effects of unilateral midbrain lesions on gaze (eye and head) movements

Ann. N.Y. Acad. Sci. ISSN 0077-8923

ANNALS OF THE NEW YORK ACADEMY OF SCIENCESIssue: Basic and Clinical Ocular Motor and Vestibular Research

Effects of unilateral midbrain lesions on gaze(eye and head) movements

Olympia Kremmyda,1,2 Stefan Glasauer,2,3 Lorenzo Guerrasio,3 and Ulrich Buttner2,3

1Department of Neurology, 2Integrated Center for Research and Treatment of Vertigo, Balance and Ocular Motor DisordersIFBLMU, Campus Grosshadern, 3Center of Sensorimotor Research, Ludwig–Maximilians University, Munich, Germany

Address for correspondence: Ulrich Buttner, M.D., Center of Sensorimotor Research, Campus Grosshadern,Ludwig–Maximilians University, Marchioninistr 23, 81377 Munich, Germany. [email protected]

The rostral midbrain, especially the rostral interstitial nucleus of the medial longitudinal fasciculus (RIMLF) and theinterstitial nucleus of Cajal (INC), plays an important role in the control of eye movements. Although the effect ofmidbrain lesions on eye movements is well investigated, little is known about its effect on head movements. In thisstudy, we measured eye and head (gaze) movements in five patients with unilateral, acute midbrain lesions and ninehealthy controls. In all patients, vertical eye velocity was reduced as a result of the lesion compared to healthy subjects,whereas peak head velocity was not affected. Further, most patients displayed an increased contralesional torsion inperipheral head positions, independently of whether they presented a head tilt in the straight-ahead position or not.Our results indicate that midbrain lesions affect the control of eye and head differently and independently.

Keywords: gaze movements; INC; RIMLF; rostral midbrain

Preferred citation: Kremmyda, O., S. Glasauer, L. Guerrasio & U. Buttner. 2011. Effects of unilateral midbrain lesions on gaze

(eye and head) movements. In Basic and Clinical Ocular Motor and Vestibular Research. Janet Rucker & David S. Zee, Eds.

Ann. N.Y. Acad. Sci. 1233: 71–77.

Introduction

The mesencephalon is a critical area for the con-trol of combined eye and head (gaze) movements,containing nuclei such as the rostral interstitial nu-cleus of the medial longitudinal fasciculus (RIMLF),which serves as the vertical-torsional saccade gen-erator, and the interstitial nucleus of Cajal (INC),which is regarded as the vertical-torsional neuronalintegrator for the eye.1

Isolated RIMLF lesions lead to contralesional tor-sional deviations during vertical saccades with a sub-sequent drift to the torsional zero,2 whereas isolatedINC lesions cause ipsilesional torsional nystagmus.Combined RIMLF and INC lesions can lead to con-tralesional torsional nystagmus.3 Torsional devia-tions can be observed during larger vertical saccadesand are always contralesional, whereas torsional nys-tagmus is present when looking straight ahead.

Midbrain lesions can also lead to a contralesionalhead tilt,4 but so far, less is known about the effectof midbrain lesions on the three-dimensional (3D)

head movement pattern. Recent studies in monkeyssuggest that the INC serves as the neuronal integra-tor also for the head,5,6 but so far human data aremissing.

In the present study, we investigated how acuteunilateral rostral midbrain lesions in patients affecteye, head, and gaze (combined eye and head move-ment) velocity and the 3D head position patternafter gaze movements to peripheral targets. Part ofthe head data have been published elsewhere.7

Patients and methods

Patients and control subjectsWe included five patients with acute (maximal fivedays old) unilateral mesencephalic lesions, withoutoculomotor nerve palsy. An overview of the patientsand the lesions is given in Table 1.

