4. Department of Psychology, University of Arizona, United States
  5. Nuffield Department of Clinical Neurosciences, University of Oxford, United Kingdom
Short Report
Cite this article as: eLife 2020;9:e56211 doi: 10.7554/eLife.56211
2 figures, 2 tables and 3 additional files

Figures

Experimental set-up and key findings.

(A) Two researchers were located in Room one which was adjacent to Room two where the participant slept. The participant was woken up at various times during their night’s sleep to report their thoughts in that moment. PSG recordings informed the decisions about when to awaken the participant to ensure sampling during non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. We used a Bluetooth intercom system equipped with a camera for continuous visual monitoring and communication with the participant. (B) The number of total awakenings was not different between the patients (HPC) and control (CTL) participants. (C) There were also no significant group differences in the proportion of awakenings from NREM and REM sleep. (D) In contrast, the patients reported significantly fewer dreams than the control participants, expressed here as the total number of dreams divided by the total number of awakenings (+ / - 1 SEM; p=0.028). (E) The few dreams the patients had were significantly less rich in content compared to those of the control participants (n = 3 patients, as one patient had no dreams at all and was not included in this analysis; + / - 1 SEM; p=0.018). For other measures see Table 2.

Example dream reports.

Experimenter probing is shown in italics. HPC1−4 = the four hippocampal-damaged patients; CTL = an example control participant.

Tables

Table 1
Demographic characteristics.
GroupAge
(years)
Chronicity
(years)
LHPC volume (mm3)RHPC volume (mm3)LHPC % volume loss relative to CTLaRHPC % volume loss relative to CTLaWASI
CTL59.20 (15.89)n.a.3173.18a (338.89)3285.91a (300.81)n.a.n.a.14.50 (2.37)
HPC161625062803−21.03%−14.70%12
HPC272817361698−45.29%−48.32%10
HPC3721126072755−17.84%−16.16%12
HPC4281128192804−11.16%−14.67%14
  1. All patients (HPC1-4) and control participants (CTL) were right-handed males. Mean and standard deviation in parentheses are shown for control participants and individual data for the four patients. aThe control group consisted of eleven participants (mean age 55.64 years ± 16.47). LHPC = left hippocampus; RHPC = right hippocampus; n.a. = not applicable; WASI = Wechsler Abbreviated Scale of Intelligence (Wechsler, 1999) Matrix Reasoning subtest scaled score. See Supplementary file 1 and Supplementary file 2 for additional neuropsychological and sleep quality data of the participants.

Table 2
Dream characteristics.
HPCCTLHPC1HPC2HPC3HPC4
M (SD)M (SD)UESP-Value
General analysesa
Number of awakenings6.75 (2.75)6.90 (1.97)18.50.110.82910.004.005.008.00
Proportion of awakenings during NREM0.73 (0.09)0.67 (0.13)14.00.470.3830.800.750.600.75
Proportion of awakenings during REM0.23 (0.17)0.33 (0.13)13.00.550.3090.00c0.250.400.25
Number of probes per awakening3.82 (1.75)4.22 (1.13)17.00.230.6715.803.501.604.38
Dream frequency0.23 (0.17)0.67 (0.28)4.51.450.0280.400.250.000.25
Proportion of dreams during NREM0.38 (0.48)0.52 (0.20)14.50.430.4151.000.000.000.50
Proportion of dreams during REM0.38 (0.48)0.48 (0.20)16.00.310.5550.001.000.000.50
Proportion of no dreams0.65 (0.31)0.21 (0.24)4.01.520.0220.600.751.000.25
Proportion of blank dreams0.13 (0.25)0.12 (0.15)15.50.350.4960.000.000.000.50
Overall qualitative attributesb
Number of informative words43.17 (16.06)95.55 (55.20)7.00.810.17655.5025.00.49.00
Complexity2.67 (0.58)3.32 (0.70)5.51.000.0983.002.00.3.00
Vividness3.10 (0.79)3.88 (1.08)7.50.750.2032.804.00.2.50
Bizarreness1.58 (1.01)2.27 (0.95)8.00.700.2322.751.00.1.00
Emotional valence2.75 (0.25)2.81 (0.22)13.00.190.7202.753.00.2.50
Proportion of self-references0.84 (0.29)0.90 (0.19)15.00.001.0001.001.00.0.50
Content characterizationb
Internal (episodic) details4.08 (1.47)9.13 (3.56)2.01.540.0285.753.00.3.50
External (semantic/other) details0.17 (0.29)1.07 (1.60)8.50.640.2580.000.00.0.50
Content score5.75 (0.90)13.10 (6.49)1.01.740.0186.755.00.5.50
  1. M = mean; SD = standard deviation; ES = effect size; HPC = hippocampal-damaged patients; CTL = control participants; NREM = non-rapid eye movement sleep; REM = rapid eye movement sleep; HPC1−4 = each individual hippocampal-damaged patient. P-values relate to between-group non-parametric Mann-Whitney U tests with significant differences depicted in bold. aAll patients included; means are per awakening. bHCP3, who had no dream reports at all, was excluded; means are per dream report. cFor HCP1, during 20% of his awakenings towards the end of the night, the EEG cap stopped functioning and so designation to NREM or REM sleep was not possible. Hence, it could be that this zero score for REM awakenings is an underestimate, given that REM is more common in the latter part of the night. Note that his dream reports from these awakenings were still included in the dream qualitative attributes and content analyses. See Table 2—source data 1 file for the data underpinning this table.

Table 2—source data 1

This file contains the individual participant data for every dream-related measure that is summarised in Table 2.

https://cdn.elifesciences.org/articles/56211/elife-56211-table2-data1-v1.xlsx

Additional files

Supplementary file 1

Summary of neuropsychological information.

This table provides details of the neuropsychological profile (summary data and statistical analyses) of the patients across a range of cognitive tests, and indicates the selective nature of their memory loss.

https://cdn.elifesciences.org/articles/56211/elife-56211-supp1-v1.docx
Supplementary file 2

Sleep quality of the patients and control participants.

This table provides details (summary data and statistical analyses) of subjective measures of the general quality and pattern of sleep, as well as on objective measures of sleep-related breathing disorders, and sleep-wake patterns across one week. There were no significant differences between the patient and control participants on any measure.

https://cdn.elifesciences.org/articles/56211/elife-56211-supp2-v1.docx
Transparent reporting form
https://cdn.elifesciences.org/articles/56211/elife-56211-transrepform-v1.docx

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