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Full download Mindfulness intervention for mild cognitive impairment led to attention-related improvements and neuroplastic changes: Results from a 9-month randomized control trial Junhong Yu file pdf all chapter on 2024
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Journal of Psychiatric Research 135 (2021) 203–211
A R T I C L E I N F O A B S T R A C T
Keywords: Mindfulness-based interventions can enhance cognitive abilities among older adults, thereby effectively delaying
Mindfulness cognitive decline. These cognitive enhancements are theorized to accompany neuroplastic changes in the brain.
Meditation However, this mindfulness-associated neuroplasticity has yet to be documented adequately. A randomized
RCT
controlled trial was carried out among participants with mild cognitive impairment (MCI) to examine the effects
Cognitive enhancement
Attention
of a mindfulness-based intervention on various cognitive outcomes and cortical thickness (CT) in the context of
Cortical thickness age-related cognitive impairment. Participants were assigned to a mindfulness awareness program (MAP)(n =
Neuroplasticity 27) and an active control condition — health education program (n = 27). In both, they attended weekly sessions
Mild cognitive impairment for three months and subsequently, monthly sessions for six months. Cognitive assessments and structural scans
were carried out across three time-points. Whole brain analyses on CT were carried out and were supplemented
with region of interest-based analyses. ROI values and cognitive outcomes were analyzed with mixed MANOVAs
and followed up with univariate ANOVAs. Nine-month MAP-associated gains in working memory span and
divided attention, along with an increased CT in the right frontal pole and decreased CT in the left anterior
cingulate were observed. Three-month MAP-associated CT increase was observed in the left inferior temporal
gyrus but did not sustain thereafter. MAP led to significant cognitive gains and various CT changes. Most of these
neurobehavioral changes, may require sustained effort across nine months, albeit at a reduced intensity. MAP can
remediate certain cognitive impairments and engender neuroplastic effects even among those with MCI.
* Corresponding author. Department of Psychological Medicine Yong Loo Lin School of Medicine, National University of Singapore MD1 Research Dry Laboratories
(North), #12-01, 12 Science Drive 2, 117549, Singapore.
** Corresponding author. Senior Consultant and Associate Professor, Department of Psychological Medicine, Yong Loo Lin School of Medicine, National University
of Singapore, NUHS Tower Block, Level 9, 1E Kent Ridge Road, 119228, Singapore.
E-mail addresses: pcmyj@nus.edu.sg (J. Yu), pcmrathi@nus.edu.sg (R. Mahendran).
https://doi.org/10.1016/j.jpsychires.2021.01.032
Received 21 February 2020; Received in revised form 23 December 2020; Accepted 16 January 2021
Available online 21 January 2021
0022-3956/© 2021 Elsevier Ltd. All rights reserved.
J. Yu et al. Journal of Psychiatric Research 135 (2021) 203–211
Fig. 1. Consort flow diagram. MCI = mild cognitive impairment; MRI = magnetic resonance imaging; MAP = Mindfulness Awareness Program; HEP = Health
Education Program; AX = assessment.
healthy aging and dementia, in which researchers are optimistic that a distracting object (attention switching) and redirects attention to
interventions would alter the course of subsequent cognitive decline another stimulus (selective attention)(Lutz et al., 2008). During open
(Petersen et al., 2014). monitoring, the meditator attends to the moment-by-moment experi
Among the non-pharmacological interventions that have been car ence in the ‘here and now’ in a nonjudgmental manner. In doing so,
ried out on the MCI population, there has been a growing interest in he/she has to inhibit automatic cognitive appraisals and divert attention
mindfulness-based interventions (Chan et al., 2019). Although such in away from distracting stimuli that would obscure attention to the
terventions traditionally target psychoaffective or behavioral issues moment-by-moment experience (Jha et al., 2019). Essentially, medita
(Baer, 2003), evidence suggests that they can bring about a strong tion can be thought of as a type of cognitive training for these different
cognitive enhancement effect (Chiesa et al., 2011) as well— which can cognitive abilities.
be exploited to delay subsequent cognitive decline. This is due to the fact Alongside these training-related improvements, repeated sessions of
that meditation recruits several cognitive processes, which are trained meditation may also trigger experience-dependent neuroplastic
upon repeated sessions. changes. In this regard, one randomized controlled trial (RCT) assigned
Mindfulness meditation generally involves focused attention and/or healthy participants (i.e., self-reported to be psychologically and phys
open monitoring. In focused attention, the meditator has to direct and ically healthy, and not taking any medications) to a nine-session
sustain attention on an internal or external stimulus for a period of time. Mindfulness-Based Stress Reduction (MBSR n = 16) intervention or a
In doing so, the meditator needs to constantly monitor his/her thoughts wait-list control condition (n = 17) and compared the gray matter (GM)
to detect mind wandering. Occasionally, the meditator disengages from changes between both groups. It was observed that the GM volumes in
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J. Yu et al. Journal of Psychiatric Research 135 (2021) 203–211
Table 3
Results of the mixed ANOVA on cognitive outcomes from baseline to ninth month.
