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Receptive field response of LGB neurons during vestibular stimulation in awake cats
Vision Res. Vol. 16, pp.
11%120. Pergamon Press 1976. Printed in Great Britain.
LETTER RECEPTIVE FIELD DURING VESTIBULAR
TO THE EDITOR RESPONSE OF LGB NEURONS STIMULATION IN AWAKE CATS
(Received
It has been clearly demonstrated that spontaneous activity in the dorsal nucleus of the lateral geniculate body (LGB) is modified by vestibular stimulation, in acute preparations (Grusser, GrusserComhels and Saur, 1959; Kornhuber and da Fonseca, 1964; Papaioannou, 1%9), as well as in fully awake cats (Magnin, Jeannerod and Putkonen, 1974). The precise role of this vestibular influence on the visual system, in the process of visuovestibular integration, is not fully understood. In the present experiment, we have tried to study the influence of vestibular stimulation on the response of the LGB neurons to visual stimuli within their receptive field. For this purpose, we used a chronic preparation where the retina was kept stationary with respect to the visual world, in spite of rotating the animal, and in spite of the eye movements which normally occur in response to rotation. Normal adult cats, in which one eye was surgically paralyzed, by a section of the three oculomotor nerves on one side were used (Berlucchi, Munson and Rizzolatti, 1966). Electrodes monitoring the position of the unparalyzed eye were implanted, together with a head-fixation device (Magnin and Jeannerod, 1973). During experimental sessions, the cat was secured to a hammock and placed with the head centered in a light-tight rotating cylinder. That the cat was in no pain was evident from that fact that the hammock could be supported up to 5 hr. At the beginning of each session, the optic disk of the paralyzed eye was projected onto the inner wall of the cylinder by means of an ophthalmoscope. This procedure allowed us to be certain of the perfect stability of the paralyzed eye, and eventually to reject the animal when slight eye movements began to reappear (usually 4-5 weeks after surgery). It also permitted the position and extent of the receptive fields to be mapped with respect to the fovea. Optical correction was made by means of a +2D spectacle lens. Stationary spots of light were projected onto the inner wall of the cylinder, which rotated with the animal. Spots of 0.4’ were used for pure center stimulation of the receptive field, and spots up to 15’ for center-surround stimulation. Interjection of a shutter system in the light beam allowed receptive field stimulation times to be varied. The exact duration of light stimulation was determined by the response of a photocell. Rotation of the cylinder and of the animal in the horizontal plane was carried out to right and left (frequency of altemation, 0.025-O-25 Hz). Mean angular velocity could be varied between 10 and 150deg/sec. Single cell
17 &lay 1975)
responses were recorded by means of glassinsulated platinum electrodes (impedence 2 MfJ), and recorded along with photocell signal, eye position, and cylinder position on FM tape for subsequent data processing on a PDP 8 computer. Histograms of receptive field response in the stationary condition (before rotation), and during vestibular stimulation were constructed. The use of the fully awake animal, added to the highly dynamic nature of the stimulation made it difficult to characterize a large number of neurons. Nevertheless, there appears to be a significant modification of the receptive field response in 20 of the 27 LGB cells successfully recorded. Consideration of the sustained or transient nature of the response both in the subsequently obtained histogram and during the experiment has enabled us to make a gross classification of the cells as being either X (e.g. Fig. 1C) or Y (e.g. Fig. 1A and B). More formal tests were not carried out as the protocole was already highly charged. Of the 13 X type cells recorded, seven showed a modified response to flashing spots during rotation; five showed an increased, and one a decreased center response (Fig. 1C). Of the 14 Y types ceils recorded, 10 showed a modified response during rotation, five increased (Fig. IB). and five decreased (Fig. IA) their center response. Spontaneous activity was modified by rotation in seven of the 27 cells. For instance, cells shown in Figs. 1A and 2A show a clear increase in background rate during rotation. However, spontaneous activity and receptive field response were not always modified in an identical manner, i.e.. the response modification could be asymmetrical (e.g. increase in spontaneous activity and no change in receptive field response