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Effects of Visual Stimulation with Bonsai Trees on Adult Male Patients with Spinal Cord Injury

International Journal of

Environmental Research

and Public Health

Article

Effects of Visual Stimulation with Bonsai Trees on

Adult Male Patients with Spinal Cord Injury

Hiroko Ochiai 1,† ID , Chorong Song 2,† ID , Harumi Ikei 2,3,† ID , Michiko Imai 4 and

Yoshifumi Miyazaki 2,* ID

1 Department of Plastic and Reconstructive Surgery, National Hospital Organization Tokyo Medical Center,

Higashigaoka 2-5-1, Meguro-ku, Tokyo 152-8902, Japan; ochiroko@gmail.com

2 Center for Environment, Health and Field Sciences, Chiba University, 6-2-1 Kashiwa-no-ha, Kashiwa,

Chiba 277-0882, Japan; crsong1028@chiba-u.jp (C.S.); ikei0224@ffpri.affrc.go.jp (H.I.)

3 Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan

4 Le Verseau Inc., 3-19-4 Miyasaka, Setagaya-ku, Tokyo 156-0051, Japan; leverseau@mvb.biglobe.ne.jp

* Correspondence: ymiyazaki@faculty.chiba-u.jp; Tel.: +81-4-7137-8113

† These authors contributed equally to this work.

Received: 10 August 2017; Accepted: 1 September 2017; Published: 5 September 2017

Abstract: Nature therapy has been demonstrated to induce physiological relaxation. The psychophysiological

effects of nature therapy (stimulation with bonsai trees) on adult male patients with spinal cord injury

(SCI) were examined. Oxyhemoglobin concentration changes in the prefrontal cortex were measured

using near-infrared spectroscopy, and heart rate variability was analyzed. Psychological responses

were evaluated using the modiﬁed semantic differential method and Proﬁle of Mood States (POMS)

subscale scores. Visual stimulation of adult male patients with SCI elicited signiﬁcantly decreased

left prefrontal cortex activity, increased parasympathetic nervous activity, decreased sympathetic

nervous activity, increased positive feelings, and resulted in lower negative POMS subscale scores.

Nature therapy can lead to a state of physiological and psychological relaxation in patients with SCI.

Keywords: spinal cord injury; nature therapy; bonsai trees; visual stimulation; near-infrared

spectroscopy; heart rate variability

1. Introduction

Stress appears to be increasingly present in our modern and demanding industrialized society.

Every aspect of our bodies and brains can be virtually inﬂuenced by stress induced by living in an

urban environment [1]. Early human civilizations lived in natural settings, demonstrating that we

can adapt to nature. Congruent with this viewpoint, individuals living in modern societies who

are experiencing stress have become interested in several types of natural therapy [2]. For example,

psychological evaluations of the effects of horticultural therapy on the elderly have been previously

reported [3,4].

The progress and development of research involving nature and forest medicine has advanced

in recent years with the development of medical equipment related to the natural and life sciences.

For example, oxyhemoglobin (oxy-Hb) concentrations in the prefrontal cortex were measured using

a portable near-infrared spectroscopy (NIRS) device, which revealed that foliage plants can have

physiological relaxation effects in male participants [5]. Heart rate variability (HRV) was measured,

which revealed that visual stimulation with roses increased parasympathetic nervous activity [6] and

that fresh pansies decreased sympathetic nervous activity [7]. Furthermore, salivary cortisol levels were

measured after the participants were subjected to gardening activity, which demonstrated decreased

stress levels [8]. A review by Song et al. presented scientiﬁc data to elucidate the physiological

relaxation effects of nature therapy on the activities of the central nervous system, autonomic nervous

Int. J. Environ. Res. Public Health 2017, 14, 1017; doi:10.3390/ijerph14091017

www.mdpi.com/journal/ijerph

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system, endocrine system, and immune system [9]. The results from these experiments are based on

advances in various physiological indicators from the viewpoint of evidence-based medicine in Japan.

Nature therapy has the potential to be more widely adopted as preventive medicine in the future.

One potential application of nature therapy is its use for patients with spinal cord injury (SCI).

SCI is a devastating event for individuals, and they frequently develop motor and sensory impairments,

as well as autonomic dysfunction. Previous studies have reported that autonomic nervous activity

plays a major role in social cognition and that difﬁculties in the ability to interpret social information

are commonly observed in a variety of mental disorders, which in turn correlate with poor autonomic

nervous system regulation [10]. Depressive disorders are the most frequent concern following SCI

and signiﬁcantly affect rehabilitation, community integration, quality of life (QOL), and health-related

outcomes [11–13]. A clinical practice guideline published in 1998 noted that 25% of men and 47% of

women with SCI experienced some form of depressive disorder [14].

