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Influence of brain stem oculomotor area stimulation on single unit activity in the visual cortex. Mathematical analysis of results
SHORT COMMUNICATIONS
351
Influence of brain stem oculomotor area stimulation on single unit activity in the visual cortex. Mathematical analysis of results Eye movements exert a three-fold influence on vision: first, blurring of the retinal image as a consequence of relative retinal movement; secondly, stimulation of the proprioceptors of the extrinsic ocular muscles; and, finally, activation of a central loop connecting oculomotor and visual centers. The latter neural activity is postulated to be the mechanism responsible for visual stability during eye movements2 and visual suppression during saccades 6. According to Hyde and Eliason 5 and to Bender and Shanzer t there are oculomotor areas in the anterior brain stem. Our experiments aimed to elucidate some aspects of the unitary processes in the connections b~tween these areas (dorsal and ventral tegmentum and anterior pons) and the visual cortex. In enc6phale isol6 cats, electrodes were introduced into various brain stem areas, whose stimulation elicited definite conjugated eye movements in different directions. After curarizing the animal with both D-tubocurarine and gallamine triiodoethylate (Flaxedil) and after thorough control of the absence of any eye movement, the receptive field and the optimal direction sensitivity of striate and parastriate neurons upon a slit (a narrow rectangle, 0.3 ° × 12°, of light), to and fro moving in different directions on a screen facing the animal, were determined. Subsequently the slit-evoked neural activity and its changes upon stimulation of the various oculomotor brain stem areas, but in the absence of any eye movement, were recorded. Mathematical analysis. The first step of the mathematical analysis was the computation of the tape-recorded 'raw data' per stimulation condition into time histograms (200 addresses/16 min of a complete to-and-fro slit movement) and their conversion to digital values, i.e. number of discharges per address for a given number of sweeps. The next step was the conversion of the response pattern into a sequence of (positive and/or negative) 'peaks' by isolating the addresses containing a number of discharges significantly deviating from the mean discharge rate, by grouping the successive addresses containing positive or negative deviations into peaks and by calculating for each peak the mean discharge frequency and the mean frequency of the addresses outside all peaks; the latter value was considered to be the mathematical expression of the 'noise' of the unit, whereas the former values were to be related to this noL,e value in order to yield a mathematical expression of the peak's 'information value' (I). The information value of a peak was defined as:
(F i - F o) ni I=
(1)
where ni is the peak interval, i.e. the number of addresses grouped in the peak, Ft the mean frequency of the peak and Fo the mean frequency outside the peaks (defined as noise): Brain Research, 17 (1970) 351-354
352
SHORT COMMUNICATIONS
(2) I1 i
Fo
=
~ _ F°
_
(3)
1]o
no being the number of addresses outside the peaks. When N is the total number of addresses, no = N -
Y~ni
(4)
The l-formula (1) is a combination of 3 essential operations: (1) The difference in absolute values between the mean peak frequency and the noise frequency: this is justified by the facts that the peak also contains noise and that the 1 of a peak is its differentiation from the noise values and not its absolute value. (2) The multiplication of this difference by the peak interval for a surface is a more adequate description of a peak than its mere height. (3) The division of this product by the noise frequency, taking into account that a peak of a given surface does not contain the same information when the noise is low or high: moreover the latter operation standardizes the I with respect to the noise and allows interunit comparisons. The I-formula takes into account some aspects of the presently accepted hypothesis that information is carried along neurons as 'positive peaks', i.e. significant increases of discharge frequency. Indeed, since in the first operation the difference in absolute values is made between the mean peak frequency and the noise frequency, the I of a negative peak is limited by the noise level, whereas the I of a positive peak is (theoretically) illimited (practically by the maximal discharge frequency of the neuron). Information transmission by significant negative peaks presupposes a high level of noise, i.e. wasted cellular activity; further, small variations of the mean peak frequency entail enormous I-fluctuations. Therefore, positive peaks are more economic and more redundant. The specific function of the negative peak might be to delimit sharply the duration of the information transmission by a positive peak to an excitatory or inhibitory synaptic connection. (It should be remembered, however, that negative peaks are partly due to experimental artifacts, since, in case of visual neurons, they are converted to positive peaks when stimulating by a dark bar instead of a slit.) Results and comments. As a preliminary remark it may be stated that the results obtained are in good agreement with those of Hubel and Wiesel 3,4, with respect to the receptive fields of the visual neurons, and with those of Hyde and Eliason 5 and Bender and Shanzer 1, with respect to the ocular deviations elicited by brain stem stimulation. Concerning the main topic of our research, namely the influence of brain stem oculomotor areas on striate and parastriate neurons, a typical example is neuron 1I/9-6 (Fig. 1), which also illustrates the valuable use of the I-formula for extracting signals out of random activity, when the latter consists of discrete events. This neuron Brain Research, 17 (1970) 351-354
SHORT COMMUNICATIONS Cell]1/9-6 A
v i s u a l cortex : a r e a l 8
rr
••
'°°
-
:'.,;::-.,';, ..