as shown in Fig. 2A and modification of receptive field response with no change in spontaneous activity as shown in Fig. 10 This occurred in 11 cases (six X types, five Y types). In three cells, vestibular stimulation was seen to act on the center-surround balance. One example is shown in Fig. 2. During pure center stimulation, rotation is seen only to increase the spontaneous activity, although the center response remains constant. Stimulation of the surround in the stationary condition results in an inhibition of the center response: in this case, rotation is seen to suppress surround inhibition of the center response (Fig. 2B, right). Our results confirm those obtained by Papaioannou (1972), on acute preparations. We have striven to retain experimental conditions in which the cat is 119
120
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Laboratoire de Neuropsychologie Exptfrimentale, INSEAM, Unite’ 94, 69500 Bron, France
Fig. 1. Vestibular modification of pure center response. A: Y “OFF-center” cell. B: Y “ON-center” cell. C: X “ON-center” cell. Post stimulus time histograms. Heavy line on lower trace indicates photo cell response. Before
Rotation
to the LGB via the reticular network. a certain degree of specificity is retained. We have been able to demonstrate that the modification of the LGB activity by velocity steps, has a definite relationship with the accompanying vestibulo-ocular response (Kennedy and Jeannerod, in preparation). In fact, these vestibular effects on the LGB cells are more complex than those obtained by Meulders and Godfraind (1%9), using somatic stimulation, where a dilatation of the receptive field occurs. The dissociation that we found (in confirmation of Papaioannou’s findings) between the change in background activity and the change in response of the receptive field, clearly indicates that the dynamics of the receptive fields are modified. These changes result in either an increased or decreased center response, or in a readjustment of the mechanisms generating the center-surround response, giving rise to a modification of the balance. This can be interpreted either in spatial terms, i.e. as an expansion of the center response, as Meulders and Godfraind (1969) reported with somatic stimulation, or in terms of responsiveness.
During
Rotation
4OOms
07
0-
4OOms
0-
I
400ms
400ms
Fig. 2. Vestibular modification of center-surround balance in a “ON-center” Y cell. A: Pure center response. B: Center + surround.
physiologically intact. There is no doubt that there is a vestibular modulation of visual response in the LGB. It does not seem necessary to stipulate to what degree what we call vestibular modulation of the light response, is mediated by vestibulogeniculate pathways, or by the brainstem reticular formation. However, we feel that even if the information from the vestibular receptors is transmitted
&f. MAGNIN
M. JEANNEROD
REFERENCES Berlucchi G.. Munson J. B. and Rizzolatti G. (1966) Surgical immobilization of the eye and pupil permitting stable photic stimulation of freely moving cats. Electroenceph. c/in. Neurophysiol. 21, 504-505. Grusser 0. J., Grusser-Cornhels U. and Saur G. (1959) Reaktionen einzelner Neurone im optischen Cortex der
A’6L16L 0-
H. KENNEDY
Katze nach electrischer Polarisation des Labyrinths.
Pj?iigers Arch. ges. Physiol. LJ9, 593-612. Komhuber H. H. and da Fonseca J. J. (1964) Optovestibular integration in the cat cortex. A study of sensory convergence on cortical neurones. In The Oculomotor System (Edited by Bender M. B.), pp. 239-279. Harper & Row, New York. Magnin M. and Jeannerod M. (1973) Fixation non traumatique de la tete chez le chat eveill& C. r. SPanc. Sot. Biol. 167, 996-999. Magnin IM., Jeannerod M. and Putkonen P. T. S. (1974) Vestibular and saccadic influences on dorsal and ventral nuclei of the lateral geniculate body. Expl Brain Res. 21, I-18. Meulders M. and Godfraind J. M. (1969) Influence du rtveil d’origine reticulaire sur I.&endue des champs visuels des neurones de la region genouillie chez le chat avec cereau intact et avec cerveau isoli. Expl Brain Res. 9, 201-220. Papaioannou J. (1%9) Vestibular influences on the spontaneous activity of neurones in the lateral geniculate nucleus of the cat. .I. Physiol., Lond. 202, 86P. Papaioannou J. N. (1972) Electrical stimulation of vestibular nuclei: effects on light evoked activity of lateral geniculate neurones. Pfliigers Arch. ges. Physiol. 334, 129-140. Papaioannou J. N. (1973) Changes in the light evoked discharges from lateral geniculate nucleus neurones in the cat, induced by caloric labyrinthine stimulation. Expl Brain Res. 17, 10-17.
11%120. Pergamon Press 1976. Printed in Great Britain.