Cognitive outcome Time Group Time * Group
F p F p F p q η2partial
Digit span forward 3.50 0.069 0.01 0.914 8.01 0.007 0.060 0.18
Digit span backward 0.61 0.438 0.90 0.348 1.85 0.182 0.484 0.05
Immediate recall 7.00 0.012 3.65 0.064 0.40 0.533 0.849 0.01
Delayed recall 10.48 0.003 3.87 0.057 0.09 0.770 0.849 <.01
Recognition <.01 0.960 2.72 0.107 0.04 0.849 0.849 <.01
CTT - interference 1.58 0.217 3.03 0.091 5.03 0.031 0.126 0.13
Block design 11.17 0.002 2.27 0.140 0.28 0.600 0.849 <.01
Semantic fluency 0.91 0.348 0.47 0.495 0.12 0.732 0.849 <.01
Note. CTT = Color trails test; q = p values adjusted for false discovery rate.
2.3. Measures were used to estimate spatial normalization deformation fields using the
high dimensional Diffeomorphic Anatomic Registration Through Expo
Eight cognitive outcomes, indexing working memory span and nentiated Lie Algebra (DARTEL) warping algorithm (Ashburner, 2007)
manipulation, divided attention, immediate, delayed and recognition which were applied to segmented images and subsequently modulated.
memory, verbal fluency and visuospatial processing from various tests These modulated images were then visually inspected.
were administered (see Table 2). The procedures for these tests are Estimation of CT and the central surface was carried out using the
described in detail in the supplementary materials. For these measures, projection-based thickness method (Dahnke et al., 2013), which con
higher scores correspond to better performance, with the exception of sisted of topology correction (Yotter et al., 2011), spherical mapping,
the CTT interference, in which smaller interference scores relate to and spherical registration (Yotter et al., 2011). After obtaining the
better performance. segmented images, WM distance was estimated and the local maxima
were projected to other GM voxels using a neighbor relationship
2.4. Intervention protocol described by the WM distance (Dahnke et al., 2013). The ‘surface
thickness and thickness estimation for ROI’ writing option was used to
The MAP was modeled on similar group-based mindfulness medita extract region-of-interest (ROI) values from the Desikan-Killiany atlas
tion for older adults (McBee, 2008) and was led by an experienced (Desikan et al., 2006).
instructor. Participants were taught 1) mindfulness of the senses
practice— to attend to the different senses (i.e., vision, hearing, touch) 2.7. Statistical analyses
to cultivate focused attention; 2) body scan practice— to develop kin
esthesia by focusing their attention on various parts of their body as a We were primarily interested in the treatment gains at the two
relaxation technique, while in a sitting and/or supine position; 3) possible ‘exit points’ —third and ninth month, hence for the following
walking meditation practice— to cultivate calmness and momentary analyses we compared the outcomes between baseline and third month,
concentration by walking slowly with mindfulness; 4) ‘movement nature as well as between baseline and ninth month timepoints.
meant’ practice— to move with awareness for flexibility, strength and First, we carried out whole brain analysis on the preprocessed sur
confidence; and 5) visuomotor limb tasks that train one’s mind-body faced images. Two subjects (one from each treatment group) were
coordination. excluded from these analyses due to significant lesions. Then, treatment
The weekly HEP didactic sessions were taught by an experienced effects were assessed using a flexible factorial GLM, modeling the three
instructor, and covered topics such as chronic medical conditions (e.g., factors of Subject, Group and Time, in which we examined the T con
hypertension, diabetes, arthritis), medication compliance, and healthy trasts for the Group * Time interaction (i.e., Timepost > Timepre & MAP
lifestyles (e.g., diet, nutrition, exercise, and relaxation). In the subse > HEP and Timepost > Timepre & MAP < HEP). The results were
quent monthly discussion sessions, participants shared how they had thresholded using p < 0.05, family-wise error (FWE) correction against a
applied what they learned to their daily lives. Both programs were null-distribution generated by 5000 nonparametric permutations using
separately carried out in a quiet room in a community location. the TFCE toolbox, with a cluster extent threshold of k > 20. Significant
clusters are labeled using the Desikan-Killiany atlas.
2.5. MRI acquisition Given the relatively small number of scanned participants, a whole
brain analysis was unlikely to yield multiple clusters that would survive
Participants were scanned in a 3-T Siemens Tim Trio scanner at the the stringent FWE corrections. Hence, we supplemented the whole brain
Clinical Imaging Research Center, Singapore. T1-weighted images were analyses with ROI-based analyses. Specifically, we selected on an a
acquired using an MPRAGE protocol (TE = 1.90s; TR = 2.30s; TI = 900 priori basis, ROIs that corresponded to the significant cortical GM
ms; 256 × 256 matrix; 192 sagittal slices; in-plane resolution = 1 mm; clusters identified in a meta-analysis that compared between experi
slice thickness = 1 mm). enced meditators and meditation naïve controls (Fox et al., 2014). These
included the bilateral regions of the anterior cingulate cortex (ACC),
2.6. Image preprocessing orbitofrontal cortex (OFC), frontal pole (FP) and insula. Apart from the
first two, these ROIs were extracted as they were parcellated in the atlas.