Considering this high prevalence of psychological distress, it is especially important to highlight

that according to research, most patients with SCI felt that their emotional needs were not sufﬁciently

addressed by their rehabilitation team [15]. Recent meta-analyses have reported medium-to-large

effect sizes for psychological interventions for post-SCI depression, and there is sufﬁcient evidence

speciﬁcally supporting the use of cognitive behavioral therapy interventions [16]. However, these

methods require the intervention of an expert psychiatrist.

An advantage of nature therapy such as viewing bonsai trees is that it allows for routine,

self-induced mental relaxation. Such therapy is also accessible for individuals who are unable to

perform certain activities (e.g., walking more than a mile or doing vigorous activities). If the physical

and mental stress of patients with SCI can be reduced via intervention with nature therapy, this therapy

can be recommended to such patients to promote improved health. Similarly, nature therapy can be

used as a preventive medicine therapy for healthy but stressed individuals. Relaxing effects have been

reported regarding exposure to forest, urban green space, ﬂowers and plants, and so on. Nature therapy

is deﬁned as “a set of practices aimed at achieving ‘preventive medical effects’ through exposure

to natural stimuli that render a state of physiological relaxation and boost the weakened immune

functions to prevent disease” [9].

Although previous analytical studies have pointed out the relevance of nature therapy and

relaxation in healthy adults, there is no previous research on adult patients with SCI. To the best of

our knowledge, this is the ﬁrst study to examine the physiological and psychological effects of nature

therapy in adult male patients with SCI and clarify its effectiveness in reducing daily stress.

In this study, 24 Japanese adult male patients with chronic-stage SCI were exposed to 10-year-old

cypress bonsai trees as visual stimuli. Bonsai is miniature natural landscapes in pots using trees and

other plants. They are a famous art form unique to Japan.

2. Materials and Methods

2.1. Experimental Design

All participants gave their informed consent for inclusion before they participated in the study.

The study was conducted in accordance with the Declaration of Helsinki, and the protocol was

approved by the Ethics Committee of the Center for Environment, Health and Field Sciences,

Chiba University, Japan (Project identiﬁcation code number: 5). In total, 24 Japanese male patients with

spinal cord injury aged 25–79 years (mean age, 49.0 ± 16.4 years) were included in this study. They had

a height of 162–182 cm (171.4 ± 5.6 cm) and weight of 52–94 kg (67.2 ± 9.2 kg). The patients had no

psychiatric disorders, which comprised part of the inclusion criteria for the study, and they were in

the chronic stage of their condition (i.e., >1 year after the lesion developed). They were diagnosed

with spinal cord injury by a doctor and their damage was located below C7. The patients were able to

independently move around in wheelchairs.

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The experiments were conducted in an experimental room at Chiba University. The room

temperature was maintained at 23.7 ± 1.3 ◦C, and the relative humidity was maintained at 50.5 ± 7.4%.

The patients moved into the experimental room and the experiments were separately carried out for

each patient.

Miniature potted 10-year-old Japanese cypress bonsai trees were used as visual stimuli.

Eight cypress trees, approximately 55 cm in height, were grouped together in a 40 × 20 × 5 cm

ceramic pot (Figure 1A). Before visual stimulation, these miniature trees were covered by a corrugated

cardboard box (rest condition). After a 60-s rest period, the patients viewed the miniature potted

trees (visualInstt. iJ.mEnuvirloant. iRoesn. P)ubolicrHneaolthth20i1n7,g14(, 1c0o17ntrol) for 60 s each; all patients were made to e3xopf 9erience both

experimentaTlhceopnatdieinttisomnosv.edDiinstotathneceexpfreorimmentthaleropoamtiaenndttsh’eeeyxpeesrimtoentthsewetreeseespawraatesly6c0a–rr6ie3d comut .foTr he order of

conditions (ie.aec.h, vpiastiuenatl. stimulation vs. control) was randomized. The patients practiced the procedure,

Miniature potted 10‐year‐old Japanese cypress bonsai trees were used as visual stimuli. Eight

using visualcsytpirmessutlraeteiso, anppwroitxhimaatpeloy t5t5ecdmpinlahneitg,hot,nwceerebgerfoourpeehdatongdet.her in a 40 × 20 × 5 cm ceramic pot

