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Modulation of visual cortex inhibition during reticular evoked arousal
Physiology and Behavior, Vol. 9, pp. 805-808. Brain Research Publications Inc., 1972. Printed in U.S.A.
Modulation of Visual Cortex Inhibition During Reticular Evoked Arousal ' DENNIS M. FEENEY AND JOHN M. OREM ~
Department o f Psychology, University o f N e w Mexico, Albuquerque, New Mexico 8 7106
(Received 15 March 1972)
FEENEY, D. M. AND J. M. OREM. Modulation of visual cortex inhibition during reticular evoked arousal. PHYSIOL. BEHAV. 9(5) 805-808, 1972.- The effects of stimulation of the mesencephalic reticular formation on inhibition of visual cortex neurons by optic radiation stimulation was studied in locally anesthetized acute cats. If reticular stimulation excited a visual ,'ortex unit an enhancement of subsequent optic radiation evoked inhibition was observed. This occurred for 50-400 msec following reticular stimulation and was maximal at 200 msec. For some cells, reticular stimulation initially inhibited spontaneous discharge. For these units a shortened duration of optic radiation evoked inhibition was often observed when that stimulus was placed during the reticular evoked inhibition. A hypothesis is presented to account for these effects. Inhibition
Cortex
Vision
Microelectrode
Arousal
THE RECEPTIVE field organization of units in the visual cortex of unanesthetized cats is markedly unstable. The inhibitory areas are the most plastic feature of these receptive fields, and their alteration is most pronounced during desynchronized EEG states whereas barbiturate anesthesia or spontaneous EEG spindles reduce receptive field variability [2]. Since the brain stem reticular formation is considered to be involved in wakefulness, these data suggest an important role for that structure in the control of inhibitory mechanisms within visual cortex. Two studies provide indirect but contradictory evidence regarding reticular influences on inhibition in visual cortex. Evarts [7] has shown that inhibition of visual cortex neurons by optic radiations (OR) stimulation is of longer duration during waking than during slow wave sleep. However, Skrebitsky [13] has reported that novel, arousing stimuli suppress flash evoked IPSPs in visual cortex and postulates an inhibition of inhibition by nonspeciflc mechanisms. This later hypothesis is in accord with work in the thalamus [3, 9, 12] and motor cortex [14]. However few cells were studied, and with photic stimuli the reticular influence may have occurred at retinal or thalamic levels. A direct investigation of reticular influence on visual cortex inhibition seemed warranted. The present study describes the effects of arousal induced by mesencephalic reticular stimulation on the duration of inhibition of visual cortex units to OR stimulation.
Sleep
Reticular formation
METHOD Acute experiments were conducted on 15 adult cats. A venous catheter was inserted and intubation of the trachea carried out under ether anesthesia. Under intravenous Brevital anesthesia a bone flap was removed over the lateral gyrus and a pneumothorax and cisternal drainage performed to reduce pulsations. Wound edges and pressure points were infiltrated with xylocaine. The animal was paralyzed with gallamine triethiodide (Flaxadil), respirated, and general anesthesia discontinued. Body temperature was maintained at 3 6 - 3 8 ° C . Bipolar concentric electrodes (inner wire dia. 150 ~ and interelectrode distance 1.5 mm) were placed in the mesencephalic reticular formation (MRF) (A 2, L 2, H - 2 ) and optic radiations. Stimulation of the MRF ( 8 - 1 0 pulses at 400/sec, 0.5 msec duration, 0.6 mA) produced physiological signs of arousal: pupillary dilitation, potentiation of the cortical evoked potential to OR stimulation [5] and blockade of EEG sleep spindles. Electrode placements in OR were aimed for coordinates A 6.0, L 10.0, H + 7 . 0 - 9 . 0 and confirmed by obtaining a clear evoked potential from the marginal gyrus to a single OR pulse (0.5 msec, 0.6 mA). Prior to unit recording the pupils were dilated with topical atropine sulfate and the eyes covered with moist cotton. Single units were sampled from both areas 17 and 18 [ 11 ] and were recorded by means of glass micropipettes
IThis research was supported by funds from the University of New Mexico and by Public Health Service Grant NS 10469-01 from the National Institute of Neurological Diseases and Stroke. 2Dr. Orem's present address is Department of Anatomy, UCLA School of Medicine, Los Angeles, Calif. 805
806
FEENEY AND OREM
(tip dia. less than 2 t~) filled with 3 M KC1. Penetrations were limited to the upper 3 mm of the cortical surface. Activity was led through a cathode follower (Picometric) and conventional amplifiers a n d displayed on an oscilloscope (Tektronix 502A). Superimposed photographs were used for analysis and in later preparations an on-line computer (Linc 8, Digital Equipment Corporation) was used to calculate poststimulus time histograms. Cells were selected which showed clear responses to both OR and MRF stimulation. Since the data of interest were the durations of silence or absence of spontaneous discharge following the OR stimulus, only cells with a stable rate of spontaneous activity were studied. After characterizing the effect of OR and MRF stimulation on a cell, conditioning test procedures were carried out at a variety of intervals between MRF and OR stimuli. When utilizing the computer, parametric conditioning test procedures were carried out at intervals of 50, 100, 200, 300, 400 and 500 msec, the order being varied. A three sec intertrial interval was employed and 15 or 30 trials run for each data point. Animals were sacrificed by an overdose of barbiturate and the electrode placements confirmed histologically using frozen 80 ~ sections stained with thionine.