T1-weighted images were preprocessed longitudinally using the The ACC ROI was created by summing the caudal and rostral anterior
CAT12 (version r1450) as implemented in SPM12 (version 6225) within cingulate ROIs, and the OFC ROI was created by summing the lateral and
MATLAB (R2019a). Baseline and follow-up images were rigidly real medial orbitofrontal ROIs. These ROIs were entered into subsequent
igned within-subject to correct for differences in head position and a analyses together with the cognitive outcomes.
subject-specific average template was computed and used as reference in For the analyses of the cognitive outcomes and CT ROIs, in order to
a subsequent realignment of the baseline and follow-up images. The minimize the false positive results associated with multiple testing,
realigned images were segmented into GM, white matter (WM) and multivariate analyses of variance (MANOVA) were carried out sepa
cerebrospinal fluid, as well as corrected for signal inhomogeneities with rately on the cognitive outcomes and CT ROIs, with time and group as
reference to the subject average template. These GM and WM images the within- and between-subject factors, respectively, to determine the
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J. Yu et al. Journal of Psychiatric Research 135 (2021) 203–211
Fig. 2. Trajectories of cognitive outcomes in each group across time. The thick colored lines represent the mean trajectory of each group, which are enclosed within
their respective 95% confidence intervals. *p < .05; **p < .01.
overall effect on the assessed outcomes. In line with our general on participants with valid data on all three timepoints, such analyses
analytical framework, the MANOVAs compared between baseline and would discard several participants with incomplete ninth month data,
third month, as well as between baseline and ninth month timepoints. If ultimately reducing statistical power. Effect sizes for the significant
significant group*time interaction effects were obtained in any of these statistics relating to the time * group interactions were quantified using
MANOVAs, post hoc univariate analyses of variance (ANOVA) were partial eta square (η2partial), where η2partial of 0.06 and 0.13 indicates
carried out individually on each outcome between the respective time medium and large effect sizes, respectively. Statistical significance was
points. Although it is possible to analyze all three timepoints in a single set at p < .05. For the post-hoc ANOVAs, we have additionally computed
MANOVA and proceed with post hoc analyses, we did not do so. This is p-values adjusted for false discovery rate (FDR). Nevertheless, we do not
because the valid sample size at the ninth month timepoint is much expect the significant results of these ANOVAs to survive such correc
smaller, given that the three-timepoint MANOVA can only be carried out tions, as this would require very large treatment effects and sample sizes
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J. Yu et al. Journal of Psychiatric Research 135 (2021) 203–211
Table 4
Results of the mixed ANOVA on the regions-of-interest from baseline to ninth month.
Regions-of-interest Time Group Time * Group
F p F p F p q η2partial
Anterior cingulate L 0.20 0.658 0.13 0.718 5.18 0.035 0.138 0.21
Anterior cingulate R 0.01 0.924 0.01 0.913 0.01 0.921 0.921 <.01
Orbitofrontal L 0.52 0.479 0.02 0.898 0.04 0.848 0.921 <.01
Orbitofrontal R 0.91 0.351 0.11 0.747 0.80 0.381 0.844 0.04
Frontal pole L 0.92 0.349 0.68 0.419 0.03 0.855 0.921 <.01
Frontal pole R 0.15 0.704 0.01 0.936 5.18 0.035 0.138 0.21
Insula L 1.63 0.217 0.08 0.784 0.16 0.695 0.921 <.01
Insula R 3.44 0.079 0.22 0.647 0.67 0.422 0.844 0.03
that are beyond what is expected or practical for this study. These an extracting the significant cluster as an ROI and entering these ROI values
alyses were carried out R 4.0.2. The R code for executing these analyses into a mixed ANOVA. The Time * Group effect across the entire 9-month
and generating the figures are available at https://osf.io/ykz2c/files/. intervention period was not significant (F(1, 36) = 0.21; p = .649;
η2partial = 0.01 see Fig. 4b), in contrast to the significant interaction across
3. Results the first three months (F(1, 19) = 23.27; p < .001; η2partial = 0.39).
The MANOVAs revealed a significant Time * Group effect on The current study examined the effects of a mindfulness-based
cognitive outcomes between the baseline and ninth month (F(8, 28) = intervention on cognitive outcomes and CT. In the cognitive domain,
1.92; p = .022; η2partial = 0.44),but not between baseline and third month we observed a gradual improvement in working memory span and
(F(8, 39) = 1.92; p = .106; η2partial = 0.27). Thus, univariate ANOVAs divided attention among MAP participants relative to their HEP coun
were carried out to follow up on the significant effects between the terparts, culminating in medium to large effect sizes across the entire 9-
baseline and ninth month. The detailed results of all modeled effects in month intervention period. As for CT, MAP participants, relative to their
these ANOVAs are presented in Table 3. In these post hoc analyses, HEP counterparts had significantly increased CT, as quantified by a large
significant Time*Group interactions emerged for digit span forward and effect size, in the right FP across the entire 9-month intervention period.
CTT interference. Fig. 2 showed that the digit span forward score and At the end of the first 3-month phase, the CT in MAP participants had
CTT interference among MAP participants had increased and decreased, significantly increased in a left ITG cluster, as quantified by a large effect
respectively over time, relative to their HEP counterparts. As expected, size, relative to HEP participants. However, these 3-month MAP-
none of these significant post-hoc results survived the FDR correction. associated CT changes in the left ITG did not sustain until the ninth
month. Overall, these results suggest that the MAP intervention led to
3.2. Effect of MAP on cortical thickness significant cognitive gains and neuroplastic changes across the 9-month
intervention period.
The MANOVAs on the CT revealed a significant Time * Group effect With repeated sessions of meditation, our MAP participants trained
between baseline and ninth month (F(8, 12) = 3.03; p = .041; η2partial = their abilities to engage and disengage their attention on various stimuli.