LETTER RECEPTIVE FIELD DURING VESTIBULAR
TO THE EDITOR RESPONSE OF LGB NEURONS STIMULATION IN AWAKE CATS
(Received
It has been clearly demonstrated that spontaneous activity in the dorsal nucleus of the lateral geniculate body (LGB) is modified by vestibular stimulation, in acute preparations (Grusser, GrusserComhels and Saur, 1959; Kornhuber and da Fonseca, 1964; Papaioannou, 1%9), as well as in fully awake cats (Magnin, Jeannerod and Putkonen, 1974). The precise role of this vestibular influence on the visual system, in the process of visuovestibular integration, is not fully understood. In the present experiment, we have tried to study the influence of vestibular stimulation on the response of the LGB neurons to visual stimuli within their receptive field. For this purpose, we used a chronic preparation where the retina was kept stationary with respect to the visual world, in spite of rotating the animal, and in spite of the eye movements which normally occur in response to rotation. Normal adult cats, in which one eye was surgically paralyzed, by a section of the three oculomotor nerves on one side were used (Berlucchi, Munson and Rizzolatti, 1966). Electrodes monitoring the position of the unparalyzed eye were implanted, together with a head-fixation device (Magnin and Jeannerod, 1973). During experimental sessions, the cat was secured to a hammock and placed with the head centered in a light-tight rotating cylinder. That the cat was in no pain was evident from that fact that the hammock could be supported up to 5 hr. At the beginning of each session, the optic disk of the paralyzed eye was projected onto the inner wall of the cylinder by means of an ophthalmoscope. This procedure allowed us to be certain of the perfect stability of the paralyzed eye, and eventually to reject the animal when slight eye movements began to reappear (usually 4-5 weeks after surgery). It also permitted the position and extent of the receptive fields to be mapped with respect to the fovea. Optical correction was made by means of a +2D spectacle lens. Stationary spots of light were projected onto the inner wall of the cylinder, which rotated with the animal. Spots of 0.4’ were used for pure center stimulation of the receptive field, and spots up to 15’ for center-surround stimulation. Interjection of a shutter system in the light beam allowed receptive field stimulation times to be varied. The exact duration of light stimulation was determined by the response of a photocell. Rotation of the cylinder and of the animal in the horizontal plane was carried out to right and left (frequency of altemation, 0.025-O-25 Hz). Mean angular velocity could be varied between 10 and 150deg/sec. Single cell
17 &lay 1975)
responses were recorded by means of glassinsulated platinum electrodes (impedence 2 MfJ), and recorded along with photocell signal, eye position, and cylinder position on FM tape for subsequent data processing on a PDP 8 computer. Histograms of receptive field response in the stationary condition (before rotation), and during vestibular stimulation were constructed. The use of the fully awake animal, added to the highly dynamic nature of the stimulation made it difficult to characterize a large number of neurons. Nevertheless, there appears to be a significant modification of the receptive field response in 20 of the 27 LGB cells successfully recorded. Consideration of the sustained or transient nature of the response both in the subsequently obtained histogram and during the experiment has enabled us to make a gross classification of the cells as being either X (e.g. Fig. 1C) or Y (e.g. Fig. 1A and B). More formal tests were not carried out as the protocole was already highly charged. Of the 13 X type cells recorded, seven showed a modified response to flashing spots during rotation; five showed an increased, and one a decreased center response (Fig. 1C). Of the 14 Y types ceils recorded, 10 showed a modified response during rotation, five increased (Fig. IB). and five decreased (Fig. IA) their center response. Spontaneous activity was modified by rotation in seven of the 27 cells. For instance, cells shown in Figs. 1A and 2A show a clear increase in background rate during rotation. However, spontaneous activity and receptive field response were not always modified in an identical manner, i.e.. the response modification could be asymmetrical (e.g. increase in spontaneous activity and no change in receptive field response as shown in Fig. 2A and modification of receptive field response with no change in spontaneous activity as shown in Fig. 10 This occurred in 11 cases (six X types, five Y types). In three cells, vestibular stimulation was seen to act on the center-surround balance. One example is shown in Fig. 2. During pure center stimulation, rotation is seen only to increase the spontaneous activity, although the center response remains constant. Stimulation of the surround in the stationary condition results in an inhibition of the center response: in this case, rotation is seen to suppress surround inhibition of the center response (Fig. 2B, right). Our results confirm those obtained by Papaioannou (1972), on acute preparations. We have striven to retain experimental conditions in which the cat is 119
120
LettertotheEditor Beforc
OwngRotallon
Rotatml
I
,
‘9
16-
I
Ol-
N50
d
agOms
450ms
I
N50
I.