Patient 1 was a 59-year-old woman who woke upwith the left side of her mouth dropping, a fallingtendency to the left, clumsiness of the left hand, anddysarthric speech. Clinical examination showed avertical gaze paresis with counterclockwise (upper

doi: 10.1111/j.1749-6632.2011.06173.xAnn. N.Y. Acad. Sci. 1233 (2011) 71–77 c© 2011 New York Academy of Sciences. 71

Midbrain lesions and gaze movements Kremmyda et al.

Table 1. Clinical characteristics of the five patients measured in this study at the day of registrationa

Lesion Oculomotor deficits

Patient Age Type Side RIMLF INC Vertical palsy Other Head tilt SVV

P1 59 Infarct Right + − + TD (CCW) No Left

P2 80 Infarct Left + + + GEN downward No Right

P3 71 Hemorrhage Right + + + TD(CCW)/GEN Yes(CCW) 15◦ Left

P4 45 Infarct Right + − + TD (CCW) No Left

P5 48 Infarct Left + + + TN (CW) Yes (CW) 10◦ Right

aGEN, gaze-evoked nystagmus; TD, torsional deviations; TN, torsional nystagmus; CW, clockwise; CCW,counterclockwise; SVV, subjective visual vertical

pole of the eyes to the left, from the patient’s point ofview) torsional deviations of vertical saccades andan initial head tilt to the left, which was no longerpresent at the day of the eye movement recordings.Subjective visual vertical was tilted to the left by 5◦.MRI revealed a right RIMLF lesion, which includedpart of the thalamus.2

Patient 2 was an 80-year-old man with a sud-den onset of vertigo, falling tendency to the right,and vertical diplopia. Clinical examination showed avertical gaze paresis, skew deviation (left over righteye), a downward gaze-evoked nystagmus, but nohead tilt. Neither torsional nystagmus nor torsionaldeviations were observed. Subjective visual verticalwas tilted to the right by 7◦. MRI revealed a small,left, mesencephalic ischemia that involved mainlythe INC and a part of the RIMLF.

Patient 3 was a 71-year-old man with acute ver-tigo and paresis of the left arm. Clinical examina-tion showed along with a vertical gaze paresis withcounterclockwise (contralesional) torsional devia-tions, a vertical gaze-evoked nystagmus, and a headtilt to the left (15◦). Subjective visual vertical wastilted to the left by 10◦. Computer tomography re-vealed a right thalamic/mesencephalic bleeding thatincluded both the INC and the RIMLF.

Patient 4 was a 45-year-old woman with acutevertigo symptoms. Clinical examination revealed avertical eye movement paresis with counterclock-wise torsional deviations. No head tilt was present.Subjective visual vertical was tilted to the left by 5◦.MRI revealed an isolated right RIMLF lesion. 8

Patient 5 was a 48-year-old man with suddenvertical diplopia. Clinical examination showed a ver-tical gaze paresis, a clockwise (contralesional) tor-sional nystagmus, a vertical gaze-evoked nystagmus,and a right head tilt of 10◦. Subjective visual vertical

was tilted to the right by 15◦. MRI revealed a leftmesencephalic infarction that extended to the levelof the red nucleus and included both RIMLF andINC.

Nine subjects (age 52–83) without known neuro-logical disease were measured as control subjects.

All patients and subjects signed an informed con-sent before the recordings.

Coil measurements

For the 3D eye movement recordings, we used adual search coil on the left eye (Skalar, Delft, TheNetherlands), and for the 3D head movements weused two coils mounted on a head ring at a 90◦ anglebetween them. Both head and eye coil measured ab-solute position in space. Therefore, when the headwas allowed to move, the eye coil recorded gaze(combined eye and head) movements. The absoluteeye contribution to the movement (eye in head) wascomputed by subtracting the head movement fromthe gaze movement. When the head is fixed, gazeand eye movement are identical. Signals were sam-pled at 1 kHz. The subjects were seated in completedarkness inside a magnetic field (Remmel Labs) andwere instructed to follow a laser dot (size 0.1◦, dis-tance 145 cm). Details on the calibration methodare given elsewhere.9 Subjects had to perform twodifferent tasks: the head-fixed task and the head-freetask.