(Figure 1A). Before visual stimulation, these miniature trees were covered by a corrugated cardboard

2.2. Physiologboicxa(lreIsntdciocnedsition). After a 60‐s rest period, the patients viewed the miniature potted trees (visual

stimulation) or nothing (control) for 60 s each; all patients were made to experience both experimental

Changecsoninditoioxnys.-HDibstacnocenfcreonmtrthaetipoantisenotsn’ etyhees tsouthrfeatcreeesowf atsh6e0–p6r3ecfmro. nThtaelocrdoerrteofxcwonedriteiomnse(ia.es.,ured using a

two-channelvinsueaal rs-tiimnufrlaatrioendvss.pceocnttrrool)swcoaspryanddeomviiczeed(. NThIeRpSa;tiPenotsckpreatctNiceIdRtSheDpruooce,dDurye,nuasSinegnvsiseu,aHl amamatsu,

Japan). NIRsStimpruolabtieons wwitehraeppolttaecdepdlanbti,loantceerbaelfloyreahnandd.symmetrically on the forehead. Two sensors were

placed over 2t.h2.ePhfryosionlotgailcarleIngdiiocens , with one sensor placed on the left side of the forehead and the other

placed on the rigChhtasnigdeseinofoxtyh‐eHbfocroenhceenatrdati(oFnisgounrtehe1sBu)rfa[1ce7o].f tThoe parnefarolyntzael ctohrteexNwIeRreSmreeasspuroendsuesi,ncghange in the

oxy-Hb concaetnwtor‐acthiaonnnselinneatrh‐ienfprarreefdrospnetcatrlocscoorptyexdedvuiceri(nNgIRvSi;sPuocaklesttNimIRuS lDautoio, DnywnaaSsenmsee, Hasaumraemda.tsTuh, e difference

between thispJalpaacanendd).oNtvhIeRerStvhpearoflruboeenstawflreorreemgipoln1a,c0ewdsitbhpiloranitoeerraseltlnyosoasnrtdpimlsaycumedlmaoetnitrotihcnaelwllyefatonssidtaheneoaffoltryheezheefoadrde..hTIewtadoisasnewdnsetohlrles eowtsheteraerblished that

oxy-Hb concpelancterdaotniothnerreigﬂhet csitdsetohf ethae cfotrievhaetaido(nFiogufrne e1Bu)r[a17l]r. eTgo iaonnalsyz[e1t8h]e.NIRS response, change in the

The patoiexyn‐tHsbplcaocnecednttrhateioirnsleifnt ftoherepﬁrnefgroenrtsaloncorttheex sdeunrisnogr voifsuaanl satcimceulleatriaontedwapslemtheaysusrmedo.gTrhaeph (ARTETT,

U-Medica Inedscift.af,ebrlOeisnhsceaedkbtaeht,awtJeoaexpnya‐tHnhbi)sc(oaFnnidcgentuhtrreaetvio1anlCuree).fflerHoctmseath1r0etasrctapivtreaiotirvontaoroifsatnibmeuiulrilaatlytrioegn(HiownRasVs[1a)8n]w.alyazseda. nItalisyzweedll . HRV was

converted by aT6he0/paat-iaentisntpelarcveadl;thtehirelesftamforpefliinngegrsfroenqtuheensecnysowr oafsa1n0a0c0celHerazte. d Tphleethypsmowogerarphlevels of the

high-frequen(AcyRT(EHTFT), U(0‐M.1e5d–ic0a.4In0c.H, Ozs)akaan, Jdaplaonw) (-Ffirgeuqreu1eCn).cHye(aLrtFr)at(e0v.0ar4ia–b0i.li1ty5(HHRzV) )cwomas panoanlyeznedts. HwReVre calculated

using the mhwaixagsihm‐cforuenqvmueertneecdnytbr(yoHapF)6y0(/m0a.‐1ae5–tinh0t.o4e0rdvaH[l;1zt)9h,ea2ns0da]m.lpoHwlinF‐fgrpefqroeuqweuneecnyrcyw(LwaF)ass(c01o.000n40–s0Hi.d1z5e. rTHehdze)ptcooowmreeprﬂolenevecentltsspowaf rtehareesympathetic

nervous acticvailtcyu,laatenddutshinegLtFhetomHaxFimruamtioenwtroapsycomnesthidoder[e1d9,2t0o]. rHeﬂFepcotwseyrmwpaas tchoentsiicdenreedrvtoo urseflaeccttivity [21,22].