45Oms
N 49 16
16
i
lllihk-L
Laboratoire de Neuropsychologie Exptfrimentale, INSEAM, Unite’ 94, 69500 Bron, France
Fig. 1. Vestibular modification of pure center response. A: Y “OFF-center” cell. B: Y “ON-center” cell. C: X “ON-center” cell. Post stimulus time histograms. Heavy line on lower trace indicates photo cell response. Before
Rotation
to the LGB via the reticular network. a certain degree of specificity is retained. We have been able to demonstrate that the modification of the LGB activity by velocity steps, has a definite relationship with the accompanying vestibulo-ocular response (Kennedy and Jeannerod, in preparation). In fact, these vestibular effects on the LGB cells are more complex than those obtained by Meulders and Godfraind (1%9), using somatic stimulation, where a dilatation of the receptive field occurs. The dissociation that we found (in confirmation of Papaioannou’s findings) between the change in background activity and the change in response of the receptive field, clearly indicates that the dynamics of the receptive fields are modified. These changes result in either an increased or decreased center response, or in a readjustment of the mechanisms generating the center-surround response, giving rise to a modification of the balance. This can be interpreted either in spatial terms, i.e. as an expansion of the center response, as Meulders and Godfraind (1969) reported with somatic stimulation, or in terms of responsiveness.
During
Rotation
4OOms
07
0-
4OOms
0-
I
400ms
400ms
Fig. 2. Vestibular modification of center-surround balance in a “ON-center” Y cell. A: Pure center response. B: Center + surround.
physiologically intact. There is no doubt that there is a vestibular modulation of visual response in the LGB. It does not seem necessary to stipulate to what degree what we call vestibular modulation of the light response, is mediated by vestibulogeniculate pathways, or by the brainstem reticular formation. However, we feel that even if the information from the vestibular receptors is transmitted
&f. MAGNIN
M. JEANNEROD
REFERENCES Berlucchi G.. Munson J. B. and Rizzolatti G. (1966) Surgical immobilization of the eye and pupil permitting stable photic stimulation of freely moving cats. Electroenceph. c/in. Neurophysiol. 21, 504-505. Grusser 0. J., Grusser-Cornhels U. and Saur G. (1959) Reaktionen einzelner Neurone im optischen Cortex der
A’6L16L 0-
H. KENNEDY
Katze nach electrischer Polarisation des Labyrinths.
Pj?iigers Arch. ges. Physiol. LJ9, 593-612. Komhuber H. H. and da Fonseca J. J. (1964) Optovestibular integration in the cat cortex. A study of sensory convergence on cortical neurones. In The Oculomotor System (Edited by Bender M. B.), pp. 239-279. Harper & Row, New York. Magnin M. and Jeannerod M. (1973) Fixation non traumatique de la tete chez le chat eveill& C. r. SPanc. Sot. Biol. 167, 996-999. Magnin IM., Jeannerod M. and Putkonen P. T. S. (1974) Vestibular and saccadic influences on dorsal and ventral nuclei of the lateral geniculate body. Expl Brain Res. 21, I-18. Meulders M. and Godfraind J. M. (1969) Influence du rtveil d’origine reticulaire sur I.&endue des champs visuels des neurones de la region genouillie chez le chat avec cereau intact et avec cerveau isoli. Expl Brain Res. 9, 201-220. Papaioannou J. (1%9) Vestibular influences on the spontaneous activity of neurones in the lateral geniculate nucleus of the cat. .I. Physiol., Lond. 202, 86P. Papaioannou J. N. (1972) Electrical stimulation of vestibular nuclei: effects on light evoked activity of lateral geniculate neurones. Pfliigers Arch. ges. Physiol. 334, 129-140. Papaioannou J. N. (1973) Changes in the light evoked discharges from lateral geniculate nucleus neurones in the cat, induced by caloric labyrinthine stimulation. Expl Brain Res. 17, 10-17.