In the head-fixed task, subjects had to follow thetarget with only the eyes, while the head was placedon a chin rest. The laser dot jumped from the centerto peripheral positions (maximal target jump 18◦

horizontally and vertically) and then back to thecenter. In each position, the laser dot remained vis-ible for 500 ms, then disappeared for 2,500 ms, andappeared again in the same position.

72 Ann. N.Y. Acad. Sci. 1233 (2011) 71–77 c© 2011 New York Academy of Sciences.

Kremmyda et al. Midbrain lesions and gaze movements

Figure 1. Gaze (A, C) and head (B, D) movement recordings from a normal subject (A, B) and from patient 2 (C, D) during thehead-free task. Positive values indicate rightward and upward movements. Although the vertical gaze amplitude was reduced in thepatient, the head movement amplitude was similar to that in the normal subject.

In the head-free task, subjects had to follow thetarget with combined eye and head (gaze) move-ments. The laser dot jumped randomly between thecenter and eight peripheral positions (28◦), so thateach final position was reached from a different ini-tial position four times (maximal target jump 56◦

horizontally and vertically; see Fig. 1A). In each po-sition, the dot was first visible for 1,000 ms, thendisappeared for 2,500 ms and appeared again in thesame position.

Eye and head rotations were expressed as quater-nions;10 their 3D scatter at fixation points (velocity<10◦/sec) was fitted with a second-order surfacedefined by the equation:

q1 = a1 +a2q2 +a3q3 +a4q2q3 +a5(q2)2 +a6(q3)2,

(1)

where q1, q2, and q3 are the torsional, horizontal,and vertical quaternion components, respectively.

Parameters a1, a2, and a3 describe the offset andtilt of the surface, while parameters a5 and a6 repre-sent the torsional curvature along the horizontal andvertical axis of rotation (vertical and horizontal ro-tations, respectively) with positive values indicatingclockwise (rightward) torsion. The a4 coefficient,also called the twist score, quantifies the twist of thecomputed surface.11 A negative twist score indicatesthat the system (the head or the eye) is behaving likea Fick gimbal—i.e., that it rotates first around thevertical axis and then around the horizontal one.The surfaces, computed from the eye and from thehead positions, are thought to reflect Donders’ law,which states that for each (eye or head) vertical andhorizontal position, only one possible torsional po-sition exists.11

The zero torsion value for the eye was computedwith the patient looking straight ahead. Accordingly,values of torsion are expressed in patient (and not

Ann. N.Y. Acad. Sci. 1233 (2011) 71–77 c© 2011 New York Academy of Sciences. 73


space) coordinates. The actual head tilt was mea-sured by means of an angulometer just before thestart of the movement recordings. Only patients 3and 5 displayed a head tilt at the day of the coilmeasurement.

The eigenvalues �1 and �2 of Eq. 1 were computedin order to describe the surface shape independentlyof its exact orientation (parameters a1, a2, and a3).Indeed, surfaces mathematically described by equa-tion in the form of Eq. 1 can be redefined by meansof their eigenvalues as

Z = c + �1x2 + �2 y2, (2)

where z is a value related to head torsion. If oneof the eigenvalues is close to zero, the shape of thesurface is flat in one direction (c.f. Fig. 2A and B);if the two eigenvalues have opposite sign, the sur-face is a saddle (Fig. 2C); and if both have the samesign, the surface is a parabola (either open on thetop or on the bottom). To reduce the two eigenval-ues to one index of symmetry SI , we calculated theabsolute ratio of the eigenvalues with the smaller(absolute) value being the numerator. An index of1 (both eigenvalues equal) thus indicates a surfacewith equal curvature in both principal directions,whereas an index of zero indicates that the curva-ture is close to zero (flat) in one direction:

S I = |�1/�2| for |�1| ≤ |�2|S I = |�2/�1| for |�2| < |�1|.