A
B
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RESULTS A total of 68 neurons were studied for interactions between MRF and OR stimulation. These cells were part of a larger group of more than 200 neurons and were selected for analysis because of their stable spontaneous rate and clear MRF and OR evoked activity. The MRF stimulation had both excitatory and inhibitory effects on visual cortex neurons and the effects of MRF stimulation on OR evoked inhibition was different for these two classes of cells.
M R F Excitatory Units Of the 68 units studied, 41 displayed an excitatory response to high frequency MRF stimulation. The evoked firing was diffused over a 5 0 - 1 0 0 0 msec period. For 28 of these driven units, MRF conditioning increased the duration of OR evoked inhibition over the control level. This effect was most striking since the increased inhibition was obtained against the background of the higher discharge rate evoked by the MRF stimuli (Fig. 1). In 9 units the OR evoked inhibition was decreased by the MRF conditioning, and no effects were seen in 4 units. F o r I 1 neurons from 3 preparations complete computer data was obtained for each of the selected conditioning test intervals. These data were averaged and are presented in Fig. 2. This figure indicates an overall increase in the duration of inhibition by the conditioning procedure, peaking at 200 msec. A repeated measure analysis of variance yielded a highly significant treatments effect (p<0.005). Specific comparisons of each conditioning interval with the control level indicated a statistically significant (p<0.05) increase in the duration of inhibition at all intervals except 500 msec.
M R F Inhibited Units In response to MRF stimulation 27 units were inhibited for 5 0 - 3 0 0 msec. For 12 of these, this initial inhibition was followed by an increase in the discharge rate. The MRF-OR interactions were less clear cut for these MRF inhibited units. At short conditioning intervals alterations
1 FIG. 1. Photos are of ten superimposed oscilloscope traces illustrating potentiation of the optic radiation evoked inhibition of a single unit in visual cortex by a preceding reticular stimulation. Stimuli are applied at arrows. (A) The high frequency reticular stimulus alone evokes sustained firing of this cell. (B) Optic radiations stimulus alone. The intensity is below threshold for evocation of inhibition. (C) The optic radiations stimulus evokes a clear period of inhibition when preceded by the reticular stimulus. Voltage calibration: 2 mV. Time: horizontal bar, 200 msec.
in OR evoked inhibition were confounded by the inhibition evoked to the MRF stimuli. However, placing the OR stimulus at the end of the MRF evoked inhibition often shortened the OR evoked inhibition. This apparent occlusive effect was clearly seen in 11 units and is illustrated in Fig. 3. In the other cells either no effect was seen or the effect could not be distinguished from simple summation. In 13 of these cells a potentiation of the inhibition was observed when the OR test stimulus was placed after the initial inhibition. The between cell variability of these effects precluded pooling these data for more quantitative analysis. DISCUSSION Against a background of reticular evoked excitation, most visual cortex neurons displayed an enhancement of inhibition evoked by OR stimulation. This enhancement was seen for 5 0 - 4 0 0 msec following MRF stimulation and was maximal at approximately 200 msec. This corresponds to the maximal period of reticular facilitation of the late positive and negative waves of the visual cortex responses to
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FIG. 2. The graph depicts the increase in the duration of optic radiations evoked inhibition by the reticular stimulation at several conditioning test intervals. This is based on averages of I 1 units all of which were excited by the reticular stimulus. See text.