[]
L~
~a~.
Receptive fietd
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"
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,,c d
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/"!
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: "'.
I " "
20T'rnformation Vatue
1.800~J. ,,weep
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50
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4Tznformation Vatue 3£R'7 t d£a ................. ...."'" ""'"-..
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Fig. 1. For explanation see text. Abbreviations: CI, colliculus inferior; CS, colliculus superior; Fr, firing rate; GL, corpus geniculatum lateral°; GM, corpus geniculatum mediale; I, information value; LM, lemniscus medialis; Py, tractus pyramidalis; Pla to P~b, 'peaks' (see text). The anatomical maps are frontal sections at the A0 and A5 levels. Arrows indicate the direction of the eye movements; solid line arrow = marked movement; broken line arrow = weak movement.
was recorded in the left parastriate cortex (area 18) at an estimated depth o f 1800 Fro; its receptive field was horizontally oriented and extended over 22.5°; it was situated in the temporo-inferior q u a d r a n t (see diagram D). The neuron was very sensitive to a temporo-nasal slit movement, the opposite direction eliciting a less marked response; it was insensitive to a vertical slit movement. Its response pattern during a single sweep, i.e. one to-and-fro slit movement, and during 29 sweeps is shown in the top left recording (A) resp. the time histogram (B), whose digital values were used to construct a peak-sequence histogram (C). Electric stimulations were applied at both mesencephalic and anterior pontine levels (see the two anatomical maps E and F: the arrows indicate the direction o f the eye movements, elicited by the stimulation at the given point before curarization; solid line arrow = marked movement, broken line arrow = weak movement). The two diagrams G and H show the effect o f the brain stem stimulations (Sz-S4) u p o n the neuron's response pattern on the moving slit after curarization and in the absence o f any eye movement, plotted in information value time coordinates, time being the real experimental time expressed in sweeps. It is to be noted that only these brain stem areas, Brain Research, 17 (1970) 351-354
354
SHORT COMMUNICATIONS
responsible for the strongest eye movements, exerted an influence on the positive peaks and only in the temporo-nasal direction, namely $1 and especially $4 on Pl,~ and Pie by a decrease and on Plb by an increase. Further it should be noted that the lcurve of both Pla and Pie can be approximated by an exponentially decaying time function: the constant o f this decay is the same for both peaks, namely IPla 12 • exp ( - - 0 . 1 6 0 and IPle = 18 • exp (--0.16t). In diagram I the noise of the neuron is plotted against time as a control. Analysis o f the hitherto available neurons indicate that there is not only a correlation between the amplitude o f the ocular deviation and the intensity o f the stimulation effect but also between the direction of movement and that o f the neuron's optimal sensitivity. The influence o f the o c u l o m o t o r areas on the visual neurons is considered to be n o r m o d r o m i c and specific. All antidromically driven neurons, as tested by the following rate upon repetitive stimulation, were discarded. The effect o f brain stem stimulation is not due to reticular activation for several reasons: the brain stem stimulations activated only particular aspects o f the neural activity, namely the neural response on the moving slit, and not its global activity; the stimulation o f neighboring areas all within the reticular formation, eliciting different eye movements, exerted different influences on the neural response; concomitant E E G recording provided further evidence for the absence o f reticular cortical activation. Laboratory for Neuro- and Psychophysiology, University of Louvain, Louvain (Belgium)