In general, ppaarrassyymmpaptahetthicetniecrvnoeursvaoctuivsitayc, tainvdittyheisLFentohaHnFcreadtiodwuarsincgonrseidlearxedattioonrefalencdt ssyymmpapthaetthicetic nervous

activity

ennahneradvnsoycumes dpacatatihvteitttyihc[en2e1tr,i2vm2o]u.esInoacfgteiavnwietryaailks, peenanrhiaansnygcmeodpraattihntehteiscittinmuereavtooifuoasnwasactkoievfnitisyntgirseoesrnsihn.asnictuedatidounrsinogf

relaxation

stress.

Figure 1. Bonsai trees and physiological measurement apparatuses. (A) Japanese cypress bonsai trees;

Figure 1. Bo(Bn)saPiarttirceipeasntanudndeprhgoyinsgiolnoegari‐cinaflramredeasspuecrteromsceonpyt a(pNpIRaSr)amtuesaesusr.em(eAn)t; J(aCp)aPnaerstiecipcaynpt ress bonsai

trees; (B) Paurntdiceirpgoainngt huenardt reartegvoairniagbinliteya(Hr-RinVf)rmaeraesduresmpeenctt.roscopy (NIRS) measurement; (C) Participant

undergoing heart rate variability (HRV) measurement.

IInntt.. JJ.. EEnnvviirroonn.. RReess.. PPuubblliiccHHeeaalltthh22001177,,1144,,11001177

44oof f190

2.3. Psychological Indices

The modified semantic differential (SD) method and Profile of Mood States (POMS) subscale

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msceotrheosdwuesreesutsherdeetopeavirasluoafteadpjesyctcihvoesloagniccahlorreinspgo1n3s‐epsofionltloswcailnegs:v“icsoumalfostritmabulleattioonu.nTcohme fmorotdabiﬁlee,d”

“SrDelmaxeetdhotodauwseaskethnrieneg,p”aairnsdo“fnaadtjuercatilvteosaartnicfihcoiarli”ng[2133].-pTohienstcsocraelsesw: e“rceomdeftoerrtmabinleedtofourntchoemffoollrotawbilneg,”

“srixelPaxOeMd Stosauwbsackaelensin: “gt,e”nasniodn“‐nanatxuieratyl t(oT‐aArt)i,ﬁ”c“iadle”p[r2e3s]s.iTonhe(Dsc)o,”re“sanwgeerre‐hdoestetirlmityin(eAd‐Hfo)r,”th“evifgoollrow(Vi)n,”g

“sifxatPigOuMe S(Fs)u,”bascnadle“sc: o“ntefunssiioonn-(aCn)x.”ietAy s(Th-oArt),f”o“rdmeporfePssOioMnS(Dw)i,t”h“3a0ngqeure-hstoiostnilsitwy a(As -uHse),d” t“ovidgeocrre(Vas),e”

“pfaarttiigcuipea(nFt),b”uarndden“[c2o4n–f2u6s]i.oTnh(eC“).t”otAal smhooortdfodrimstuorfbaPnOcMe (STMwiDth)”3s0coqrueeswtiaosncsawlcuaslautesdedbyto[(dTe‐cAre+asDe

+paArt‐iHcip+aFn+t bCu)r–dVen]. [A24h–i2g6h].TTMheD“stcootarel minodoicdadteisstaunrbuannfcaev(oTrMabDle)”pssycochreolwogasiccaallsctualtaet.ed by [(T-A + D +

A-H + F + C) –V]. A high TMD score indicates an unfavorable psychological state.

2.4. Statistical Analysis

We used paired t‐tests to compare physiological indices and the Wilcoxon signed‐rank test to

compWareeupsseydchpoalioregdicat-ltetesstst stococroems. pAalrlesptahtiysstiiocalol gaincaallyisnedsicweesraenpderthfoermWeildcouxsoinngsiSgPnSeSd-vrearnskiotnes2t0t.0o

(cIoBmMpCaroerpp.s,yAchrmoloongkic,aNl tYe,sUt sScAor).esD. aAtallasrteateixstpicreaslsaendaalyssmesewanesre± pstearnfodramrdederurosirn(gmSePaSnS±vSeErs)i.oFnor20a.l0l

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wcaesehsy, ppo<th0e.0s5iz(eodnteh-saitdtehde)pwaatisencotsnswidoeurleddbsetarteilsatxiceadllyafsteigrnviiﬁecwanintg. Othnee-bsoidnesdaittersetessw. ere used because

we hypothesized that the patients would be relaxed after viewing the bonsai trees.