optic path stimulation [5]. Also, reticular evoked unit excitation is more prominent in area 18 than 17 of the cat [10] as is the reticular facilitation of the OR evoked potential [5]. A simple relationship between reticular facilitation of evoked potential amplitude and duration of unit inhibition is not fully supported, however, since during sustained wakefulness there is a facilitation of OR evoked unit inhibition over slow wave sleep [7] yet the evoked potentials are of smaller amplitude [5, 7]. Perhaps as has been hypothesized [7, 15] the longer recovery cycle of these potentials during waking and attentiveness reflect the increase in afferent evoked inhibition. In contrast to units excited by reticular activation, for some cells initially inhibited by the MRF stimulus, OR evoked inhibition was shortened or suppressed by the preceding reticular stimulation. This effect Was only observed when the OR stimulation was presented during the MRF evoked inhibition. Such an occlusive effect implies a sharing of substrates and a possible convergence of nonspecific and specific inputs onto inhibitory mechanisms within visual cortex. The effects of MRF stimulation on visual cortex evoked inhibition are interpreted as intracortical interactions since retinal and thalamic loci were by-passed by stimulation of
2
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FIG. 3. Poststimulus time histograms based on 15 trials each, depicting the interaction of optic radiations evoked inhibition and reticular evoked inhibition on a single cell in visual cortex. (A) Computer triggered after reticular stimulation. (B) Computer triggered after optic radiations stimulus. (C) Computer triggered after optic radiations stimulus as in B; however, for this series the reticular stimulus preceded the optic radiations stimulus by 250 msec. Note the shorter duration optic radiations inhibition in this last condition. the optic radiations. An intracortical interpretation is also supported by the observation of similar MRF influences on visual cortex inhibition evoked by antidromic callosal volleys [8]. An increase in evoked inhibition on a background of evoked excitation and a decrease on a background of evoked inhibition, has been observed previously [1, 4, 9]. There are several possible explanations for this seemingly paradoxical interaction. Inhibition of visual cortex neurons is, at least in part, a product of recurrent collaterals which requires temporal summation [8]. The diffuse firing evoked by MRF stimulation in visual cortex neurons may be too temporally dispersed, in most cases, to fully activate the recurrent inhibitory circuit. This diffuse MRF excitation could, however, summate with a subsequent synchronous volley evoked by the OR stimulus resulting in a potentiation of the inhibition. If reticular excitation was for some neurons sufficiently intense and synchronous to activate the recurrent inhibitory mechanism, some units would be inhibited by the reticular stimulation. As observed, these MRF inhibited units would occlusively interact with OR
808
FEENEY AND OREM
evoked inhibition. This hypothesis does not exclude alternative and/or parallel mechanisms such as direct reticular influence on hypothetical inhibitory interneurons [6]. The present study indicates that during reticular activation there is a modulation of inhibitory mechanisms in visual cortex. During MRF evoked inhibition a suppression or occlusion of OR evoked inhibition is observed, whereas during MRF evoked excitation, a facilitation of afferent inhibition occurs. The facilitation of afferent inhibition during reticular evoked excitation contrasts with the
suppression of inhibition at the motor cortex [14] and thalamic nuclei [3, 9, 12] during reticular activation. This regulation of visual cortex inhibitory mechanisms by the MRF may be involved in the alteration of visual cortex receptive fields seen in waking cats [ 2] and in the alteration of sensory function seen in focused attention [15]. Inhibition is thought to play an important role in focusing or sharpening the transduction of sensory information; its modulation at the cortex by the reticular formation could provide a powerful influence on perceptual experience.