GUY ORBAN ROLAND WISSAERT MARK CALLENS
1 BENDER, M. B., AND SHANZER, S., Oculomotor pathways defined by electrical stimulation and
2
3 4 5 6
lesions in the brainstem of monkey. In M. B. BENDER(Ed.), The Oculomotor System, Harper and Row, New York, 1964, pp. 81-140. HELMHOLTZ, H. VON, Handbuch der Physiologischen Optik, Vol. 1II, Voss, Hamburg, 1896, pp. 242-267. HUBEL,D. H., AND WIESEL, T. N., Receptive fields of single neurons in the cat's striate cortex, J. Physiol. (Lond.), 148 (1959) 574-591. HUBEL, D. H., AND WIESEL, T. N., Receptive fields and functional organization in two nonstriate visual areas (18 and 19) of the cat, J. Neurophysiol., 28 (1965) 229-289. HYDE, J. E., AND ELIASON,S. G., Brainstem induced eye movements in cats, J. comp. Neurok, 108 (1957) 139-173. ZUBER, B. g., AND STARK, L., Saccadic suppression: elevation of visual threshold associated with saccadic eye movements, Exp. NeuroL, 16 (1966) 65-79.
(Accepted November 4th, 1969)
Brain Research, 17 (1970) 351-354
351
Influence of brain stem oculomotor area stimulation on single unit activity in the visual cortex. Mathematical analysis of results Eye movements exert a three-fold influence on vision: first, blurring of the retinal image as a consequence of relative retinal movement; secondly, stimulation of the proprioceptors of the extrinsic ocular muscles; and, finally, activation of a central loop connecting oculomotor and visual centers. The latter neural activity is postulated to be the mechanism responsible for visual stability during eye movements2 and visual suppression during saccades 6. According to Hyde and Eliason 5 and to Bender and Shanzer t there are oculomotor areas in the anterior brain stem. Our experiments aimed to elucidate some aspects of the unitary processes in the connections b~tween these areas (dorsal and ventral tegmentum and anterior pons) and the visual cortex. In enc6phale isol6 cats, electrodes were introduced into various brain stem areas, whose stimulation elicited definite conjugated eye movements in different directions. After curarizing the animal with both D-tubocurarine and gallamine triiodoethylate (Flaxedil) and after thorough control of the absence of any eye movement, the receptive field and the optimal direction sensitivity of striate and parastriate neurons upon a slit (a narrow rectangle, 0.3 ° × 12°, of light), to and fro moving in different directions on a screen facing the animal, were determined. Subsequently the slit-evoked neural activity and its changes upon stimulation of the various oculomotor brain stem areas, but in the absence of any eye movement, were recorded. Mathematical analysis. The first step of the mathematical analysis was the computation of the tape-recorded 'raw data' per stimulation condition into time histograms (200 addresses/16 min of a complete to-and-fro slit movement) and their conversion to digital values, i.e. number of discharges per address for a given number of sweeps. The next step was the conversion of the response pattern into a sequence of (positive and/or negative) 'peaks' by isolating the addresses containing a number of discharges significantly deviating from the mean discharge rate, by grouping the successive addresses containing positive or negative deviations into peaks and by calculating for each peak the mean discharge frequency and the mean frequency of the addresses outside all peaks; the latter value was considered to be the mathematical expression of the 'noise' of the unit, whereas the former values were to be related to this noL,e value in order to yield a mathematical expression of the peak's 'information value' (I). The information value of a peak was defined as:
(F i - F o) ni I=
(1)
where ni is the peak interval, i.e. the number of addresses grouped in the peak, Ft the mean frequency of the peak and Fo the mean frequency outside the peaks (defined as noise): Brain Research, 17 (1970) 351-354
352
SHORT COMMUNICATIONS
(2) I1 i
Fo
=
~ _ F°
_
(3)
1]o
no being the number of addresses outside the peaks. When N is the total number of addresses, no = N -
Y~ni
(4)
The l-formula (1) is a combination of 3 essential operations: (1) The difference in absolute values between the mean peak frequency and the noise frequency: this is justified by the facts that the peak also contains noise and that the 1 of a peak is its differentiation from the noise values and not its absolute value. (2) The multiplication of this difference by the peak interval for a surface is a more adequate description of a peak than its mere height. (3) The division of this product by the noise frequency, taking into account that a peak of a given surface does not contain the same information when the noise is low or high: moreover the latter operation standardizes the I with respect to the noise and allows interunit comparisons. The I-formula takes into account some aspects of the presently accepted hypothesis that information is carried along neurons as 'positive peaks', i.e. significant increases of discharge frequency. Indeed, since in the first operation the difference in absolute values is made between the mean peak frequency and the noise frequency, the I of a negative peak is limited by the noise level, whereas the I of a positive peak is (theoretically) illimited (practically by the maximal discharge frequency of the neuron). Information transmission by significant negative peaks presupposes a high level of noise, i.e. wasted cellular activity; further, small variations of the mean peak frequency entail enormous I-fluctuations. Therefore, positive peaks are more economic and more redundant. The specific function of the negative peak might be to delimit sharply the duration of the information transmission by a positive peak to an excitatory or inhibitory synaptic connection. (It should be remembered, however, that negative peaks are partly due to experimental artifacts, since, in case of visual neurons, they are converted to positive peaks when stimulating by a dark bar instead of a slit.) Results and comments. As a preliminary remark it may be stated that the results obtained are in good agreement with those of Hubel and Wiesel 3,4, with respect to the receptive fields of the visual neurons, and with those of Hyde and Eliason 5 and Bender and Shanzer 1, with respect to the ocular deviations elicited by brain stem stimulation. Concerning the main topic of our research, namely the influence of brain stem oculomotor areas on striate and parastriate neurons, a typical example is neuron 1I/9-6 (Fig. 1), which also illustrates the valuable use of the I-formula for extracting signals out of random activity, when the latter consists of discrete events. This neuron Brain Research, 17 (1970) 351-354
SHORT COMMUNICATIONS Cell]1/9-6 A
v i s u a l cortex : a r e a l 8
rr
••
'°°
-
:'.,;::-.,';, ..
[]
L~
~a~.
Receptive fietd
'1i
~ ""
.. .. ,_...
• o,~,~,;s~,~;..po.,,,,;Ao;,,',~° "ee;",e,,, ,'-; o. ~. o ,~
"
(3
i~s ... /| IO-~R__\ / l a ~ ,
,,c d
,:., .-" .'" ." ~"
/"!
29 sweeps 200addresses
: "'.
I " "
20T'rnformation Vatue
1.800~J. ,,weep
150 ~ B
50
353
"
P2aP2b
I I
Tempor4t : : : "45Nastt hori..... L ~1 22,5°targ~ £" L J=.
'1
'~~----~'--I
. ,,,° -°v,t.
noise
|
~$1. ,
4,S4 '
,0
$$2
"
4Tznformation Vatue 3£R'7 t d£a ................. ...."'" ""'"-..
H
1 I~b/
lo,25o t
8
,s,.
24
,s4..