3. Results

Oxy‐Hb concentrations of the left and right prefrontal cortices were measured using a two‐

channOexly-NHIbRScondceevnitcrea.tioCnhsaonfgteheinleftthaendorxigyh‐Ht pbrecforonncteanltcroartitoicnesowfertehemeleafsturperdeufrsoinngtaal tcwoort-echxanwnaesl

sNigIRniSfidcaenvitclye.lCowhaenrgwe hinenthtehoexpya-tHiebnctsonvcieewnteradtitohne obfotnhsealietfrtepersef(rvoisnutaall csotirmteuxlwataiosns)igtnhiaﬁncawnhtleynlotwheeyr

vwiehwenedthneopthaitniegn(tcsovniterowl)ed(vtihsueabl osntismaiultarteieosn(=vi−su0.a2l0s±tim0.0u2laµtiMon;)ctohnatnrolw=he0n.17th±ey0.0v2ieµwMed; pno<t0h.i0n5g;

F(ciognutrreo2l)A()v. iOsuxayl‐Hstbimcounlacteionntra=tio−n0o.2f0th±e r0i.g0h2tµpMre;frcoonnttarloclo=rte0x.1d7id±n0o.0t 2sigµnMif;icpan<tl0y.0d5i;ffFerigbuertew2eAen).

vOisxuya-Hl sbtimcounlcaetinotnra(t0i.o0n0 ±of0.t0h1eµrMig)hatnpdrceofrnotnrotal l(0c.o09rte±x0.d01idµMno;tFsigigunrieﬁ2cBan) tcloynddiitfifoenr sb. etween visual

stimulation (0.00 ± 0.01 µM) and control (0.09 ± 0.01 µM; Figure 2B) conditions.

(A)

0.30

0.20

(B)

0.30

0.20

0.10

0.00

-0.10

Control

0.00

-0.10

Bonsai Control

-0.20

-0.30

Bonsai

-0.20

-0.30

Figure 2. Mean oxy-Hb concentrations in the prefrontal cortices. (A) Changes in the left prefrontal

Fcoigruterxe w2.hMeneavnieowxyin‐Hg bbocnosnacientrtereastiovns.s icnonthtreolp; r(eBf)roCnhtaalncgoerstiicnest.h(eAr)igChht apnrgefersoinntatlhecolretfetxp.reNfro=nt2a4l,

cmoertaenx±wshteanndvairedweinrrgorb. o*nps<ai0t.r0e5e,spavisr.edcotn-tterostl.; ∆(B, )chCahnagneg. es in the right prefrontal cortex. N = 24,

mean ± standard error. * p < 0.05, paired t‐test. Δ, change.

The average power of the high-frequency (HF) components of HRV, which is related to

parasTyhmepaavtheertaigceneprovwouesr aocftivthitey, ihnicgrhe‐afsreesquwehnecnyw(He fFe)elcroemlapxoedne[n21ts,22o]f. THhRisVv, awluheicwhasissigrenliaﬁtceadnttloy

pgareraasteyrmwpahtehnettihcenepravtoieunstasctviiveiwtye, dincthreeasbeosnwsahientrewees fceoeml rpelaarxeedd w[2i1t,h22t]h. eThciosnvtarloulecwonads istiigonnif(icvaisnutlayl

gstriematuelratwiohnen= t5h.4e5p±ati0e.n2t3s lvnimews2e;dcothnetroblo=ns4a.i9t5re±es0c.2o1mlpnamresd2; wp i<th0t.0h1e; cFoingturroel 3cAon).dTithioena(vveirsaugael

stimulation = 5.45 ± 0.23 lnms2; control = 4.95 ± 0.21 lnms2; p < 0.01; Figure 3A). The average low‐

frequency (LF) to HF ratio of HRV, which is related to sympathetic nervous activity, increases when

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Int. J. Environ. Res. Public Health 2017, 14, 1017

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low-frequency (LF) to HF ratio of HRV, which is related to sympathetic nervous activity, increases

whwenewfeeelfesetrlesstsreedsse[2d1[,2221],2. 2T]h. iTshriastiroatwioaws saisgnsiigfinciaﬁnctalyntlloywloewr werhwenhethnethpeatpieantitesnvtsievwieewdetdhethbeobnosanistariees

treecsomcopmarpeadrewditwhitthhethcoenctoronltrcoolncdointidointio(vnis(uvaislusatilmstuimlatuiolanti=on0.8=50±.805.0±4;0c.o0n4;trcooln=tr0o.9l 5=±0.09.506±; p0<.006.;01;

p <F0i.g0u1r;eFi3gBu)r. e 3B).