0.67), but not between baseline and third month (F(8, 29) = 2.01; p = Naturally, the effect of such attentional training would transfer to our
.080; η2partial = 0.36). Univariate ANOVAs were carried out to follow up measure of divided attention, where participants had to repeatedly
on the significant effects between baseline and ninth month. The engage and disengage between two sets of stimuli (i.e., pink and yellow
detailed results of all modeled effects in these ANOVAs are presented in circles in the CTT). Furthermore, we observed MAP-associated working
Table 4.These ANOVAs revealed a significant Time * Group on the right memory improvements as measured by the digit span forward. Gener
FP (F(1, 19) = 5.19; p = .035; η2partial = 0.21) and left ACC (F(1, 19) = ally, working memory span benefits from an improved attention. A
5.18; p = .035; η2partial = 0.21). Fig. 3 showed that, relative to HEP larger working memory span can be the result of a greater ability to
participants, the CT in the right FP and left ACC among MAP participants control attention to avoid distraction and thereby maintain more stored
had increased and decreased, respectively, across this period. None of items (Engle, 2002). Such controlled attention was practiced in our MAP
these significant post-hoc results survived the FDR correction. Addi as participants focused and sustained their attention on various external
tionally, none of the CT changes in any ROIs were significantly corre and interoceptive stimuli. However, we did not observe a similar
lated with any of the changes in cognitive outcomes. The descriptive MAP-associated improvement for working memory manipulation as
statistics of the ROI CT values across the three time-points are reported measured by the digit span backward. Although meditation typically
in the supplementary materials (see table S2). involves the manipulation information in the working memory, such
Next, CT was analyzed at the whole brain level. Across the first three manipulation is largely restricted to the engagement and disengagement
months, whole brain analyses within the contrast of Time3-month > of information in the present moment without judgment or elaboration
Timebaseline & MAP > HEP revealed a significant cluster in the left (Jha et al., 2019). Arguably, this involves a relatively low cognitive load.
inferior temporal gyrus (ITG)(k = 28, peak level FWE-corrected p = Our measure of working memory manipulation requires elaborate pro
.009; MNI = − 55, − 33, − 24; see Fig. 4a). No significant clusters cessing of information— to reverse the order of the digits while holding
emerged in the reverse contrast (i.e., Time3-month > Timebaseline & MAP these digits in the working memory. Essentially, for the digit span
< HEP). Across the entire 9-month intervention period, no significant backward, working memory is being tested while being weighed down
clusters were observed in any of the interaction contrasts. The uncor by an additional cognitive load. This is not something our MAP partic
rected statistical maps of these contrasts are presented in the supple ipants would have had more practice with than their HEP counterparts.
mentary materials (see figures S1 and S2). Given these results, there is a In terms of MAP-associated neuroplasticity, we observed some CT
possibility that the significant cluster obtained from the first 3-month changes which are consistent with previous findings. First, there was a
period did not appear in the subsequent 6-month period, merely due significant MAP-associated increase in the CT of the left ITG (at least
to the reduced sample size. Hence, we investigated this further by within the first three months) and right FP. A meta-analysis (Fox et al.,
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J. Yu et al. Journal of Psychiatric Research 135 (2021) 203–211
Fig. 3. Trajectories of cortical thickness values in each group across time. The thick colored lines represent the mean trajectory of each group, which are enclosed
within their respective 95% confidence intervals. *p < .05.
2014) that compared between experienced meditators and medi meditation. As our intervention transitioned from weekly to monthly
tation-naïve controls had observed similar clusters of GM volume in sessions, it was observed that the increased CT in the left ITG, were no
crease in the right frontopolar cortex (including the FP) and left ITG. longer sustained at the ninth month. Perhaps, this suggests that the
Relatedly, task-based functional MRI studies have shown that activa monthly meditation sessions were not adequate to maintain such gains.
tions in the frontopolar cortex (Molenberghs et al., 2016) and the left It is plausible that if our intervention had continued its weekly sessions,
ITG (Hasenkamp et al., 2012) were linked to meditation-associated greater neuroplastic changes and perhaps cognitive gains would be
meta-cognitive processes, such as meta-cognitive judgments and observed. Indeed, a meta-analysis on mind-body exercises observed that
awareness of mind wandering. Given this, the MAP-associated CT in interventions with more frequent sessions were more likely to result in
creases in these regions could speculatively be linked to the enhanced greater cognitive gains than those of less frequent sessions (Chan et al.,
meta-cognitive abilities typically brought about via repeated sessions of 2019).
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J. Yu et al. Journal of Psychiatric Research 135 (2021) 203–211
Fig. 4. a) Significant cluster (FWE-corrected p < 0.05) in left inferior temporal gyrus within the contrast of Time3-month > Timebaseline & MAP > HEP. b) trajectories
of cortical thickness values of extracted cluster in each group across time. The thick colored lines represent the mean trajectory of each group, which are enclosed
within their respective 95% confidence intervals. ***p < .001.
