Neuroscience Letters, 118 (1990) 37~40 Elsevier Scientific Publishers Ireland Ltd.
37
NSL 07176
Eye movement-related neurons in the red nucleus J. Leiva a n d H. S a a v e d r a Departamento de Ciencias Preclinicas, Divisi6n Ciencias MOdicas Oriente, Facultad de Medicina, Universidad de Chile, Santiago (Chile)
(Received 21 December 1989; Revised version received 5 June 1990;Accepted5 June 1990) Key words." Eye movement;Red nucleus; Parvocellular neuron; Microelectrode;Cat
Extracellular unit activity of the parvocellular red nucleus (RN) and spontaneous horizontal eye movementswere recorded in adult, nitrous oxideanesthetized and C~ transected cats. It was found that 7.5% of the neurons of each RN were related to spontaneous horizontal saccadic eye movements. Three types of neurons were observed: (1) bidirectional neurons which increased their frequency of discharge in relation to any horizontal eye movement;(2) unidirectional neurons which altered their frequencyof discharge in relation to a horizontal eye movement of a precise direction; and (3) neurons which increased their frequency of discharge in relation to the rapid phase of an horizontal nystagmus. These 3 types of neurons modified their frequency of discharge before the initiation of the eye movement. One pair of oculomotor neurons recorded simultaneously in both RN showed a significant correlation coefficient. These results suggest that the RN may contribute to the preparation or execution of horizontal eye movements.
The role of the red nucleus (RN) as an integral part of the motor system has been extensively studied. There is well documented knowledge on its relation with the motor cortex, basal ganglia, thalamus, brainstem and spinal cord [2, 4, 5, 9, 12, 14-17, 20]. We did not find in the literature any report about a direct connection between the R N with eye motility. On the other hand, other structures related to the m o t o r system such as the substantia nigra (SN) and the superior colliculus (SC) possess a significant population of eye movement-related neurons [3, 8, 22]. This fact, and the known relations between the SN and the R N [1], and those which we have described between the SC and the RN [21] prompted us to do the present experimental research about eye movement-related neurons in the RN. This research was even more justified considering that R N electrical stimulation induces turning in the freely moving cat [13-19]. Ten adult cats were anaesthetized with ether; a cannula was placed inside the trachea, and a spinal section performed at Cl. The animals were artificially ventilated with a mixture of 40% N 2 0 and 60% 02. With this anesthetic mixture most animals did not present eye movements; however, with a 5% decrease in the N20 concentration the eye movements reappeared. A continuous monitoring of the E E G and E O G allowed us to control Correspondence." J. Leiva R., Departamento de Ciencias Preclinicas Oriente, Facultad de Medicina, Universidad de Chile, Casilla 16038, Santiago 9, Chile.
0304-3940/90/$ 03.50 © 1990 Elsevier ScientificPublishers Ireland Ltd.
the analgesic conditions. Besides, the borders of the surgical wounds were infiltrated with 2% lidocaine. Body temperature was maintained near 38+0.5°C using an electrical hot pad attached to the body, and was regulated by a rectal termistor. Ag-AgC1 electrodes were implanted on the orbital ridges to record horizontal eye movements. Simultaneous unitary extracellular recording of both R N were carried out through tungsten (Tg) microelectrodes having a 5-10 MI2 impedance. The microelectrodes were introduced at A 6-7 according to the atlas of Jasper and Ajmone-Marsan [11], trying to reach the most anterior or parvocellular portion of the RN. This part of the structure was selected because the magnocellular region is well known for its relation to other motor areas. The microelectrodes were lowered with the help of two micromanipulators. The AC-coupled extracellular neuronal activity was amplified using two preamplifiers (Grass Model P. 511), monitored by an oscilloscope, filtered through two spike discriminators, and its frequency of pulses displayed through an electroencephalograph (Grass Model 6, 8) simultaneously with eye movements. The records were stored in an analog tape and processed at a later period with the help of an Apple IIe microcomputer. At the end of the experiment the cats were deeply anaesthetized with Nembutal (40 mg/kg, i.p.). Through the microelectrodes two lesions were made using 300/tA, DC cathodal current for 10 s, to reconstruct the microelectrode pathway in each RN. Then the brain was per-
38
fused through the internal carotids with 10% formalin and the location of the microelectrode lesions histologically determined using tissue sections stained with Methylene blue. The animals showed mainly horizontal saccadic eye movements and occasionally oblique movements. Forty neurons were recorded in both RN, 16 in the left structure and 24 in the right. Six neurons (15%) were related to eye movements and the rest (75%) was unresponsive. The 6 eye movement-related neurons were equally distributed between both R N (see Fig. 1). They showed 3 types of relation with eye movements: (i) the first type corresponded to bidirectionally eye movements-related neurons. These cells had an average resting discharge (RD) of 1.5 + 1.16 pps (n = 19). The ocular movement to the right caused an increase in the average response rate of 14.2 + 10.1 pps (n = 19). The return of the eye to the initial position was preceded by a significant increase in the average response rate of 14.8+10.1 pps (n=19). These neurons increased their activity about 252 and 546 ms before the initiation of the eye movement (see Figs. 2,Ai and 3, A2). (ii) The second type corresponded to
t Y'.F'I
unidirectionally eye movement-related neurons found in the left RN. They had an average response rate of 38.33 + 3.7 pps (n = 14). In these neurons the movement of the eye to the right produced a strong decrease in the average response rate of 3.4 + 2.1 pps (n = 14). The correlation coefficient (CC) between both phenomena was - 0 . 8 5 and P
37
NSL 07176
Eye movement-related neurons in the red nucleus J. Leiva a n d H. S a a v e d r a Departamento de Ciencias Preclinicas, Divisi6n Ciencias MOdicas Oriente, Facultad de Medicina, Universidad de Chile, Santiago (Chile)
(Received 21 December 1989; Revised version received 5 June 1990;Accepted5 June 1990) Key words." Eye movement;Red nucleus; Parvocellular neuron; Microelectrode;Cat
Extracellular unit activity of the parvocellular red nucleus (RN) and spontaneous horizontal eye movementswere recorded in adult, nitrous oxideanesthetized and C~ transected cats. It was found that 7.5% of the neurons of each RN were related to spontaneous horizontal saccadic eye movements. Three types of neurons were observed: (1) bidirectional neurons which increased their frequency of discharge in relation to any horizontal eye movement;(2) unidirectional neurons which altered their frequencyof discharge in relation to a horizontal eye movement of a precise direction; and (3) neurons which increased their frequency of discharge in relation to the rapid phase of an horizontal nystagmus. These 3 types of neurons modified their frequency of discharge before the initiation of the eye movement. One pair of oculomotor neurons recorded simultaneously in both RN showed a significant correlation coefficient. These results suggest that the RN may contribute to the preparation or execution of horizontal eye movements.