Data analysis was performed using MatLab. Stu-dent’s t-test or Wilcoxon’s rank-sum test were usedfor statistical analysis. Statistical significance was setat P < 0.05.

Results

Velocity and amplitude analysisIn order to describe the differences between patientsand control subjects in saccade amplitudes and ve-locities, we averaged the largest value of amplitude(maximal amplitude) and peak velocity (maximalpeak velocity) of each element of the two groups.Statistical results were the same also by averagingeach subject’s mean values, instead of the largest, ofall the saccades performed during a task (mean peakvelocity and mean amplitude).

Head-fixed task. With the head fixed, all midbrainpatients had reduced peak vertical eye velocities(average peak velocity upward: 199 ± 77◦/sec;downward: 137 ± 54◦/sec) comparing to controlsubjects (average peak velocity upward: 338 ±38◦/sec; downward: 331 ± 73◦/sec: P < 0.001 forboth vertical directions) while attempting to per-form 18◦ saccades. Further, the vertical componentof saccades was consistently smaller in patients thanin control subjects (average largest value: patients:upward: 14 ± 4◦, downward: 9 ± 3◦; controls: up-ward: 17.6 ± 2◦, downward: 17.4 ± 2◦; P = 0.04and P < 0.001, respectively). As expected, the peakhorizontal eye velocity was not affected by the mid-brain lesion (patients: rightward: 359 ± 125◦/sec,leftward: 352 ± 85◦/sec; controls: rightward: 344 ±43◦/sec, leftward: 326 ± 61◦/sec; P = 0.74 and P =0.52, respectively).

Head-free task. Eye data. Similarly to the head-fixed task, the vertical eye (in head) velocity waslower in the midbrain patient group than in thecontrol group (patients: upward: 252 ± 164.8◦/sec,

Figure 2. 3D head surfaces of patient 4 (A), 5 (B), and from a normal subject (C). The z-axis indicates torsion (positive valuesindicate clockwise torsion). In a normal subject (C), the surface has the form of a double saddle, whereas in patients the surfacebecomes a contralesionally curved parabola; for patient 4 (right lesion-A), the surface is curved counterclockwise (left), and forpatient 5 (left lesion-B) the surface is curved clockwise (right).



downward: 175.8 ± 104.9◦/sec; controls: upward:400.8 ± 30◦/sec, downward: 410.4 ± 59.5◦/sec; P =0.019 and P = 0.005, respectively). Peak down-ward, but not upward amplitude was significantlyreduced (patients: upward: 26.3 ± 16.1◦, downward:21.7 ± 12.2◦; controls: upward: 36.7 ± 6.6◦, down-ward: 40.2 ± 5.7◦; P = 0.128 and P = 0.0022,respectively).

Head data. Despite the impairments affectingthe eye movements of midbrain patients, the ver-tical head velocity was not significantly differentin the two groups. The peak vertical head veloc-ity in the patient group was 69.3 ± 23.1◦/sec and68.2 ± 21.8◦/sec for upward and downward headmovements, and in the control group was 71.4 ±29.7◦/sec and 63.8 ± 31.1◦/sec respectively (P >

0.05 for both directions). The peak head amplitudewas also similar in both groups (patients: upward:18.1 ± 10◦, downward: 18 ± 7.2◦; controls: upward18.5 ± 8.1◦/sec, downward: 18.2 ± 8.5◦; P > 0.1 forboth directions; Fig. 1B and D). Similar results wereobtained by using mean velocity and amplitude val-ues. The values for the control group correspond tomain sequence data for head movements in normalsubjects, as reported in other studies.12

Gaze data. Overall, the vertical peak gaze velocitywas lower in the midbrain group (patients: upward:256.2 ± 154.1◦/sec, downward: 167.7 ± 81.4◦/sec;controls: upward: 423.2 ± 22.5◦/sec, downward:432.3 ± 61.9◦/sec; P = 0.007 and P = 0.003, re-spectively). Although the downward peak gaze am-plitude was also lower in the patients (patients 29.6± 8◦/sec; controls 44.2 ± 4.8◦; P = 0.001), sig-nificance was not reached for the upward peakgaze amplitude (patients: 38 ± 10.3◦; controls:43 ± 7.1◦; P = 0.29). Note that although the maxi-mal target jump was 56◦ in the paradigm, even nor-mal subjects usually needed more than one saccadeto reach the target, and therefore the peak amplitudewas lower than that.