(A)

5.80

5.60

(B)

1.20

1.10

5.40

1.00

5.20

0.90

5.00

0.80

4.80

0.70

4.60

Bonsai Control

0.60

Bonsai Control

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neravcotuivsiatyc:tivmiteya:nmneaatnurnaaltuloraglalroitghamrith(lmn)(olnf)tohfethheighhig‐fhre-fqrueqeunecync(yH(FH)Fc)ocmompopnoennetn;t;(B(B) )SSyymmppaatthheettiicc nervous

nervacotuivsiatyct:ivmityea: nmenaantunraatlurlaolglaorgiathrimthm(ln(l)n)ooff tthhee raratitoioofolof wlo-fwre‐qfrueeqnuceyn(cLyF)(tLoFH) Fto(LHF/FHF(L).FN/H=F)2.4,N = 24,

meamne±ans t±a sntdanarddaredrreorrr. o*r*.p**<p0<.001.,0p1a, ipreadiret-dtets‐tt.est.

“w(vNMepfviaheeoa<tggSweNhacweiolovgntualin0dehFoagintuad.angit0biehldvevtSeggu5anaie“”sFeiitou)talteraft.iivniwrPahtwvgt“(owOieiestPOeteoueneiisonghOinwnr4rMbnPte((eueAsgaMtopPdiOnheSslninO4in<i”teMScgmsgsvsAhdah)Mu0aonwietSotieo.ibthiecw0sSohwﬁewstsadbeh5)drreccuatoi)eoesraabewtns.bnedhwldnohgOstessasaiuhtniacsstaslgtsncthasenysthiconutuealtadotheelhmrdtiirhsto,rfreebeebetisteewtspcrhadhpcstoeuearooanoeeeasnoeenltrtrrcttopfshssestegisecwuacelda“eso”gcayoinlottrhoumateiowrwttfselmheuenrgsfonpneistaesegofwt“phetainrehoevsftosaeerletdefitnefhrtttrencse,“hhmedh-sewoislavtdwieegethimgoniiwonpsgpchennwdxminpioaoaggeiiifis‐tﬁieatnriﬁtnontcahi,ctitrchet”oedehnyiaerafvnd,nrtneoixadit”nhfietchtiltei’btpsae’“SeleswelwscyotndyodDooyipcncptsiefltnm,nlooiospsh”Ssy(t“dnganywyisrDovvm“tiieetctcrhtrtieredtsmhheighooroerso(eosoeoseli“lranpuwocelelerccnoocosrbnbm,o(oh”“togegnpso,cminc”esanicictaoncocs<ndrand“fmsaaiomdploitocaie0llvtilrtoiopniic,f.rfiitoc0rnoseoafe,wato”enei1dwrfrrsnbtsurnete)eipil“a(ep.vidrfeesdp(oncfbneToies,peioo”ngwlt<tnshresninicsi<“eaosiu,eto0gef,”thnrel”nuhb.mn)es00tet“ss“cloiit1(.tmraﬁpiac0oaopbhoe)xaslca1n.roele)nt<elaear)gsTinet,d.encsmxmth”e0,hsoid,teroom.aw”leune0“T-dydifhwt1ataluehP,hirtg.”oh)nnrrloeir.o(lseiitgedaooFlgTShtdenePfisbci(hu“hl.sigrFidoirtlaeng‐beteuhoiScnhlyrg“najoﬁeure,sdo“ownut”iemcclbuftifscaerotiotah4tjreociMitpeirntoavBeualoncaeaidlnnen4o)rttfs”ltr.iyarBtoevolol,dd)y””efl.

mowodithditshtuercboanntcreo”l cwoenrdeistiiognni(ﬁpca<n0t.l0y1l)o; winedrewedh,ennevgiaetwiviengemthoetiboonnsswaietrreeessigcnoimfipcaanretldywreidthutcheedcwonhternolthe

conpdaittiieonnts(pw<er0e.0e1x)p; oinseddeetdo,nnaetugaratilvsetiemmuolit.ions were signiﬁcantly reduced when the patients were

exposed to natural stimuli.