40
,~ 56 Sweeps
| Noise 3010 t spikes~/sec
8
T
24 " 40 ' 5~ Sweeps
Fig. 1. For explanation see text. Abbreviations: CI, colliculus inferior; CS, colliculus superior; Fr, firing rate; GL, corpus geniculatum lateral°; GM, corpus geniculatum mediale; I, information value; LM, lemniscus medialis; Py, tractus pyramidalis; Pla to P~b, 'peaks' (see text). The anatomical maps are frontal sections at the A0 and A5 levels. Arrows indicate the direction of the eye movements; solid line arrow = marked movement; broken line arrow = weak movement.
was recorded in the left parastriate cortex (area 18) at an estimated depth o f 1800 Fro; its receptive field was horizontally oriented and extended over 22.5°; it was situated in the temporo-inferior q u a d r a n t (see diagram D). The neuron was very sensitive to a temporo-nasal slit movement, the opposite direction eliciting a less marked response; it was insensitive to a vertical slit movement. Its response pattern during a single sweep, i.e. one to-and-fro slit movement, and during 29 sweeps is shown in the top left recording (A) resp. the time histogram (B), whose digital values were used to construct a peak-sequence histogram (C). Electric stimulations were applied at both mesencephalic and anterior pontine levels (see the two anatomical maps E and F: the arrows indicate the direction o f the eye movements, elicited by the stimulation at the given point before curarization; solid line arrow = marked movement, broken line arrow = weak movement). The two diagrams G and H show the effect o f the brain stem stimulations (Sz-S4) u p o n the neuron's response pattern on the moving slit after curarization and in the absence o f any eye movement, plotted in information value time coordinates, time being the real experimental time expressed in sweeps. It is to be noted that only these brain stem areas, Brain Research, 17 (1970) 351-354
354
SHORT COMMUNICATIONS
responsible for the strongest eye movements, exerted an influence on the positive peaks and only in the temporo-nasal direction, namely $1 and especially $4 on Pl,~ and Pie by a decrease and on Plb by an increase. Further it should be noted that the lcurve of both Pla and Pie can be approximated by an exponentially decaying time function: the constant o f this decay is the same for both peaks, namely IPla 12 • exp ( - - 0 . 1 6 0 and IPle = 18 • exp (--0.16t). In diagram I the noise of the neuron is plotted against time as a control. Analysis o f the hitherto available neurons indicate that there is not only a correlation between the amplitude o f the ocular deviation and the intensity o f the stimulation effect but also between the direction of movement and that o f the neuron's optimal sensitivity. The influence o f the o c u l o m o t o r areas on the visual neurons is considered to be n o r m o d r o m i c and specific. All antidromically driven neurons, as tested by the following rate upon repetitive stimulation, were discarded. The effect o f brain stem stimulation is not due to reticular activation for several reasons: the brain stem stimulations activated only particular aspects o f the neural activity, namely the neural response on the moving slit, and not its global activity; the stimulation o f neighboring areas all within the reticular formation, eliciting different eye movements, exerted different influences on the neural response; concomitant E E G recording provided further evidence for the absence o f reticular cortical activation. Laboratory for Neuro- and Psychophysiology, University of Louvain, Louvain (Belgium)
GUY ORBAN ROLAND WISSAERT MARK CALLENS
1 BENDER, M. B., AND SHANZER, S., Oculomotor pathways defined by electrical stimulation and
2
3 4 5 6
lesions in the brainstem of monkey. In M. B. BENDER(Ed.), The Oculomotor System, Harper and Row, New York, 1964, pp. 81-140. HELMHOLTZ, H. VON, Handbuch der Physiologischen Optik, Vol. 1II, Voss, Hamburg, 1896, pp. 242-267. HUBEL,D. H., AND WIESEL, T. N., Receptive fields of single neurons in the cat's striate cortex, J. Physiol. (Lond.), 148 (1959) 574-591. HUBEL, D. H., AND WIESEL, T. N., Receptive fields and functional organization in two nonstriate visual areas (18 and 19) of the cat, J. Neurophysiol., 28 (1965) 229-289. HYDE, J. E., AND ELIASON,S. G., Brainstem induced eye movements in cats, J. comp. Neurok, 108 (1957) 139-173. ZUBER, B. g., AND STARK, L., Saccadic suppression: elevation of visual threshold associated with saccadic eye movements, Exp. NeuroL, 16 (1966) 65-79.
(Accepted November 4th, 1969)
Brain Research, 17 (1970) 351-354