In contrast to previous cross-sectional studies that found increased discomforts in order to retain as many MRI-eligible participants as
ACC GM volume among experienced meditators (Fox et al., 2014), we possible, especially among the older adult population.
observed a MAP-associated CT decrease in the ACC. Notwithstanding,
the problems of comparing the current intervention results to CRediT authorship contribution statement
cross-sectional findings, this decrease in ACC CT or volume should not
always be viewed negatively, especially since the ACC is involved in Junhong Yu: Writing - original draft, Formal analysis, Software,
several functions. One such function includes emotional processing Visualization. Iris Rawtaer: Writing - original draft. Lei Feng: Writing -
(García-Cabezas and Barbas, 2016). In relation to this, a lesion study review & editing. Johnson Fam: Writing - review & editing. Alan Prem
(Tolomeo et al., 2016) suggests that the removal of the anterior cingu Kumar: Formal analysis, Writing - review & editing. Irwin Kee-Mun
late may be therapeutic for patients with intractable mood, anxiety and Cheah: Writing - review & editing. William G. Honer: Writing - re
pain syndromes, specifically in terms of reducing negative affect. view & editing. Wayne Su: Software, Formal analysis, Writing - review
Relatedly, we speculate that the reduced ACC CT among MAP partici & editing. Yuan Kun Lee: Writing - review & editing. Ene Choo Tan:
pants may reflect the neuroplastic changes corresponding to the Writing - review & editing. Ee Heok Kua: Writing - review & editing,
MAP-associated attenuations in emotional reactivity to negative affect Funding acquisition. Rathi Mahendran: Writing - review & editing,
(Britton et al., 2012). Funding acquisition, Project administration, Supervision.
These findings present important implications in the clinical context.
We have shown that a relatively low intensity (i.e., weekly or monthly
Declaration of competing interest
sessions) non-pharmacological intervention can result in significant
cognitive gains and neuroplastic changes in the context of age-related
None.
cognitive impairment. In essence, our intervention would be instru
mental in delaying further cognitive decline or even enhancing one’s
functional status, without the side-effects of medications (Smith, 2016) Acknowledgement
or exhaustion associated with intensive cognitive training (Vranic,
2017). Additionally, the MAP-associated cognitive gains were mostly We acknowledge the contributions of the following: the Late Mr Wee
observed within the domains of executive-attention. This would suggest Sin Tho for developing and structuring the Mindfulness Program for this
that such mindfulness-based interventions would be more appropriate study and Dr Goh Lee Gan for developing and delivering the Health
for older adults with executive-attentional impairments, such as those Education Talks
with nonamnestic MCI or at risk for frontotemporal dementia, than
those with amnestic MCI or at risk for Alzheimer’s disease. It should also Appendix A. Supplementary data
be noted that while the targeted cognitive gains are most relevant to this
group of older adults, their executive functions deficits may bring about Supplementary data to this article can be found online at https://doi.
some difficulties during meditation, especially when they are required to org/10.1016/j.jpsychires.2021.01.032.
sustain and focus their attention for a period of time.
The current study is subjected to a few limitations. First, this was an Financial support
open-label study, in which both participants and the experimenters were
aware of which treatment group the former was assigned to. There is a This work was supported by Research Donations from Kwan Im
small possibility that the results may be confounded by observer- Thong Hood Cho Temple and Lee Kim Tah Holdings Pte Ltd under the
expectancy effects among experimenters and the differences in partici Mind Science Center, Department of Psychological Medicine, National
pants’ treatment expectancies between both groups. Second, the attri University of Singapore.
tion rate for MRI data was quite significant; by the ninth month, the
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Along the shore of the sounding sea they went, making prayer to
Zeus that he would grant them success in what they sought.
When they came to the ships and huts of Achilles they found him
sitting with a lyre in his hand. Of beautiful workmanship it was, with a
silver cross-bar upon it, and as the hands of Achilles drew from it
wondrous melody, he sang of the glorious deeds of the heroes of
old.
Beside him sat Patroclus, listening silently to the song of the
friend that he loved.
Then did Odysseus step forward, and Achilles, amazed, sprang
to his feet, his lyre in his hand, and Patroclus also arose.
‘Welcome ye are,’ said Achilles; ‘truly ye are friends that are
come. Even in my anger are ye the dearest of all the Greeks to me.’
Then he led them forward and made them sit on seats covered
with lordly purple.
To Patroclus he said:
‘Bring forth the biggest bowl and the finest of my wines, for I have
no dearer friends than those who are here with me now.’
So did Achilles have a rich feast of precious wines and of dainties
of all sorts made ready for those who brought him the message of
Agamemnon the king.
And when the feast was ended, Odysseus did tell him of the dire
woes of the Greeks and of the royal gifts of Agamemnon, and of the
pleadings of the Greeks and of their overlord, that their hero,
Achilles, would come and fight for them once again.
Then did Achilles make answer:
‘Hateful to me as are the gates of death, O great Odysseus, is
the man who hideth in his heart one thing and sayeth another. So will
I speak to thee as seemeth me best. Hard have I laboured, fiercely
have I fought for Agamemnon, yet what is my gain after it all?
Hateful to me are the gifts of Agamemnon. Wealth and power can be
mine without aid from him, yet know I well, for my mother, Thetis the
silver-footed, hath told me, that death swiftly draweth nigh. Let the
Greeks seek help elsewhere, for fierce is my anger, and no help
shall ye gain from me.’
Then said Ajax:
‘Let us go hence, Odysseus. Our embassy is vain. Yet evil though
the news we carry with speed must we bear it back to the Greek
host. Merciless art thou, Achilles! Anger hath made thee set at
naught thy comrades’ love and the love of thine own dear land.’