3D plot analysisHead-free task. Eye data. Torsional variability (av-erage torsional distance of the fixation pointsaround the plotted surface) for the eye data wasmarginally larger in the patient group (2.2 ± 0.9◦

versus 1.4 ± 0.6; P = 0.05). Twist scores (parametera4) did not significantly change with the midbrainlesion (patients: −0.05 ± 0.74; controls: 0.3 ± 0.18;P = 0.235). Gaze surfaces of patients 1, 3, and 5

had increased contralesional curvatures during ver-tical movements (a5 = −0.81, −1.08, and 0.29, val-ues lying outside the confidence interval (CI) of thecontrol group; CI = −0.64 to −0.08).

Head data. In the patient group, neither the tor-sional variability nor the twist score (a4) was signif-icantly different from the controls (torsional vari-ability: patients: 1.31 ± 0.53◦; controls: 1.15 ± 0.51◦;P = 0.594; twist score: patients: −2.13 ± 1.54;controls: −1.73 ± 1.73; P = 0.6793). The curva-ture of Donders’ surface along the horizontal axis(during vertical head movements), quantified bythe parameter a5, increased in patients 1, 3, and 5(a5 = −1.4, 0.5, and 0.70; CI = −0.665 to 0.2650).Interestingly, the curvature always increased in theopposite direction of the lesion. This was also truefor patients 3 and 4, but values remained within theCI (−0.47 and −0.59, respectively). For horizontalhead movements, patients 1, 3, and 5 showed anincreased contralateral torsional curvature (−0.89,−2.1, and 0.72; CI: −0.72 to 0.70).

The SI calculated from the eigenvalues of the headposition surface showed a significant difference be-tween control subjects and patients, controls sur-faces being more symmetric (controls: SI = 0.45 ±0.24; patients: SI = 0.13 ± 0.16; P < 0.007 Wilcoxonrank-sum test). Figure 2 shows examples of two pa-tients (patient 4 [A]: 0.049; patient 5 [B]: 0.040) andone control subject (C: 0.78).

Gaze data. Torsional variability was larger in thepatient group (2.6 ± 1.4◦ vs. 1.6 ± 0.46), butthis difference did not reach statistical significance(P = 0.067). Twist scores (a4) were lower than in thehead data, but remained unchanged by the midbrainlesion (patients: −0.13 ± 0.33; controls: −0.18 ±0.3; P = 0.774). Contralesional torsional curvaturealong the horizontal axis was, like for the head data,larger in patients 1 and 5 (−0.67 and 0.02; CI: −0.28to −0.07), but also for patient 3 (−0.72). In patient4, the gaze surface was also curved contralateral tothe lesion (−0.26). In patient 2, Donders’ surfacedid not change.

Discussion

In the current study, we present gaze data from fivepatients with acute unilateral midbrain lesions. Allpatients had a vertical gaze paresis, but not a com-plete loss of vertical eye movements. The palsy wasmore evident for downward than for upward sac-cades, in agreement with the previous literature.13



This has been explained by the fact that projectionsfrom the RIMLF to the elevator eye muscles are bi-lateral,14 whereas projections from the RIMLF to thesuppressor eye muscles are mostly unilateral, so thatdownward movements are more affected by unilat-eral RIMLF lesions.15 As expected, horizontal eyemovements were not affected by the lesion.