IntI.nJ.t.EJn. vEinrovnir.oRne.sR. ePsu. bPliucbHliceaHltehal2t0h1270,1174,,1140,117017

(A)

Very comfortable/

relaxed/natural

Moderately

6 6ofo9f 10

Slightly

Indifferent

Slightly

Comfortable

feeling

Relaxed

feeling

Natural feeling

Moderately

■: Bonsai ■: Control

Very uncomfortable/

awakening/artificial

(B)

■: Bosai

■: Control

4 ** ** *

T-A

D -A-H V

-2

-4

TMD

-6

FigFuigreur4e. Q4.ueQstuioenstniaoinrenarierseulrtess.u(Alts).Su(Abj)ecStiuvbejefceteilvinegfseemlienagssurmedeaussuinregdthuesimngodtihfieedmsoedmiﬁanedticsdemiffaenretinctial

medtihffoedreanfttiearl mvieetwhoindgafttheer vbioenwsianigtrtheeesbvons.saciotnrtereosl.vsN. c=on2t4r,oml. eNan= 2±4s, tmaneadnar±d setrarnodra. r*d* eprr<or0..0**1,pW< i0l.c0o1x,on

sigWneildc‐orxaonnk stiegsnt;e(dB-)raSnckorteessto; n(Bt)hSecPorroesfiloenotfhMe PoroodﬁlSetaotfeMs aofotedr Svtiaetwesinagftethrevibeownisnagi ttrheeesbovns.saciotnrtereosl.vTs.‐A,

tencsoinotnr‐oaln. xTi-eAty, t;eDns,iodne-parnexsiseitoyn;;DA, ‐dHep, raensgsieorn‐h; oAs-tHili,tayn; gVe,r-vhiogsotirl;itFy,; Vfa,tvigiguoer;; CF,,facotingfuues;iCon, ;coannfdusTioMn;Da,ntdotal

moToMdDd,isttoutrablamncoeo.dNd=is1t9u,rmbaenacne.± Nsta=nd19a,rdmeerarnor±. *spta<n0d.0a5rdanerdro**r.p*<p0<.010,.0W5 ialcnodxo**npsi<gn0e.0d1‐,raWniklctoexsto.n

signed-rank test.

4. Discussion

4. DReissceuasrcshiodnemonstrates that oxygen consumption, regional cerebral blood response, and oxy‐Hb

supplyRaereseianrccrheadseemdoinnshtirgahtelsytahcattivoaxtyedgennecuornalsuremgpiotniosn[,1r8e]g. iAonloawl ceerreobxrya‐lHbblocoodnrceesnptroantsioe,nainnddiocxayte-sHb

thasut pthpelyquaraenitnitcyreoafsoexdyignehnigtrhalnysamctitivteadtetdo ntheeurparlerfergoinotnasl c[1o8rt]e. xAtilsoswueerisoxsym-Halbl. cTohnecleonwtreartiporneifnrodnictaaltes

cotrhteaxt athcetivqiutyanfotiutyndofinoxtyhgeecnurtrreanntsmstuitdteydistocothnesipstreenfrtowntitahl cthoratterxeptiossruteedisinsmpraelvl.ioTuhsesltouwdeiersp[r2e7f,r2o8n],tal

shcoowrtienxg athctaitviltoywfoouxnyd‐Hinb tchoencceunrrtreanttiosntusdryepisrecsoennstisthteenctawlmitihngthoaft brerpaionrtaecdtiivnitpyr. eFvoirouexsasmtupdliee,sin[2t7h,2e8],

dosrhsoowlatienrgalthparteflorowntoaxlyc-oHrtbexc,ohnecmenistrpahteiornicssrpeepcrieaslieznattitohne ocaf lemmiontgioonfablrparinocaecstsiivnigtyh. aFsobr eeexnamprpolpe,oisnedthe

bydfournscotliaotneraallmparegfnroetnictarlecsoornteaxn,cheeimmiasgpihneinrigc.sIpnepcaiarltiizcautliaorn, tohfeeamcotitvioatniaolnporfotcheesslienfgt phraesfrboenetnalpcroorptoesxed

has been associated with positive mood and the processing of positive stimuli, whereas the activation

of the right prefrontal cortex has been linked to negative mood and the processing of negative stimuli

Int. J. Environ. Res. Public Health 2017, 14, 1017

7 of 10

by functional magnetic resonance imagining. In particular, the activation of the left prefrontal cortex

has been associated with positive mood and the processing of positive stimuli, whereas the activation of

the right prefrontal cortex has been linked to negative mood and the processing of negative stimuli [29].

However, the precise details of the function of the right and left prefrontal cortex as measured using

the NIRS device remain unknown. In this experiment, the activity of the left prefrontal cortex was

suppressed, whereas that of the right prefrontal cortex did not change when the patients viewed the

bonsai trees. Based on these results, we can only conclude that the patients were in a relaxed state

when they viewed the bonsai trees.