REFERENCES
1. Arduini, A. and L. R. Pinneo. Properties of the retina in response to steady illumination. Archs ital. Biol. 100: 425-448, 1962. 2. Bear, D. M., H. Sasaki and F. R. Ervin. Sequential change in receptive fields of striate neurons in dark adapted cats. Expl Brain Res. 13: 256-272, 1971. 3. Bremer, F. Inhibitions intrathalamiques recurrentielles et physiologic du sommeil. Electroenceph. clin. Neurophysiol. 28: 1-16, 1970. 4. Corazza, R., V. Tradardi and C. Umilta. Types of response to steady illumination and levels of neuronal dark discharge in the central visual pathways. Brain Res. 16:121-132, 1969. 5. Courtois, A. and J. P. Cordeau. Changes in cortical responsiveness during transition from sleep to wakefulness. Brain Res. 14: 199-214, 1969. 6, Eccles, J. C. The Inhibitory Pathways o f the Central Nervous System. Springfield, Massachusetts: Charles Thomas, 1969. 7. Evarts, E. V. Neuronal activity in visual and motor cortex during sleep and waking. In: Neurophysiologie des Etats de Sommeil, edited by M. Jouvet. Pads: Centre National de la Recherche Scientifique, 189-212, 1965. 8. Feeney, D. M. and J. M. Orem. Influence of antidromic callosal volleys on single units in visual cortex. Expl Neurol. 33: 310-321, 1971.
9. Fukuda, Y. and K. lwama. Reticular inhibition of internuncial cells in the rat lateral geniculate. Brain Res. 35: 107-120, 1971. 10. Orem, J. M. and D. M. Feeney. Reciprocal reticular influences on cells in rostral and caudal visual cortex of the cat. Brain Res. 30: 200-203, 1971. 11. Otsuka, R. und R. Hassler. Uber Auffau und Gleiderund der corticalen Sehsphare bei der Katz. Archs Psychiat. nervenkr. 203: 212-234, 1962. 12. Purpura, D. and R. J. Shofer. lntraceUular recording from thalamic neurons during reticulocortical activation. J. Neurophysiol. 26: 494-505, 1963. 13. Skrebitsky, V. Postsynaptic inhibition in photically evoked responses and its change during distraction of the animal. Brain Res. 14: 510-512, 1969. 14. Steriade, M., P. Wyzinsky, M. Deschenes and M. Guerin. Disinhibition during waking in motor cortex neuronal chains in cat and monkey. Brain Res. 30: 211-217, 1971. 15. Young, D. N., G. D. Ellison and D. M. Feeney. Electrophysiological correlates of selective attention: Modality specific changes in thalamocortical evoked potentials. Brain Res. 28: 501-510, 1971.
Modulation of Visual Cortex Inhibition During Reticular Evoked Arousal ' DENNIS M. FEENEY AND JOHN M. OREM ~
Department o f Psychology, University o f N e w Mexico, Albuquerque, New Mexico 8 7106
(Received 15 March 1972)
FEENEY, D. M. AND J. M. OREM. Modulation of visual cortex inhibition during reticular evoked arousal. PHYSIOL. BEHAV. 9(5) 805-808, 1972.- The effects of stimulation of the mesencephalic reticular formation on inhibition of visual cortex neurons by optic radiation stimulation was studied in locally anesthetized acute cats. If reticular stimulation excited a visual ,'ortex unit an enhancement of subsequent optic radiation evoked inhibition was observed. This occurred for 50-400 msec following reticular stimulation and was maximal at 200 msec. For some cells, reticular stimulation initially inhibited spontaneous discharge. For these units a shortened duration of optic radiation evoked inhibition was often observed when that stimulus was placed during the reticular evoked inhibition. A hypothesis is presented to account for these effects. Inhibition
Cortex
Vision
Microelectrode
Arousal
THE RECEPTIVE field organization of units in the visual cortex of unanesthetized cats is markedly unstable. The inhibitory areas are the most plastic feature of these receptive fields, and their alteration is most pronounced during desynchronized EEG states whereas barbiturate anesthesia or spontaneous EEG spindles reduce receptive field variability [2]. Since the brain stem reticular formation is considered to be involved in wakefulness, these data suggest an important role for that structure in the control of inhibitory mechanisms within visual cortex. Two studies provide indirect but contradictory evidence regarding reticular influences on inhibition in visual cortex. Evarts [7] has shown that inhibition of visual cortex neurons by optic radiations (OR) stimulation is of longer duration during waking than during slow wave sleep. However, Skrebitsky [13] has reported that novel, arousing stimuli suppress flash evoked IPSPs in visual cortex and postulates an inhibition of inhibition by nonspeciflc mechanisms. This later hypothesis is in accord with work in the thalamus [3, 9, 12] and motor cortex [14]. However few cells were studied, and with photic stimuli the reticular influence may have occurred at retinal or thalamic levels. A direct investigation of reticular influence on visual cortex inhibition seemed warranted. The present study describes the effects of arousal induced by mesencephalic reticular stimulation on the duration of inhibition of visual cortex units to OR stimulation.