The role of the red nucleus (RN) as an integral part of the motor system has been extensively studied. There is well documented knowledge on its relation with the motor cortex, basal ganglia, thalamus, brainstem and spinal cord [2, 4, 5, 9, 12, 14-17, 20]. We did not find in the literature any report about a direct connection between the R N with eye motility. On the other hand, other structures related to the m o t o r system such as the substantia nigra (SN) and the superior colliculus (SC) possess a significant population of eye movement-related neurons [3, 8, 22]. This fact, and the known relations between the SN and the R N [1], and those which we have described between the SC and the RN [21] prompted us to do the present experimental research about eye movement-related neurons in the RN. This research was even more justified considering that R N electrical stimulation induces turning in the freely moving cat [13-19]. Ten adult cats were anaesthetized with ether; a cannula was placed inside the trachea, and a spinal section performed at Cl. The animals were artificially ventilated with a mixture of 40% N 2 0 and 60% 02. With this anesthetic mixture most animals did not present eye movements; however, with a 5% decrease in the N20 concentration the eye movements reappeared. A continuous monitoring of the E E G and E O G allowed us to control Correspondence." J. Leiva R., Departamento de Ciencias Preclinicas Oriente, Facultad de Medicina, Universidad de Chile, Casilla 16038, Santiago 9, Chile.
0304-3940/90/$ 03.50 © 1990 Elsevier ScientificPublishers Ireland Ltd.
the analgesic conditions. Besides, the borders of the surgical wounds were infiltrated with 2% lidocaine. Body temperature was maintained near 38+0.5°C using an electrical hot pad attached to the body, and was regulated by a rectal termistor. Ag-AgC1 electrodes were implanted on the orbital ridges to record horizontal eye movements. Simultaneous unitary extracellular recording of both R N were carried out through tungsten (Tg) microelectrodes having a 5-10 MI2 impedance. The microelectrodes were introduced at A 6-7 according to the atlas of Jasper and Ajmone-Marsan [11], trying to reach the most anterior or parvocellular portion of the RN. This part of the structure was selected because the magnocellular region is well known for its relation to other motor areas. The microelectrodes were lowered with the help of two micromanipulators. The AC-coupled extracellular neuronal activity was amplified using two preamplifiers (Grass Model P. 511), monitored by an oscilloscope, filtered through two spike discriminators, and its frequency of pulses displayed through an electroencephalograph (Grass Model 6, 8) simultaneously with eye movements. The records were stored in an analog tape and processed at a later period with the help of an Apple IIe microcomputer. At the end of the experiment the cats were deeply anaesthetized with Nembutal (40 mg/kg, i.p.). Through the microelectrodes two lesions were made using 300/tA, DC cathodal current for 10 s, to reconstruct the microelectrode pathway in each RN. Then the brain was per-
38
fused through the internal carotids with 10% formalin and the location of the microelectrode lesions histologically determined using tissue sections stained with Methylene blue. The animals showed mainly horizontal saccadic eye movements and occasionally oblique movements. Forty neurons were recorded in both RN, 16 in the left structure and 24 in the right. Six neurons (15%) were related to eye movements and the rest (75%) was unresponsive. The 6 eye movement-related neurons were equally distributed between both R N (see Fig. 1). They showed 3 types of relation with eye movements: (i) the first type corresponded to bidirectionally eye movements-related neurons. These cells had an average resting discharge (RD) of 1.5 + 1.16 pps (n = 19). The ocular movement to the right caused an increase in the average response rate of 14.2 + 10.1 pps (n = 19). The return of the eye to the initial position was preceded by a significant increase in the average response rate of 14.8+10.1 pps (n=19). These neurons increased their activity about 252 and 546 ms before the initiation of the eye movement (see Figs. 2,Ai and 3, A2). (ii) The second type corresponded to
t Y'.F'I
unidirectionally eye movement-related neurons found in the left RN. They had an average response rate of 38.33 + 3.7 pps (n = 14). In these neurons the movement of the eye to the right produced a strong decrease in the average response rate of 3.4 + 2.1 pps (n = 14). The correlation coefficient (CC) between both phenomena was - 0 . 8 5 and P