When the patients were allowed to move the head(head-free task), vertical peak velocity and ampli-tude of both the eye and gaze were also reduced incomparison to control subjects. On the contrary,head peak velocity and amplitude were not signifi-cantly different. Thus, all deficits in gaze were due toeye movement deficits or, in other words, head didnot compensate for the eye impairment. Supportingthis hypothesis, gaze data from patients with pro-gressive supranuclear palsy (PSP) show no correla-tion of the vertical gaze palsy with head amplitudeduring downward pitch (vertical) movements.16 Inaddition, data from healthy monkeys showed thatvertical head peak velocity and duration did notdepend either on gaze or on the eye velocity andamplitude.17

The effects of rostral midbrain lesions on eyemovements have been thoroughly investigated bothin monkeys18,19 and in humans.2,3 However, muchless is known about the effects of the same lesionson head movements. Recent experimental data onmonkeys5 suggest that the INC acts as an ipsilateralvertical-torsional integrator not only for the eye, butalso for the head. Accordingly, unilateral INC lesionsin monkeys cause a contralesional head tilt in gazestraight ahead and an initial head drift.6 Althoughthree out of five patients did not show a head tiltwhen looking straight ahead, 3D analysis of periph-eral head fixations showed that contralesional headtilt was larger in these patients than in the controlgroup, which was expressed as increased contrale-sional curvature of Donders’ surfaces, so that theform of the surface changed from a double saddleto a parabola. These changes in the head surface didnot always correlate with changes in the eye move-ments, since each patient had a different eye move-ment deficit, further supporting the hypothesis thateye and head commands operate independently atthe midbrain level.

Two of the patients (1 and 4) who exhibitedan increased head contralesional torsional curva-ture had a RIMLF lesion, with no involvement ofthe INC. Anatomical data from monkeys20,21 show

that although the RIMLF itself does not have di-rect anatomical projections to neck muscles, theadjacent rostral part of the mesencephalic reticu-lar formation (also called piMRF) plays a role in thevertical component of gaze through connections tothe cervical muscles.22 The pathway from the supe-rior colliculus through the mesencephalic reticularformation to the spinal cord is mostly an ipsilat-eral one;23 therefore, lesions in this pathway coulddisturb the symmetry of the 3D head movementpattern, shifting the direction preference contrale-sionally, as shown by the lower symmetry index inthe patient group. Thus, different anatomical lesionsin the midbrain level could affect eye and head dif-ferently, depending on the level of participation ofthose structures in the lesions.

So far, the number of patients was small and thelesion sites were not identical; thus, no final conclu-sions can be drawn from this study on the separaterole of each midbrain gaze structure in humans.However, our results clearly show that a head orien-tation deficit can be demonstrated with 3D analysisof Donders’ plane, also in patients with no headdeficit when looking straight ahead.

Acknowledgments

The authors would like to thank Dr. Thomas Eggertfor the maintenance of the coil lab. This work wassupported by the Integrated Center for Research andTreatment of Vertigo, Balance, and Ocular MotorDisorders IFBLMU-01EO0901.

Conflicts of interest

The authors declare no conflicts of interest.

References

1. Buttner, U. & J.A. Buttner-Ennever. 2005. Present conceptsof oculomotor organization. Prog. Brain Res. 151: 1–42.

2. Kremmyda, O., J.A. Buttner-Ennever, U. Buttner & S.Glasauer. 2007. Torsional deviations with voluntary saccadescaused by a unilateral midbrain lesion. J. Neurol. Neurosurg.Psychiatr. 78: 1155–1157.

3. Helmchen, C., H. Rambold, U. Kempermann, et al. 2002.Localizing value of torsional nystagmus in small midbrainlesions. Neurology 59: 1956–1964.

4. Brandt, T. & M. Dieterich. 1994. Vestibular syndromes in theroll plane: topographic diagnosis from brainstem to cortex.Ann. Neurol. 36: 337–347.

5. Klier, E.M., H. Wang, A.G. Constantin & J.D. Crawford.2002. Midbrain control of three-dimensional head orienta-tion. Science 295: 1314–1316.