And to Ajax did Achilles make answer:
‘Take ye, then, my message, brave Ajax! Tell Agamemnon that
until the day that the men of Troy come even to my ships and my
huts and smirch them with fire, no finger will I raise for Greece. But
on that day, then, surely, will the power of the Trojans be stayed.’
Then did Odysseus and Ajax and the others return in sorrow to
the host of the Greeks, and gave to them the message of Achilles.
In silence did the warriors listen.
Then said Diomedes:
‘Achilles, then, must bide his time. When his heart is aroused
again within him, he will fight. But let us now take meat and drink and
sleep, and when rosy-fingered Dawn doth come, strength shall be
ours for the battle, and with courage shall we fight for the cause of
Agamemnon our king!’
CHAPTER IX
THE WHITE HORSES OF RHESUS
Sound was the sleep of the Greek chiefs that night, but Agamemnon
the king slept not. From his enemies’ camp came the sound of pipe
and flute and laughter of men, as the Trojans feasted and made
merry in the red light of their camp-fires. As he looked seawards at
the ships of the sleeping Greeks, his heart was heavy within him and
he groaned aloud.
On his feet he bound his sandals, over his shoulders did he throw
his great mantle of a tawny lion’s skin, and, grasping his spear, he
went forth into the night to take counsel of wise Nestor.
Neither to Menelaus came there sleep, for his heart was full of
fear lest harm should come to the Greeks who had crossed the wide
seas to fight for his sake in Troyland.
Agamemnon heard the sound of pipe and flute and laughter of men as
the Trojans feasted and made merry (page 86)
The night passed, and grey dawn saw a mighty fight begin.
Fiercely did the battle wax and wane, and valiant deeds were
done that day.
Mightily fought Agamemnon, but against him fought the gods,
and when the sun blazed forth at noon, he and many another Greek
warrior, grievously wounded, were forced to leave the field.
An arrow, from the bow of Paris, smote Machaon, skilled
physician of the Greeks, and fear seized them lest he who healed
their wounds might himself perish.
Into his chariot did old Nestor take Machaon, and right willingly
his horses galloped back to their stables by the shore.
By the stern of his ship stood Achilles, watching the battle from
afar, and his dear friend and comrade, Patroclus, he sent speeding
to the tent of Nestor for tidings of the battle and to ask the name of
the wounded warrior.
Scornfully spake Nestor:
‘What matters it to Achilles which of the sons of Greece lie
wounded? Many chiefs of the Greeks have shed their blood this day,
yet Achilles heedeth not. Hast thou forgotten, Patroclus, that day
when thy father didst speak to thee of thyself and of Achilles? “Of
nobler birth than thou is Achilles,” he said, “and in might much
greater. Yet he is younger than thou, so see that thou counsel him
gently and wisely when there is need, and he will obey thee.” Even
now, Patroclus, thou mightest persuade Achilles to go forth to battle.
But if he will not go, then let him lend thee his armour so that the
men of Troy may flee before thee, thinking that Achilles goeth forth to
war once more.’
So did Nestor rouse the heart of Patroclus, and swiftly Patroclus
returned to the ship of Achilles.
Fiercer and ever more fierce grew the battle as the hours went
by. Up to the walls that the Greeks had built did the Trojans press
their furious way. Up the battlements, spear in hand, they swarmed,
nor heeded the storm of stones that crashed down upon them from
above.
In front of the gates lay a stone so huge that two strong men
could not together have lifted it and placed it on a wagon. With one
hand did mighty Hector, legs wide apart, hurl it against the great
double gates. Before it, hinges burst, bars smashed, and the gates
crashed backwards. Then in leapt Hector, his eyes flashing fire.
None but the gods could have withstood him, and on his heels came
the men of Troy. Before them they swept the Greek host to their
ships.
But down by the sea fought Ajax, and round him the Greeks took
their stand. Mighty was the wall of living men that sought to die for
their honour and for their own dear land.
Yet, like a great rock that the fierce floods of winter tear from a
mountain-side, and that crashes through the forests and thunders
down the valleys, destroying as it goes, so did Hector press onward.
Behind him in heaps lay the slain, the moans of the dying mingled
with the din of battle, and the dark night of death blinded the eyes of
many a mighty chief.
‘Thinkest thou to spoil our ships!’ called Ajax to Hector. ‘To the
gods, and not to the men of Troy do we owe our evil plight. Yet ere
long will Troy fall before us, and thou thyself wilt pray to Zeus to
make thy steeds fleet as falcons as they bear thee in shameful plight
back to thy city, across the plain.’
To Ajax did Hector make answer:
‘Blundering boaster art thou! Woe cometh this day to the Greeks!
And thou, Ajax, if thou hast courage to meet my spear, shalt be food
for the birds and the dogs.’
In his tent the heart of Agamemnon sank within him, and those
beside him did he counsel that they should drag their ships down to
the sea and swiftly sail away.
‘There is no shame in fleeing from ruin,’ said he.
But Odysseus and Diomedes replied with angry scorn to the
coward words of their overlord.
‘Let us go down to the battle, wounded though we be,’ said
Diomedes.
So they set forth, and with them went Agamemnon, and through
the long day did that mortal fight go on. Now would the Trojans
triumph, and again to the men of Greece would come the victory.
