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ARTICLE The Correlation between Primitive Reflexes and Saccadic Eye Movements in 5th Grade Children with Teacher-Reported Reading Problems Sergio Ramirez González, MS,' Kenneth J CiufFreda, OD, PhD, FAAO, FCOVD-A/ Luis Castillo Hernández, PhD,' Jaime Bernai Escalante, MS' ' Universidad Autónoma de Aguascalientes, Departamento de Optometría, México •^ State University New York, State College of Optometry, USA ABSTRACT Background: The association between the primitive reflexes of vestibular origin and the developmental control of ocular movements has been of interest to many. The objective of the present study was to determine the association, if any, between any remaining primitive reflexes and saccadic eye movements in 5th grade children with teacher- reported reading problems. Method: The primitive reflexes included: the Moro Reflex (MR), Asymmetrical Tonic Neck Reflex (ATNR), Tonic Labyrinthine Reflex (TLR), and Symmetrical Neck Tonic Reflex (STNR). Non- predictable, horizontal saccadic eye movements were tested objectively, and the saccadic ratio (number of tracking saccades to target displacements) and saccadic gain (initial saccade amplitude to target amplitude) were calculated. In addition, DEM scores and completion times were assessed. The saccadic parameters were compared to the primitive reflex scores Correspondence regarding this article can be e-mailed to kciu sunyopt.edu or sent to: Dr. Kenneth Ciuffreda, State University of New York State College of Optometry, 33 West 42nd St. NY, NY 10036. All statements are the author's personal opinion and may not reflect the opinions of the College of Optometrists in Vision Development, Optometry & Vision Development or any institution or organization to which the author may he affiliated. Pertnission to use reprints of this article must he obtained from ¡he editor. Copyright 2008 College of Optometrists in Vision Development. OVD is indexed in the Directory of Open Access Journals. Online access is available at http://www.covd.org. Gonzales SR, CiufFreda K, Hernandez LC, Escalante JB. The corrélation berween primitive reflexes and saccadic eye movements in 5tli grade children with teacher-reported reading problems. Opt Vis Dev 2008: 39(3):14O, 140 in 60 children (28 without reading problems and 32 with reading problems) in the fifth grade. Of the 60 stibjects, 34 were females (14 with reading problems) and 26 were males (18 with reading problems). Results: The results suggested that selected resid- ual primitive reflexes were correlated with reduced saccadic accuracy and impaired reading ability. In addition, the laboratory-based saccadic testing provided an objective and confirmatory correlate to the presence of abnormal primitive reflexes. Furthermore, the results provided insight into the child's gross and flne motor development as related to vision, with possible therapeutic ramiflcations. Conclusion: There were significant associations between the saccadic eye movement parameters and the primitive reflexes, especially as related to SR and TLR, in those children with reading problems. Keywords: saccades, primitive reflexes, reading, vision development, vestibular system Background Ihe vestibular oculomotor subsystem maintains body posture and stabilizes foveal gaze on the target when either an individual's head or body is displaced. Thus, any vestibular dysfunction may produce postural imbalance and/or ocular motility disorders.' The vestibular-based primitive reflexes of survival are automatic, Stereotypie movements directed from the brain stem and executed without cortical influence." They are essential for survival in the flrst weeks of life. Furthermore, they provide an important prerequisite for later development of voluntary motor-based abilities. Thus, they should normally be present for only a short period of one's life, and later they should be inhibited by higher-level centers in Opcornetry & Vision Development

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The Correlation between Primitive Reflexes and Saccadic EyeMovements in 5th Grade Children with Teacher-ReportedReading ProblemsSergio Ramirez González, MS,' Kenneth J CiufFreda, OD, PhD, FAAO, FCOVD-A/Luis Castillo Hernández, PhD,' Jaime Bernai Escalante, MS'' Universidad Autónoma de Aguascalientes, Departamento de Optometría, México•^ State University New York, State College of Optometry, USA

ABSTRACTBackground: The association between the

primitive reflexes of vestibular origin and thedevelopmental control of ocular movements has beenof interest to many. The objective of the present studywas to determine the association, if any, betweenany remaining primitive reflexes and saccadic eyemovements in 5th grade children with teacher-reported reading problems.