Patients with SCI have reduced autonomic ﬂexibility, as measured using HRV, and exhibit reduced

autonomic modulation during emotion recognition tasks [10]. However, in the current study, the

patients with SCI showed signiﬁcantly higher parasympathetic nervous activity and signiﬁcantly lower

sympathetic nervous activity when exposed to a natural stimulus. These results demonstrate that in

patients with SCI, the autonomic nervous system responds to natural stimuli in a similar manner to

that in healthy adults [9,30].

Patients with SCI report pain-related disability, depression, fatigue, pressure sores, spasticity, and

issues with bladder and bowel management [31]. These conditions often induce negative mood states

in patients with SCI; thus, emotional support is an important factor inﬂuencing the rehabilitation

process [32]. The focus of rehabilitation for such patients has shifted from medical management to

QOL issues, and exposure to natural stimuli represents one way to improve QOL in patients with SCI.

Viewing bonsai trees simulates “forest therapy,” a therapeutic activity that has become popular

in Japan, and utilizes the scientiﬁcally proven effects of walking through and viewing forests [33,34].

Indeed, forest therapy is increasingly recognized as a relaxation and stress management strategy

with demonstrated clinical efﬁcacy. Forest therapy suppresses sympathetic nervous activity, increases

parasympathetic nervous activity, and reduces cortisol levels and cerebral blood ﬂow in the prefrontal

cortex [9]. Forest therapy has also been shown to increase human natural killer cell activity and

improve immunity [35–37], and these effects have been proven to last for at least seven days [36,37].

In addition, psychological studies have demonstrated the beneﬁts of forest environments on subjective

measures of stress, cognitive function, and mood [38]. There is a difference between forest therapy and

this experiment; namely, one is performed in the ﬁeld and the other indoors. The ﬁeld experiment

reveals the general inﬂuence of nature on humans through their ﬁve senses. On the other hand, we

can pick up the effect of stimulating a single sense in the indoor experiment and clarify its inﬂuence.

Here, we chose vision as one of the senses that we use in the forest, and we clariﬁed the inﬂuence of

visual stimulation by bonsai trees.

In the current study, the same psychophysiological effects of visual stimulation with bonsai trees

were shown in adult male patients with SCI as in healthy adults. We consider it an important point

that a relaxation effect could also be obtained in SCI patients by applying nature therapy, because it is

difﬁcult to perform forest therapy with SCI patients with restricted activities. Further, these ﬁndings

may help promote the development of the environment, which is beneﬁcial to the physical and mental

health of individuals with disability.

The main limitation of the present study was its small sample size. Also, the results of the present

study cannot yet be extrapolated to females. On the other hand, we compared only the condition of

viewing miniature potted trees (visual stimulation) with viewing nothing (control) in this study, but it

would be useful to investigate a third condition with a non-nature object. Furthermore, a short-term

stimulus was used; the results were compared before and after only 60 s of stimulation with bonsai

trees. In addition, we do not know for how long the effect of this natural therapy may last. Future

studies examining the duration of effects following exposure to natural stimuli are required.

5. Conclusions

In conclusion, the current study revealed that visual stimulation with bonsai trees in adult male

patients with SCI elicited the following: (1) signiﬁcantly suppressed left prefrontal cortex activity;

Int. J. Environ. Res. Public Health 2017, 14, 1017

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(2) signiﬁcantly increased parasympathetic nervous activity and decreased sympathetic nervous

activity; (3) signiﬁcantly increased “comfortable,” “relaxed,” and “natural” feelings as assessed using

the modiﬁed SD method; and (4) signiﬁcantly decreased negative and increased positive POMS

subscale scores. The ﬁndings of this study can be applied to SCI patients by taking advantage of their

natural surroundings to ensure improved health and reduced mental stress. Generally, considerably

less practice is supported by research, and the reality is that little research is applied in practice. We can

say that this study is useful because in practice the effects are proved by research data.

Acknowledgments: This work was supported by the Vehicle Racing Commemorative Foundation.

Author Contributions: Hiroko Ochiai contributed to data acquisition, interpretation of results, and manuscript

preparation. Chorong Song and Harumi Ikei contributed to the experimental design, data acquisition, statistical

analysis, and interpretation of results. Michiko Imai conceived the study and participated in the interpretation of

results. Yoshifumi Miyazaki conceived and designed the study and contributed to the interpretation of results

and manuscript preparation. All authors have read and approved the ﬁnal version submitted for publication.

Conﬂicts of Interest: The authors declare no conﬂict of interest.

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