At last, before a huge stone, hurled by Ajax, did Hector fall. Like a
mighty oak smitten by lightning he fell, and the Trojans bore him
away, the black blood gushing from his mouth.
Then pressed the men of Greece the more. Back from the ships
they drove the men of Troy.
But to Hector where he lay a-dying came Apollo, and into his
fainting body and heart he breathed fresh strength and courage.
With strength as the strength of ten Hector once again faced the
foe, and before him the Greeks fell back in dismay.
Patroclus in his tent, tending the wounds of a friend, marked how
the Greeks fell back, and he groaned aloud.
‘To Achilles must I hasten,’ he said. ‘Who knows but that the time
has come when I may arouse him to join in the battle.’
CHAPTER XI
HOW PATROCLUS FOUGHT AND DIED
While round the dark ships of Greece the fierce fight raged, Achilles,
from afar, listened unmoved to the din of battle, and watched with
stony eyes the men of Greece as they fell and died on the reddened
ground.
To him came Patroclus.
‘Why dost thou weep, Patroclus?’ asked Achilles. ‘Like a fond
little maid art thou that runs by her mother’s side, plucking at her
gown, hindering her as she walks, and with tearful eyes looking up at
her until the mother lifts her in her arms. Like her, Patroclus, dost
thou softly weep.’
Then Patroclus, heavily groaning, made answer:
‘Among the ships lie the bravest and best of the men of Greece,
sore wounded or dead. Pitiless art thou, Achilles, pitiless and
unforgiving. Yet if thou dost still hold back from the battle, give me, I
pray thee, thine armour, and send me forth in thy stead. Perchance
the Trojans may take me for the mighty Achilles, and even now the
victory be ours.’
Then said Achilles, and heavy was his heart within him:
‘These Greeks took from me my well-won prize, Patroclus. Yet let
the past be past; no man may keep his anger for ever. I have said
that until the men of Troy come to burn my own ships I will hold me
back from the battle. But take you my armour; lead my men in the
fight, and drive from the ships the men of Troy. But to others leave it
to chase them across the plain.’
Even as Achilles spoke, the strength of mighty Ajax had come to
an end, and with furious rush did the Trojans board the ships. In their
hands they bore blazing torches, and up to the sky rushed the
fiercely roaring flames.
Then cried Achilles, smiting his thighs:
‘Haste thee, Patroclus! They burn the ships! Arm thyself speedily,
and I will call my men!’
Corslet and shield and helmet did Patroclus swiftly don, and
girded on the silver-studded sword and took two strong lances in his
hand.
In the chariot of Achilles he mounted, and Automedon, best and
bravest of charioteers, took the reins.
Swift as the wild west wind were Bayard and Piebald, the two
horses of Achilles, and in the side harness was Pedasus, a horse
only less swift than they.
Gladly did the men of Achilles meet his call to arms, for fierce as
wolves were they.
‘Many times hast thou blamed me,’ cried Achilles, ‘because in my
wrath I kept ye back from battle. Here for ye now is a mighty fight,
such as ye love.’
To battle they went, and while Patroclus led them forth, Achilles in
his tent offered up an offering to Zeus.
Like wasps that pour forth from their nests by the wayside to sting
the boys who have stoned them, so now did the Greeks swarm from
their ships.
Before the sword of Patroclus fell a mighty warrior, and when the
men of Troy saw the shining armour of Achilles in his own chariot
their hearts sank within them.
Out of the ships were they driven, the fire was quenched, and
back to the trench rolled the tide of battle. In the trench writhed many
a horse and many a man in dying agonies. But clear across it leaped
the horses of Achilles, and close to the walls of Troy did Patroclus
drive brave Hector before him.
His chariot then he turned, and headed off the fleeing Trojans,
driving them down to the ships. Before the furious rush of his swift
steeds, other horses were borne off their feet, other chariots cast in
ruins on the ground, and men crushed to death under his wheels.
Chief after chief did Patroclus slay. A mighty destroyer was he that
day.
One only of the chiefs of Troy kept his courage before the
destroyer who wore the shining arms of Achilles.
‘Shame on ye!’ cried Sarpedon to his men, ‘whither do ye flee? I
myself will fight this man who deals death and destruction to the
Trojan host.’
From their chariots leaped Sarpedon and Patroclus.
With the first cast of his spear Patroclus missed Sarpedon, but
slew his charioteer. Then did Sarpedon cast, and his spear whizzed
past Patroclus, and smote the good horse Pedasus. With a dreadful
scream Pedasus fell, kicking and struggling, in the dust. This way
and that did the other two horses plunge and rear, until the yoke
creaked and the reins became entangled. But the charioteer leaped
down, with his sword slashed clear the traces from Pedasus, and the
horses righted themselves.
Once again did Sarpedon cast his spear, and the point flew over
the left shoulder of Patroclus. But Patroclus missed not. Through the
heart of Sarpedon sped the fiercely hurled spear, and like a slim tree
before the axe of the woodcutter he fell, his dying hands clutching at
the bloody dust.
Furious was the combat then over the body of Sarpedon. One
brave warrior after another did Patroclus lay dead.
And more terrible still was the fight because in the ranks of the
men of Troy there fought now, in all-devouring wrath, the god Apollo.
Nine men, good warriors all, did Patroclus slay; then, waxing
bolder, he tried to climb the very walls of Troy.