Method: The primitive reflexes included: theMoro Reflex (MR), Asymmetrical Tonic NeckReflex (ATNR), Tonic Labyrinthine Reflex (TLR),and Symmetrical Neck Tonic Reflex (STNR). Non-predictable, horizontal saccadic eye movements weretested objectively, and the saccadic ratio (numberof tracking saccades to target displacements) andsaccadic gain (initial saccade amplitude to targetamplitude) were calculated. In addition, DEM scoresand completion times were assessed. The saccadicparameters were compared to the primitive reflex scores

Correspondence regarding this article can be e-mailed to kciusunyopt.edu or sent to: Dr. Kenneth Ciuffreda, State University of NewYork State College of Optometry, 33 West 42nd St. NY, NY 10036. Allstatements are the author's personal opinion and may not reflect the opinionsof the College of Optometrists in Vision Development, Optometry & VisionDevelopment or any institution or organization to which the author mayhe affiliated. Pertnission to use reprints of this article must he obtained from¡he editor. Copyright 2008 College of Optometrists in Vision Development.OVD is indexed in the Directory of Open Access Journals. Online access isavailable at http://www.covd.org.

Gonzales SR, CiufFreda K, Hernandez LC, Escalante JB. The corrélationberween primitive reflexes and saccadic eye movements in 5tli gradechildren with teacher-reported reading problems. Opt Vis Dev 2008:39(3):14O,

140

in 60 children (28 without reading problems and 32with reading problems) in the fifth grade. Of the 60stibjects, 34 were females (14 with reading problems)and 26 were males (18 with reading problems).

Results: The results suggested that selected resid-ual primitive reflexes were correlated with reducedsaccadic accuracy and impaired reading ability.In addition, the laboratory-based saccadic testingprovided an objective and confirmatory correlate to thepresence of abnormal primitive reflexes. Furthermore,the results provided insight into the child's gross andflne motor development as related to vision, withpossible therapeutic ramiflcations.

Conclusion: There were significant associationsbetween the saccadic eye movement parameters andthe primitive reflexes, especially as related to SR andTLR, in those children with reading problems.

Keywords: saccades, primitive reflexes, reading,vision development, vestibular system

BackgroundIhe vestibular oculomotor subsystem maintains

body posture and stabilizes foveal gaze on the targetwhen either an individual's head or body is displaced.Thus, any vestibular dysfunction may produce posturalimbalance and/or ocular motility disorders.'

The vestibular-based primitive reflexes of survivalare automatic, Stereotypie movements directedfrom the brain stem and executed without corticalinfluence." They are essential for survival in the flrstweeks of life. Furthermore, they provide an importantprerequisite for later development of voluntarymotor-based abilities. Thus, they should normally bepresent for only a short period of one's life, and laterthey should be inhibited by higher-level centers in

Opcornetry & Vision Development

the brain, so that the postural reflexes at these higher of visual space and poor eye-hand coordination maybrain centers can develop and mature properly.^ be evident.

At birth, vision ofthe newborn is only adapted Thus, the purpose ofthe present investigationfor their immediate necessities. With relatively close was to determitiate the relation between the prim-focusing at a distance of 20-25 cm,' their visual world itive reflexes, saccadic oculomotor control, andis a near patchwork of changing forms, shades, and reading ability.^patterns. The primitive reflexes of survival providethe mechanism through which the intant can learn Subjectshow to understand what is being seen during the Sixty fifth-grade children from 5 public schoolsfirst months of life, and furthermore they teach the in Aguascalientes, México, were selected. Ages rangedinfant to coordinate the fine ocular musculature in from 10 to 13 years, with a mean of 10.6 years. Thesuch a way as to acquire appropriate accommodative schoolswerechosenbystratum:childrenwereexcludedabilities, fusion, fixation, and convergence, as well as with general binocular vision problerns, strabismus,provide protection from excessive light.' amblyopia, delay in development, and systemic

However, if the primitive reflexes of survival or neurological problems based on an optometricremain after 6 months of age, they may hinder normal vision screening. The children were classified as eitherdevelopment of the postural reflexes and of ocular "having" or "not having" a reading problem based onmotility.^ Development of the visual system depends classroom performance and school history as assessedfirst on the early presence of these reflexes, and then by their teacher. 28 were classified as not having alater on inhibition of at least the following primitive reading problem, and 32 were classified as having areflexes: Moro Reflex (MR), Asymmetrical Tonic Neck reading problem.Reflex (ATNR), Tonic Labyrinthine Reflex (TLR),and the Symmetrical Tonic Neck Reflex (STNR). Apparatus