Sleep
Reticular formation
METHOD Acute experiments were conducted on 15 adult cats. A venous catheter was inserted and intubation of the trachea carried out under ether anesthesia. Under intravenous Brevital anesthesia a bone flap was removed over the lateral gyrus and a pneumothorax and cisternal drainage performed to reduce pulsations. Wound edges and pressure points were infiltrated with xylocaine. The animal was paralyzed with gallamine triethiodide (Flaxadil), respirated, and general anesthesia discontinued. Body temperature was maintained at 3 6 - 3 8 ° C . Bipolar concentric electrodes (inner wire dia. 150 ~ and interelectrode distance 1.5 mm) were placed in the mesencephalic reticular formation (MRF) (A 2, L 2, H - 2 ) and optic radiations. Stimulation of the MRF ( 8 - 1 0 pulses at 400/sec, 0.5 msec duration, 0.6 mA) produced physiological signs of arousal: pupillary dilitation, potentiation of the cortical evoked potential to OR stimulation [5] and blockade of EEG sleep spindles. Electrode placements in OR were aimed for coordinates A 6.0, L 10.0, H + 7 . 0 - 9 . 0 and confirmed by obtaining a clear evoked potential from the marginal gyrus to a single OR pulse (0.5 msec, 0.6 mA). Prior to unit recording the pupils were dilated with topical atropine sulfate and the eyes covered with moist cotton. Single units were sampled from both areas 17 and 18 [ 11 ] and were recorded by means of glass micropipettes
IThis research was supported by funds from the University of New Mexico and by Public Health Service Grant NS 10469-01 from the National Institute of Neurological Diseases and Stroke. 2Dr. Orem's present address is Department of Anatomy, UCLA School of Medicine, Los Angeles, Calif. 805
806
FEENEY AND OREM
(tip dia. less than 2 t~) filled with 3 M KC1. Penetrations were limited to the upper 3 mm of the cortical surface. Activity was led through a cathode follower (Picometric) and conventional amplifiers a n d displayed on an oscilloscope (Tektronix 502A). Superimposed photographs were used for analysis and in later preparations an on-line computer (Linc 8, Digital Equipment Corporation) was used to calculate poststimulus time histograms. Cells were selected which showed clear responses to both OR and MRF stimulation. Since the data of interest were the durations of silence or absence of spontaneous discharge following the OR stimulus, only cells with a stable rate of spontaneous activity were studied. After characterizing the effect of OR and MRF stimulation on a cell, conditioning test procedures were carried out at a variety of intervals between MRF and OR stimuli. When utilizing the computer, parametric conditioning test procedures were carried out at intervals of 50, 100, 200, 300, 400 and 500 msec, the order being varied. A three sec intertrial interval was employed and 15 or 30 trials run for each data point. Animals were sacrificed by an overdose of barbiturate and the electrode placements confirmed histologically using frozen 80 ~ sections stained with thionine.
A
B
t "
I
RESULTS A total of 68 neurons were studied for interactions between MRF and OR stimulation. These cells were part of a larger group of more than 200 neurons and were selected for analysis because of their stable spontaneous rate and clear MRF and OR evoked activity. The MRF stimulation had both excitatory and inhibitory effects on visual cortex neurons and the effects of MRF stimulation on OR evoked inhibition was different for these two classes of cells.
M R F Excitatory Units Of the 68 units studied, 41 displayed an excitatory response to high frequency MRF stimulation. The evoked firing was diffused over a 5 0 - 1 0 0 0 msec period. For 28 of these driven units, MRF conditioning increased the duration of OR evoked inhibition over the control level. This effect was most striking since the increased inhibition was obtained against the background of the higher discharge rate evoked by the MRF stimuli (Fig. 1). In 9 units the OR evoked inhibition was decreased by the MRF conditioning, and no effects were seen in 4 units. F o r I 1 neurons from 3 preparations complete computer data was obtained for each of the selected conditioning test intervals. These data were averaged and are presented in Fig. 2. This figure indicates an overall increase in the duration of inhibition by the conditioning procedure, peaking at 200 msec. A repeated measure analysis of variance yielded a highly significant treatments effect (p<0.005). Specific comparisons of each conditioning interval with the control level indicated a statistically significant (p<0.05) increase in the duration of inhibition at all intervals except 500 msec.
