Effects of lesion of pontomedullary reticular formation on visually triggered vertical and oblique head orienting movements in alert cats

Neuroscience Letters 265 (1999) 13–16

Effects of lesion of pontomedullary reticular formation on visually triggered vertical and oblique head orienting movements in alert cats Shigeto Sasaki a ,*, Tadashi Isa b, Kimisato Naito a a

Department of Neurophysiology, Tokyo Metropolitan Institute for Neuroscience, 2–6 Musashidai, Fuchu-shi, Tokyo 183–8526, Japan b Department of Integrative Physiology, National Institute for Physiological Sciences, Myodaiji Okazaki 444–8585, Japan Received 2 February 1999; received in revised form 15 February 1999; accepted 15 February 1999

Abstract The role of the nucleus reticularis pontis caudalis (NRPC) and the nucleus reticularis gigantocellularis (NRG) in control of vertical and oblique head orienting movements was investigated in alert cats by lesion of these nuclei with kainic acid. Cats were trained to orient the head vertically or obliquely to various targets. Following unilateral lesion of these nuclei, vertical orienting could be performed correctly with a slight decrease in velocity, while oblique orienting tended to exhibit zigzag course because of severe impairment of horizontal orienting. The horizontal and vertical components became coordinated in the course of experiments due to a significant decrease in vertical component velocity, resulting in smooth oblique trajectories. Results suggest that horizontal and vertical components of head orienting are controlled separately, but impairment of horizontal component causes adaptive change of vertical component velocity in oblique orienting.  1999 Elsevier Science Ireland Ltd. All rights reserved.

Keywords: Head orienting; Vertical head rotation; Oblique head rotation; Pontomedullary reticular formation; Kainic acid lesion; Cat

When an object appears in the visual field, animals rapidly move the eyes and the head in the same direction to look at the object (orienting movements). The superior colliculus is a crucial structure for generation of orienting movements. Regarding the head orienting, pathways from the superior colliculus to neck motoneurons have been extensively studied in the cat [1–4,6,14,15,17]. There are two major routes from the superior colliculus to neck motoneurons: one is through reticulospinal neurons (RSNs) in the nucleus reticularis pontis caudalis (NRPC) and the nucleus reticularis gigantocellularis (NRG) [1–3,14,15] and the other through the Forel’s field H (FFH) in the rostral mesencephalic reticular formation [7,12,13]. Neck motoneurons innervating lateral head flexors receive dense projection from RSNs in the NRPC and the NRG but rarely from FFH neurons, whereas head elevator motoneurons receive both disynaptic and monosynaptic excitation from FFH neu* Corresponding author. Tel.: +81-423-25-3881 ext. 4216; fax: +81423-21-8678.

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rons [13]. A burst of spikes is generated in pontine RSNs in association with synergic eye and head movements in horizontal orienting [6,10] and in FFH neurons in association with vertical eye and head movements [9]. These findings imply that the NRPC and NRG would participate in control of horizontal head movements and the FFH would concern vertical head movements. However, the dichotomy of neural elements for horizontal and vertical head movements may not be strict, and the NRPC and the NRG may in part be involved in control of vertical head movements, because RSNs in the NRG project to both lateral head flexor and elevator motoneurons with almost the same density of synaptic contact [14] and FFH neurons send axon collaterals to the NRPC and NRG [12]. A previous study [11], showed that lesion of the NRPC and NRG produced severe impairment of horizontal head orienting. The present study aims at elucidating the functional role of the NRPC and NRG in vertical and oblique head orienting by quantitatively analyzing behavioral impairment after lesion of these structures. The impairment will be evaluated on the basis of so far