The MR and TLR are closely bound in the first Binocular horizontal movements were recordedmonths of life. They are of vestibular origin, and both with the elcctro-oculographic technique (EOG)**can be activated either by stimulation ofthe labyrinth usitig the EOG Biopac System Inc., (Goleta, CA). Itor by alteration of body position in space. If the MR had an analog input and an acquisition sample rate ofremains active too long, however, the infant will be 200 samples/second. Random, horizontal step (4-10hypersensitive in one or more ofthe sensorial channels, degrees) stimuli comprised of a matrix of 20/30 sizeand the eyes will be attracted automatically toward any letters at 40 cm. were used. Overall target size was 1.1bright light, movement, or any alteration in the visual deg. square. The target was presented on a computerfield. Hence, this may lead to distractibility, poor screen. The head was maintained stable in a headrest/balance and coordination, and oculomotor problems, chinrest assembly during the objective saccadic eyeA retained ILR may prevent complete development of movement testing,these later postural reflexes, particularly of the ocularreflex and ofthe head righting-reaction.'* Balance will Procedurebe adversely afl ected by poor visual information, and Subjects were administered the following batteryvision will be aflected by poor balance. Poor egocentric of tests: Developmental Eye MovementTest (DEM),''locus and difliculty with spatial judgment may also objective EOG electrooculography,** and evaluationbe evident/' of the primitive reflexes - ' inciuding the Moro

The ATNR has an important function in reflex (MR), asymmetrical tonic neck reflex (ATNR)establishing hand, leg, head, and eye preferences, (Schilder test), tonic labyrinthine reflex (TLR),or body dominances. Problems related to ocular and symmetrical neck tonic reflex (STNR), in adominance can affect reading, writing, and spelling.^ counterbalanced manner to avoid test order efl"ects.The permanency of this reflex will act like an invisible Testing was as follows. After the horizontal eyebarrier to crossing the midline ofthe body in such a movement calibration, 50 horizontal, random stepsway that the whole body will execute tasks effectively were presented. Saccadic test parameters includedtising only one side at a same time. And, lastly, if the saccadic gain (initial saccade amplitude divided bySTNR is functional too long, delayed upper and lower target amplitude) and saccadic ratio (total numberbody coordination, cross-pattern creeping, expansion of saccades executed divided by the total number of

Volume .iy/Niimber 3/2008 141

target step displacements). Total time for completionof the DEM test, as well as the horizontal and verticalscores, was also recorded. The 4 primitive reflexeswere tested in the manner described by Goddard." Foreach test, the score ranged from 0 - 4 , with zero beingthe best, and 4 being the worst, in units of wholenumbers. The reflexes included the asymmetrical tonicreflex tested in the quadruped position (ATNRAT)(the Ayres Test), symmetrical tonic neck reflex, toniclabyrinthine reflex,'*' and Moro's reflex. See Figuresla-d for the basic primitive reflex test positions.

Figure Ic. STNR

142

Figure Id. TLR

Optometry & Vision Development

Table 1: Descriptive statistics of the two groups

ReadingProblem

NO

YES

AGE (years )

10

18

11

11

9

17

12

1

2

13

0

2

GENDER

Female

20

14

Male

8

18

TOTAL

28

32

60

Table 2: Mean valueswithout (NO RP) and

of the testwith (RP) a

parameters for thosereading problem

SAC RATIO

SAC GAIN

DEM V

DEM H

DEM TIME

MR

ATNR

STNR

TLR

NO RPRP

NO RPRP

NO RPRP

NO RPRP

NO RPRP

NO RPRP

NO RPRP

NO RPRP

NO RP

RP

Mean1.212.87

.81

.5949.3217.9742.1411.5039.4541.50

.71

1.881.071,841,182,691.04

3.06

SEM

7.89E-028.69E-021.63E-021.95E-02

4,163,294.142.723.152.42

.17

.14

.10

.14

.10

.11

9.60E-02

.19

T-test

p<0.01

p<0.01

p<0.01

p<0,01

p=0.603

p<0,01

p<0,01

p<0,01

p<0,01

ResultsTable 1 shows the descriptive stat-

istics related to age, gender, and presenceor absence ofa reading problem in thetwo populations.