M R F Inhibited Units In response to MRF stimulation 27 units were inhibited for 5 0 - 3 0 0 msec. For 12 of these, this initial inhibition was followed by an increase in the discharge rate. The MRF-OR interactions were less clear cut for these MRF inhibited units. At short conditioning intervals alterations
1 FIG. 1. Photos are of ten superimposed oscilloscope traces illustrating potentiation of the optic radiation evoked inhibition of a single unit in visual cortex by a preceding reticular stimulation. Stimuli are applied at arrows. (A) The high frequency reticular stimulus alone evokes sustained firing of this cell. (B) Optic radiations stimulus alone. The intensity is below threshold for evocation of inhibition. (C) The optic radiations stimulus evokes a clear period of inhibition when preceded by the reticular stimulus. Voltage calibration: 2 mV. Time: horizontal bar, 200 msec.
in OR evoked inhibition were confounded by the inhibition evoked to the MRF stimuli. However, placing the OR stimulus at the end of the MRF evoked inhibition often shortened the OR evoked inhibition. This apparent occlusive effect was clearly seen in 11 units and is illustrated in Fig. 3. In the other cells either no effect was seen or the effect could not be distinguished from simple summation. In 13 of these cells a potentiation of the inhibition was observed when the OR test stimulus was placed after the initial inhibition. The between cell variability of these effects precluded pooling these data for more quantitative analysis. DISCUSSION Against a background of reticular evoked excitation, most visual cortex neurons displayed an enhancement of inhibition evoked by OR stimulation. This enhancement was seen for 5 0 - 4 0 0 msec following MRF stimulation and was maximal at approximately 200 msec. This corresponds to the maximal period of reticular facilitation of the late positive and negative waves of the visual cortex responses to
AROUSAL AND VISUAL CORTEX INHIBITION
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optic path stimulation [5]. Also, reticular evoked unit excitation is more prominent in area 18 than 17 of the cat [10] as is the reticular facilitation of the OR evoked potential [5]. A simple relationship between reticular facilitation of evoked potential amplitude and duration of unit inhibition is not fully supported, however, since during sustained wakefulness there is a facilitation of OR evoked unit inhibition over slow wave sleep [7] yet the evoked potentials are of smaller amplitude [5, 7]. Perhaps as has been hypothesized [7, 15] the longer recovery cycle of these potentials during waking and attentiveness reflect the increase in afferent evoked inhibition. In contrast to units excited by reticular activation, for some cells initially inhibited by the MRF stimulus, OR evoked inhibition was shortened or suppressed by the preceding reticular stimulation. This effect Was only observed when the OR stimulation was presented during the MRF evoked inhibition. Such an occlusive effect implies a sharing of substrates and a possible convergence of nonspecific and specific inputs onto inhibitory mechanisms within visual cortex. The effects of MRF stimulation on visual cortex evoked inhibition are interpreted as intracortical interactions since retinal and thalamic loci were by-passed by stimulation of
2
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MSEC
FIG. 3. Poststimulus time histograms based on 15 trials each, depicting the interaction of optic radiations evoked inhibition and reticular evoked inhibition on a single cell in visual cortex. (A) Computer triggered after reticular stimulation. (B) Computer triggered after optic radiations stimulus. (C) Computer triggered after optic radiations stimulus as in B; however, for this series the reticular stimulus preceded the optic radiations stimulus by 250 msec. Note the shorter duration optic radiations inhibition in this last condition. the optic radiations. An intracortical interpretation is also supported by the observation of similar MRF influences on visual cortex inhibition evoked by antidromic callosal volleys [8]. An increase in evoked inhibition on a background of evoked excitation and a decrease on a background of evoked inhibition, has been observed previously [1, 4, 9]. There