6. Farshadmanesh, F., E.M. Klier, P. Chang, et al. 2007.Three-dimensional eye–head coordination after injection of



muscimol into the interstitial nucleus of Cajal (INC). J. Neu-rophysiol. 97: 2322–2338.

7. Kremmyda, O., S. Glasauer, T. Eggert & U. Buttner. 2008.Eye and head torsion is affected in patients with midbrainlesions. Prog. Brain Res. 171: 591–595.

8. Kremmyda, O., N. Rettinger, M. Strupp, et al. 2009. Teachingvideo neuroimages: unilateral RIMLF lesion. Pathologic eyemovement torsion indicates lesion side and site. Neurology73: e92–e93.

9. Glasauer, S., M. Hoshi, U. Kempermann, et al. 2003. Three-dimensional eye position and slow phase velocity in hu-mans with downbeat nystagmus. J. Neurophysiol. 89: 338–354.

10. Haslwanter, T. 1995. Mathematics of three-dimensional eyerotations. Vis. Res. 35: 1727–1739.

11. Glenn, B. & T. Vilis. 1992. Violations of Listing’s law afterlarge eye and head gaze shifts. J. Neurophysiol. 68: 309–318.

12. Liao, K., A.N. Kumar, Y.H. Han, et al. 2005. Comparison ofvelocity waveforms of eye and head saccades. Ann. N.Y. Acad.Sci. 1039: 477–479.

13. Bhidayasiri, R., G.T. Plant & R.J. Leigh. 2000. A hypotheticalscheme for the brainstem control of vertical gaze. Neurology54: 1985–1993.

14. Moschovakis, A.K., C.A. Scudder & S.M. Highstein. 1991.Structure of the primate oculomotor burst generator: I.Medium-lead burst neurons with upward on-directions. J.Neurophysiol. 65: 203–217.

15. Moschovakis, A.K., C.A. Scudder, S.M. Highstein & J.D.Warren. 1991. Structure of the primate oculomotor burst

generator: II. Medium-lead burst neurons with downwardon-directions. J. Neurophysiol. 65: 218–229.

16. Di Fabio, R.P., C. Zampieri & P. Tuite. 2007. Gaze-shiftstrategies during functional activity in progressive supranu-clear palsy. Exp. Brain Res. 178: 351–362.

17. Freedman, E.G. 2005. Head-eye interactions during verticalgaze shifts made by rhesus monkeys. Exp. Brain Res. 167:557–570.

18. Crawford J.D. & T. Vilis. 1992. Symmetry of oculomotorburst neuron coordinates about Listing’s plane. J. Neuro-physiol. 68: 432–448.

19. Helmchen, C., H. Rambold, L. Fuhry & U. Buttner. 1998.Deficits in vertical and torsional eye movements after uni-and bilateral muscimol inactivation of the interstitial nucleusof Cajal of the alert monkey. Exp. Brain Res. 119: 436–452.

20. Robinson, F.R., J.O. Phillips & A.F. Fuchs. 1994. Coordina-tion of gaze shifts in primates: brainstem inputs to neck andextraocular motoneuron pools. J. Comp. Neurol. 346: 43–62.

21. Horn, A.K. 2005. The reticular formation. Prog. Brain Res.151: 127–155.

22. Scudder, C.A., A.K. Moschovakis, A.B. Karabelas & S.M.Highstein. 1996. Anatomy and physiology of saccadic long-lead burst neurons recorded in the alert squirrel monkey: I.Descending projections from the mesencephalon. J. Neuro-physiol. 76: 332–352.

23. Perkins E., S. Warren & P.J. May. 2009. The mesencephalicreticular formation as a conduit for primate collicular gazecontrol: tectal inputs to neurons targeting the spinal cordand medulla. Anat. Rec. 292: 1162–1181.


effects of unilateral midbrain lesions on gaze (eye and head) movements

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