Table 2 presents the mean valuesof the various test parameters for bothgroups of children. All parametersexcept DEM completion time weresignificantly different and abnormalin the children manifesting readingproblems. Thus, both global saccadicaccuracy and visual search, as well asail primitive reflexes, were poorer inthe reading-disabled children.

Table 3 presents the correlationsfor all test parameters in both groupsof children. In those without readingproblems, several key points deservemention. (1) Saccadic ratio andsaccadic gain were correlated, asexpected; the fewer the saccades,the higher the saccadic gain and thelower the ratio, and (2) Four of the5 saccadic parameters correlated withthe primitive reflex STNR, with itbeing most predictive of a saccade-based interrelationship. (3) Saccadicparameters also correlated with manyof the other primitive reflexes {e.g.,TLR). (4) The clinical DEM test was

Table 3: Significant correlations for all test parameters in those without(NO RP; top) and with a reading problem (RP; bottom)

wo RP

SAC RATIO

SAC GAINDEMV

DEM HDEM TIME

SAC RATIO

1.000

SAC GAIN

-,418

1,000

DEMV

1,000

DEM H

,600

1.000

DEM TIME

1.000

MR

-075

ATNR

-.347

STNR

.635

-.383

-.395

-.069

TLR

.486

-.117

RP

SAC RATIO

SAC GAINDEMV

DEM H

DEM TIME

SAC RATIO

1.000

SAC GAIN

-.252

1,000

DEMV

1.000

DEM H

,706

1.000

DEM TIME

.341

1,000

MR ATNR

,374

STNR

.382

-.391

TLR

.442

-.214

-.355

Volume 3'J/Numbcr 3/2008 143

A. Correlation values between primitiverefiexes and sac ratio

B. Correlation values between sac gainand primitive refiexes

ATNR STNR TLR

• NORP• RP

0.1

0

-0.1

-0.2

-0.3

-0.4^A

D

MR y

[

1 11 •1\TNR STNR

NORPRP

TLR

Figure 2; Correlation values for the primitive reflexes in both groups of children for sac ratio and (A) sac gain (B).

correlated with two of the 4 primitive reflexes (i.e.,STNR and TLR). In those with reading problems,several key points deserve mention. (1) Saccadic ratioand saccadic gain were not highly correlated, thussuggesting increased variability in saccadic accuracy.(2) Three of the 5 saccadic parameters correlated withthe primitive reflex TLR, with it being most predictiveof a saccade-based interrelationship. (3) Saccadicparameters also correlated with many of the otherprimitive reflexes (e.g., STNR), and (4) the clinicalDEM test was correlated with one of the primitivereflexes (i.e., TLR).

Figure 2 shows the correlation values in bothgroups of children as related to saccadic ratio andsaccadic gain, and the 4 primitive reflexes. The MR wasconsistently least correlated in the two populations,whereas STNR and TLR were most consistentlycorrelated in the two populations.

DiscussionThe spinal cord is composed of a series of ascending

and descending fibers that transport informationfrom the periphery toward the brain centers andvice versa.'^ The vestibular pathway has considerableimportance for the acquisition and development ofposture and balance. It is connected fiindamentallywith the cerebellum and the spinal cord, as well aswith cortical visual areas. These relationships are of

importance to facilitate head movement with relatedcoordinated eye movements. From this labyrinthineanatomical and functional integration, namely that ofthe propioceptive, reticular, ocular, visual, cerebellumand cortical systems, there arise the mechanisms thatwill give a rise to the neurobiological foundationfor the processes of postural tonic control, as well ascoordinated and intentional movement of the eyes.

The primitive reflexes and the postural reactionscomprise one of the earliest, simplest, and mostfrequently used tools for the pédiatrie neurologist toassess central nervous system integrity of infants andvery young children. The clinical significance of theprimitive reflexes, either alone or in combination,contributes to the early diagnosis. Moreover, infantswith 5 or more abnormal postural reactions may bediagnosed with either cerebral palsy or developmentaldelay.'- The combined examination of the primitivereflexes and postural reactions is useful and should beconsidered as a simple but predictive screening test forthe early identification of developmental risks factorsfor the pédiatrie optometrist.