are several possible explanations for this seemingly paradoxical interaction. Inhibition of visual cortex neurons is, at least in part, a product of recurrent collaterals which requires temporal summation [8]. The diffuse firing evoked by MRF stimulation in visual cortex neurons may be too temporally dispersed, in most cases, to fully activate the recurrent inhibitory circuit. This diffuse MRF excitation could, however, summate with a subsequent synchronous volley evoked by the OR stimulus resulting in a potentiation of the inhibition. If reticular excitation was for some neurons sufficiently intense and synchronous to activate the recurrent inhibitory mechanism, some units would be inhibited by the reticular stimulation. As observed, these MRF inhibited units would occlusively interact with OR
808
FEENEY AND OREM
evoked inhibition. This hypothesis does not exclude alternative and/or parallel mechanisms such as direct reticular influence on hypothetical inhibitory interneurons [6]. The present study indicates that during reticular activation there is a modulation of inhibitory mechanisms in visual cortex. During MRF evoked inhibition a suppression or occlusion of OR evoked inhibition is observed, whereas during MRF evoked excitation, a facilitation of afferent inhibition occurs. The facilitation of afferent inhibition during reticular evoked excitation contrasts with the
suppression of inhibition at the motor cortex [14] and thalamic nuclei [3, 9, 12] during reticular activation. This regulation of visual cortex inhibitory mechanisms by the MRF may be involved in the alteration of visual cortex receptive fields seen in waking cats [ 2] and in the alteration of sensory function seen in focused attention [15]. Inhibition is thought to play an important role in focusing or sharpening the transduction of sensory information; its modulation at the cortex by the reticular formation could provide a powerful influence on perceptual experience.
REFERENCES
1. Arduini, A. and L. R. Pinneo. Properties of the retina in response to steady illumination. Archs ital. Biol. 100: 425-448, 1962. 2. Bear, D. M., H. Sasaki and F. R. Ervin. Sequential change in receptive fields of striate neurons in dark adapted cats. Expl Brain Res. 13: 256-272, 1971. 3. Bremer, F. Inhibitions intrathalamiques recurrentielles et physiologic du sommeil. Electroenceph. clin. Neurophysiol. 28: 1-16, 1970. 4. Corazza, R., V. Tradardi and C. Umilta. Types of response to steady illumination and levels of neuronal dark discharge in the central visual pathways. Brain Res. 16:121-132, 1969. 5. Courtois, A. and J. P. Cordeau. Changes in cortical responsiveness during transition from sleep to wakefulness. Brain Res. 14: 199-214, 1969. 6, Eccles, J. C. The Inhibitory Pathways o f the Central Nervous System. Springfield, Massachusetts: Charles Thomas, 1969. 7. Evarts, E. V. Neuronal activity in visual and motor cortex during sleep and waking. In: Neurophysiologie des Etats de Sommeil, edited by M. Jouvet. Pads: Centre National de la Recherche Scientifique, 189-212, 1965. 8. Feeney, D. M. and J. M. Orem. Influence of antidromic callosal volleys on single units in visual cortex. Expl Neurol. 33: 310-321, 1971.
9. Fukuda, Y. and K. lwama. Reticular inhibition of internuncial cells in the rat lateral geniculate. Brain Res. 35: 107-120, 1971. 10. Orem, J. M. and D. M. Feeney. Reciprocal reticular influences on cells in rostral and caudal visual cortex of the cat. Brain Res. 30: 200-203, 1971. 11. Otsuka, R. und R. Hassler. Uber Auffau und Gleiderund der corticalen Sehsphare bei der Katz. Archs Psychiat. nervenkr. 203: 212-234, 1962. 12. Purpura, D. and R. J. Shofer. lntraceUular recording from thalamic neurons during reticulocortical activation. J. Neurophysiol. 26: 494-505, 1963. 13. Skrebitsky, V. Postsynaptic inhibition in photically evoked responses and its change during distraction of the animal. Brain Res. 14: 510-512, 1969. 14. Steriade, M., P. Wyzinsky, M. Deschenes and M. Guerin. Disinhibition during waking in motor cortex neuronal chains in cat and monkey. Brain Res. 30: 211-217, 1971. 15. Young, D. N., G. D. Ellison and D. M. Feeney. Electrophysiological correlates of selective attention: Modality specific changes in thalamocortical evoked potentials. Brain Res. 28: 501-510, 1971.