 1999 Elsevier Science Ireland Ltd. All rights reserved.

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S. Sasaki et al. / Neuroscience Letters 265 (1999) 13–16

verified neural connections of the pontomedullary reticular formation. Experiments were performed in six adult trained cats. The training procedures and surgery for attaching recording system were similar to those described previously [11]. Briefly, the cat stood in front of a perimeter screen and freely rotated the head. On the perimeter an array of 17 light-emitting diodes (LEDs) was placed. The cat was trained to fixate the center LED and orient the head to a new target to get a reward, each LED being aligned vertically and horizontally. Two pairs of Ag-AgCl electrodes were implanted in the temporal and frontal bones under pentobarbital anesthesia to record horizontal and vertical eye movements. Head position was recorded by a position sensor system (Hamamatsu Photonics). Two infra-red LEDs, separated by 8 cm, were attached to a socket on the head and aligned along the mid-sagittal axis of the head in parallel with the horizontal plane in Horsley–Clarke coordinates. The positions of the two head LEDs were recorded by two cameras and stored on a tape recorder for off-line analysis using a computer. Angular velocity of head rotation was calculated from the trajectory in every 10-ms interval. After collecting control data, the NRPC and the NRG were lesioned on the right side by kainic acid injections (0.1%, 3–6 ml, dissolved with 10% gelatin in saline to minimize diffusion) under deep anesthesia. Behavioral experiments began 1–3 days after the lesion.

After the experiments were completed, the animal was killed under deep anesthesia, and the extent of the lesion (cell loss) was studied histologically. In transverse sections, cells disappeared completely in most part of the NRPC and NRG confined to the injected side (Fig. 1C). In parasagittal planes, the lesion extended from the NRPC to the rostral half of the NRG (Fig. 1C). Care and experimental manipulation of animals were in accord with the guidelines of the Physiological Society of Japan. The cat first looked at the center LED and, when a target LED appeared in the upper or lower visual field on the same vertical plane, directed the head to the target. The line connecting LED 1 and LED 2 on the head will be called ‘head axis’ and its projection to the perimeter ‘head orienting point’. Fig. 1A shows that the head axis rotated downward with almost no horizontal rotation. Fig. 1B shows time courses of head angle and angular velocity associated with vertical head orienting together with vertical eye movements. When the animal oriented to different targets, maximum angular velocity increased with an increase in the amplitude of head rotation. Regression analysis indicated that the two parameters were significantly correlated (Fig. 1E, open circles, P , 0.001). After lesion of the NRPC and NRG, the head was slightly deviated to the intact side at the fifth postoperative day (Fig. 1Db), but the cat could direct the head correctly to the target LED (Fig. 1Da) with con-

Fig. 1. Effects of lesion of the NRPC and NRG on vertical head orienting. (A) Rotation of the head axis before lesion. (a) View in sagittal plane; (b) view in horizontal plane; (c) frontal view of trajectory of head orienting points. In this and other head axis records, filled circle indicates head orienting point before starting movement and open circle at the end of movement. Arrows indicate direction of rotation. (B) Time course of head angle (top), angular velocity (middle) and eye movements (bottom) before lesion. Calibration: 20 deg for head angle and 100 deg/s for head velocity. (C) Parasagittal (left) and frontal (right three) sections of the brainstem, showing the lesion (shaded area) confirmed by cell loss. G, genu facialis; IO, inferior olive; TB, trapezoid body; VI, abducens nucleus. (D) Rotation of the head axis 5 days after lesion. Same arrangement of records as in (A). (E) Relationship between maximum angular velocity and amplitude of vertical rotation. Open and filled circles indicate data before and after lesion, respectively.

S. Sasaki et al. / Neuroscience Letters 265 (1999) 13–16

comitant small horizontal rotation to the lesioned side (Fig. 1Db). After the tenth postoperative day, the sustained head deviation decreased, and vertical head orienting was almost undistinguishable from that in the intact cat. Similar findings were obtained in all of six cats: i.e. they could perform vertical head rotation in the tonically deviated vertical plane or in the mid-sagittal plane after recovery from tonic head deviation. The relationship between maximum angular velocity and amplitude of vertical head rotation after the lesion was compared with that before the lesion (Fig. 1E). The mean slope of the regression line for six cats was 3.99 ± 1.10 (SD) deg/s per deg before and 3.16 ± 0.43 deg/s per deg after the lesion. Thus, the head angular velocity tended to decrease after the lesion, though the difference was statistically not significant (P . 0.1, t-test). This was in contrast with a highly significant decrease (P , 0.001) in the slope of regression line for horizontal head orienting after the lesion (6.12 ± 1.93 deg/s per deg before vs. 2.59 ± 0.49 deg/s per deg after the lesion). Fig. 2A shows vertical (a) and horizontal (b) components of head rotation in the right-down orienting in control records. Properties of the vertical and horizontal components were almost the same as those observed in pure vertical (Fig. 1Aa) and pure horizontal [11] orienting. The smooth oblique course of head orienting point (Fig. 2Ac) indicated that the vertical and horizontal components were well coordinated. After lesion of the NRPC and NRG, the trajectory of oblique movements to the lesioned side often