Three times did Apollo thrust him back, and when, a fourth time,
he attacked, the god cried aloud to him in anger, warning him not to
dare so much.
Against Patroclus did Hector then drive his war-horses, but
Patroclus, leaping from his chariot, hurled at Hector a jagged stone.
In the eyes it smote the charioteer of Hector, and the slain man
dropped to the ground.
‘How nimble a man is this!’ jeered Patroclus. ‘How lightly he
diveth! Were this the sea, how good an oyster-seeker would this
fellow be!’
The point of the spear flew over the left shoulder of Patroclus (page 107)
Then from his chariot leaped Hector and met Patroclus, and the
noise of the battle was as the noise of a mighty gale in the forest
when great trees fall crashing to the ground.
When the sun went down, victory was with the Greeks. Three
mighty charges did Patroclus make, and each time he slew nine
men. But when, a fourth time, he charged, Apollo met him. In thick
mist he met him, and Patroclus knew not that he fought with a god.
With a fierce downstroke from behind, Apollo smote his broad
shoulders, and from off his head the helmet of Achilles fell with a
clang, rattling under the hoofs of the horses. Before the smiting of
the god, Patroclus stood stricken, stupid and amazed. Shattered in
his hands was the spear of Achilles, and his mighty shield clanged
on the ground.
Ere he could know who was the smiter, a Trojan ally drove a
spear between his shoulders, and Patroclus, sore wounded, fell
back.
Marking his dismay, Hector pressed forward, and clean through
his body drove his bronze spear. With a crash Patroclus fell.
‘Thou that didst boast that thou wouldst sack my town, here shall
vultures devour thee!’ cried Hector.
And in a faint voice Patroclus made answer:
‘Not to thee do I owe my doom, great Hector. Twenty such as
thou would I have fought and conquered, but the gods have slain
me. Yet verily I tell thee that thou thyself hast not long to live. Even
now doth Death stand beside thee!’
As he spoke, the shadow of Death fell upon Patroclus. No more
in his ears roared the din of battle; still and silent for ever he lay.
CHAPTER XII
THE ROUSING OF ACHILLES
Fierce had been the fight before Patroclus died. More fiercely yet it
raged when he lay dead.
From his body did Hector take the arms of Achilles, and the dead
Patroclus would the Trojans fain have dragged to their city, there to
bring shame to him and to all the Greek host.
But for him fought the Greeks, until the earth was wet with blood
and the very skies echoed the clang of battle.
To Achilles came Antilochos, a messenger fleet of foot.
‘Fallen is Patroclus!’ he cried, ‘and around his naked body do
they fight, for his armour is held by Hector.’
Then did Achilles moan aloud. On the ground he lay, and in his
hair he poured black ashes. And the sound of his terrible lament was
heard by his mother, Thetis, the goddess, as she sat in her palace
down under the depths of the green sea.
Up from under the waves swiftly came she to Achilles, and
tenderly did she listen while he poured forth to her the tale of the
death of his dear comrade.
Then said Thetis:
‘Not long, methinks, shall Hector glory in the armour that was
thine, for Death presseth hard upon him. Go not forth to battle, my
son, until I return, bearing with me new and fair armour for thee.’
But when Thetis had departed, to Achilles in his sorrow came Iris,
fair messenger of the gods.
‘Unto windy Ilios will the Trojans drag the body of Patroclus
unless thou comest now. Thou needst not fight, Achilles, only show
thyself to the men of Troy, for sore is the need of Patroclus thy
friend.’
Then, all unarmed, did Achilles go forth, and stood beside the
trench. With a mighty voice he shouted, and at the sound of his voice
terror fell upon the Trojans. Backward in flight they went, and from
among the dead did the Greeks draw the body of Patroclus, and hot
were the tears that Achilles shed for the friend whom he had sent
forth to battle.
The making of the arms of Achilles (page 113)
All that night, in the house of the Immortals, resounded the clang
of hammer on anvil as Hephaistus, the lame god, fashioned new
arms for Achilles.
Bronze and silver and gold he threw in his fire, and golden
handmaidens helped their master to wield the great bellows and to
send on the crucibles blasts that made the ruddy flames dance.
No fairer shield was ever borne by man than that which
Hephaistus made for Achilles. For him also he wrought a corslet
brighter than a flame of fire, and a helmet with a golden crest.
And in the morning light did Thetis dart down from snowy
Olympus, bearing in her arms the splendid gift of a god.
Glad was Achilles as he put on the armour, and terrible was his
war-cry as he roused the Greek warriors. No man, however sore his
wounds, held back when the voice of Achilles called him to the fight
once again. Wounded was Agamemnon, overlord of the Greeks, but
forth also came he. And there, while the sun rose on many a warrior
who would fight no more, did Achilles and Agamemnon speak as
friends once again, their long strife ended.
Hungry for war, with Achilles as their leader, did the Greeks then
meet the Trojans on the plain. And as a fierce fire rages through the
forest, its flames driven by the wind, so did Achilles in his wrath drive
through the host of Troy.
Down to the Scamander he drove the fleeing Trojans, and the
water reddened with blood, as he smote and spared not.
Merciless was Achilles; pitilessly did he exult as one brave man
after another was sent by him to dye red the swift flood of the
Scamander.
At length, at his lack of mercy, did even the river grow wrathful.