The correlation between the remaining primitivereflexes and saccadic eye movements in 5th gradechildren with reading problems was investigated todetermine the level of association of each reflex withthe eye movements, and furthermore to considertraining to inhibit these reflexes, with the potential

144 Optonietry & Vision Development

to faster normal vision development. These reflexescomprise the basic units of movement, and theycombine together to create more varied and complexpatterns of movement with further development andmaturity. Tiiere were significant associations betweenthe remaining primitive reflexes and saccadic eyemovements, with the STNR showing the greatestassociation in those without reading problems andthe TLR in those with reading problems. The STNRand TLR also exhibited a strong relationship with thesaccade ratio and some ofthe DEM findings.

The information obtained in the present study maybe of value in the future to determine if vision therapycan be implemented to inhibit these reflexes and toimprove the development of saccadic movements andreading,'^ as well as vision development in general.Primitive reflexes which are poorly integrated andpersist may not allow the proper development ofvisually-guided movement necessary for adequatevisuomotor coordination, and furthermore it mayinterfere with development of higher-level visual-spatial concepts.

References1. Bürde RM,,SavinnMJ.TrobcJD. Clinical decisions in neuro-ophchalmoingy.

S[. Louis: Tliird Edirion. Mosby, 2002:200-211.

2. Goddard SC. Reflexes, learning and behavior: A winiiow into the cliildVmind. Eugene. Oregon: Kern Ridge Press, 2002:1-95.

3. Banks MS. The development of visual accommodation during early infancy.Child Dev 1980:51:646-666.

4. Marquis PJ. Ruiz NA, Lundy MS, Dillard RG. Retention of primitivereflexes.] Dev BchavPediatrl984:5(3):l24-126.

5. Wc^cnan T, Brov/n JK, Fulford GE, Minns RA. A study of normal babymovements. Child Care Health Dev 1987:13(l):41-58,

6. Capute AJ, Shapiro KC, Accardo PJ. Wachtel RC. Ross A, Palmer FB.Motor functions: associated primitive reflex profiles. Dev Med Child Neuroli984:26(3):375-383.

7. Marusich CE. integration of primitive motor rt'fiexesi Why should I care.Optometry 2005:76(2): 123-127.

8. Ciuffreda KJ,Tannen B. Eye movement basics for che clinician. St Louis CVMosby. 1995:184-2005.

9. Garzia RP, Richmon JE, Nicholson SB. A new visual-verbal saccade test:the developmental eye movement test (DEM). J Am Optom Assoc 1990:{61):124-128.

10. Wahlberg T, Ireland D. Can replicating primar)' reflex movements improvereading ability? Optom Vis Dev 2005:36(2);89-91.

11. Kline LB, Bajandas EJ. Neuro-Ophthalmology. Thorofare, NJ: SIACK,2004:97-103.

12. Bartlett D, Piper M, Oku» N, Byrne P, Watt J. Primitive reflexes and thedetermination of fetal presentation at birth. Early Hum Dev 1997:48(3):26i-27.

13. Wahiberg T, Ireland D. Can Replicating Primary Reflex MovementsImprove Reading Ability? Optom Vis Dev 2005;36(2):89-91

AWARDS FOR EXCELLENCEIN VT GIVEN TO

GRADUATING OPTOMETRYSTUDENTS

COVD is pleased to announce that the followingstudents received the 2008 COVD Award forExcellence ¡n Vision Therapy during graduationservices this spring at their school or collegeof optometry.

Jeffrey D. ColemanInter American University of Puerto Rico

Alicia FeisSouthern California College of Optometry

Joan HarpenauIndiana University School of Optometry

Efrat KeinanHadassah College in Jerusalem

Diana S. MaSalus University{Pennsylvania College of Optometry)

Rebecca MaidaNew England College of Optometry

Ghadeer A. MakoshiPacific University College of Optometry

Catherine McDanielThe Ohio State University College of Optometry

Melissa MiskoIllinois College of Optometry

Katherine ShuellFerris State UniversityMichigan College of Optometry

Christina WilliamsUniversity of Waterloo

Benjamin WintersSouthern College of Optometry

Emily WuUniversity of California, Berkeley

The COVD Excellence in Vision Therapy Award is givento recognize those students who have demonstrateda strong interest and clinical skills in vision therapy.Congratulations to each of these new optometrists.

Volume 39/Numbcr 3/2008 145