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showed a zigzag course shortly after the lesion because of severe impairment of horizontal head rotation [11] and only slight effects on vertical head rotation. In the course of experiments, vertical and horizontal components gradually became coordinated (Fig. 2Bc), and the vertical component of head rotation could attain the vertical level of target (Fig. 2Ba). Vertical and horizontal components were adjusted by the quasi-parallel horizontal shift of the head with small rotation component (Fig. 2Bb), which enabled the head orienting point to attain the target relatively smoothly. Fig. 2C,D show regression lines for the relationship between maximum head angular velocity and amplitude of head rotation for vertical (Fig. 2C) and horizontal (Fig. 2D) components before (solid lines) and after (dotted lines) lesion in six cats. The mean slope of the regression line for vertical component was 4.85 ± 0.15 deg/s per deg before and 3.12 ± 0.72 deg/s per deg after the lesion, the difference being statistically significant (P , 0.01). There was also highly significant difference between the mean slopes for horizontal component before and after the lesion; 6.05 ± 1.27 vs. 2.55 ± 0.85 deg/s per deg (P , 0.001). Thus, the decrease in the slope after the lesion was found for both vertical and horizontal components, though less remarkable for vertical than for horizontal component. The present study shows that vertical head rotation is preserved after NRPC and NRG lesion which produces severe impairment of horizontal head rotation. In contrast, vertical head rotation is severely impaired by lesion of the

Fig. 2. Effects of lesion of the NRPC and NRG on oblique head orienting. (A) Rotation of the head axis in the right-down direction before lesion. (a–c) Same arrangement of records as in A. (B) Rotation of the head axis 8 days after lesion. Same arrangement of records as in A. (C) Regression lines for the relation between the maximum angular velocity of vertical component and the amplitude of vertical component before (solid lines) and after lesion (dotted lines) for six cats. Numerals indicate the cat number. (D) Regression lines for the horizontal component. Same arrangement as in (C).

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FFH [8]. These findings suggest that there are distinct control systems for horizontal and vertical head rotation. Masino and Knudsen [16] have also suggested that distinct neural circuits control horizontal and vertical components of head movements in the barn owl. However, the NRPC and NRG probably participate to some extent in control of vertical head rotation as well, since FFH neurons project to head elevator motoneurons via the NRPC and NRG in addition to the direct FFH-spinal pathway [12,13]. The slight decrease in head velocity in pure vertical orienting after the lesion is probably caused by elimination of indirect FFHspinal projection. The significant decrease of vertical component velocity in oblique orienting appeared to be caused by other mechanisms than elimination of NRPC-NRG pathway: i.e. in oblique head movements, horizontal and vertical components are interrelated and impairment of the former may cause adaptive changes of the latter as suggested for oblique saccadic eye movements [5]. The authors wish to express their gratitude to Professor T. Hongo for critical comments on the manuscript. This study was supported by grants from the Ministry of Education, Science, Sports and Culture of Japan. [1] Alstermark, B., Pinter, M. and Sasaki, S., Tectal and tegmental excitation in dorsal neck motoneurones of the cat, J. Physiol. (Lond.), 454 (1992) 517–532. [2] Alstermark, B., Pinter, M. and Sasaki, S., Descending pathway mediating disynaptic excitation on dorsal neck motoneurones in the cat: facilitatory interactions, Neurosci. Res., 15 (1992) 32– 41. [3] Alstermark, B., Pinter, M. and Sasaki, S., Descending pathway mediating disynaptic excitation on dorsal neck motoneurones in the cat: brainstem relay, Neurosci. Res., 15 (1992) 42– 57. [4] Anderson, M.E., Yoshida, M. and Wilson, V.J., Influence of superior colliculus on cat neck motoneurons, J. Neurophysiol., 34 (1971) 898–907. [5] Evinger, C., Kaneko, C.R.S. and Fuchs, A.F., Oblique saccadic

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