EXPERIMENTAL
NEUROLOGY
51,
41-53 (1976)
Effects of Visual Attention on the Intensity of Auditory Evoked Potentials LYNN II. S. Amy Aberdeen Receiwd
October
Human Proving 1,1975,
C. OATMAN~ Esgineering Laboratory, Maryland 21005
G~ozltzd,
revisio?t
rrceizlcd Decmzber
9,1975
Click-evoked potentials were recorded from the round window (cochlear microphonic and auditory nerve), cochlear nucleus, and auditory cortex of unanesthetized cats during periods of visual attention and increased auditory intensity. The clicks (irrelevant stimuli) were presented continuously as background before, during, and after the presentation of a visual discrimination task (relevant stimuli) which attempted to alter the attentive state of the animals. At all electrode sites, the mean peak-to-peak amplitudes of click-evoked potentials were significantly smaller during attention to the visual discrimination stimuli when compared with the pretest and posttest control periods. Although the amplitudes of the click-evoked potentials were suppressed at all intensities during visual attention, much greater suppression occurred at low auditory intensities than at high auditory intensities. The results suggest that during attention, a central inhibitory mechanism suppresses irrelevant auditory stimuli presumably via the olivo-cochlear bundle at the peripheral stages in the afferent auditory pathways.
INTRODUCTION The effect of attention on afferent sensory information has been shown to produce a variety of behavioral and neurophysiological results (7, 12, 13, 16, 30). When an organism is engaged in attentive behavior, a selective process occurs within the central nervous system where relevant sensory stimuli are perceived and irrelevant stimuli are rejected (12). Some stimuli are suppressedat very early stages in the afferent auditory pathways (13, 16) and sensory information is transmitted to the auditory cortex only after having been subjected to a “filtering” at a peripheral level. described herein, the investigator adhered to the for Laboratovy Animal Resources, National Academy of Sciences, National Research Council, Washington, D.C. The author and the gratefully acknowledges the electronic assistance of Joseph Mazurczak assistance of Janet L. Makarevich and Timothy G. Coughlin in reducing the data. 1 In conducting
Guide
for
Laboratory
the research A&au1
Facilities
41 Copyright All rights
0 1976 by Academic Press, of reproduction in any form
Inc. reserved.
42
LYNN
C.
OATMAN
Auditory evoked potentials can be attenuated by peripheral processes which regulate auditory stimuli either through middle-ear muscle contractions (5, 14, 25) or through the action of the olivo-cochlear bundle (3). The existence of a descending neural pathway from the region of the superior olivary nuclei to the hair cells in the cochlea has been firmly established anatomically (20,21) , Electrical stimulation of the olivo-cochlear bundle in the region of the fourth ventricle results in suppression of the auditory nerve action potential as recorded from the round window (6, S-10) and decreases the firing rate of single fibers of the auditory nerve (9, 29). This evidence has led to the notion that the bundle performs an inhibitory function which controls auditory stimuli to the central nervous system at the peripheral level. Guzman-Flores and Alcaraz (11) showed that lesion of the olivocochlear bundle abolishes the attenuation of cochlear nucleus evoked potentials during attentive behavior to a visual stimulus, which suggests that the auditory and visual systems are connected via the bundle. Burro et al. (3) h ave presented the first direct evidence that the olivocochlear bundle inhibits auditory input at the receptor level. They reported that in unanesthetized guinea pigs, both the cochlear microphonic and auditory nerve (N1) amplitudes recorded from the round window were decreased during habituation and distraction experiments. However, these changes associated with habituation and distraction were not observed after sectioning the crossed olivocochlear bundle. Oatman (19) observed that auditory evoked potentials at the receptor level and the cortical level are suppressed in amplitude while an animal, whose middle-ear muscles have been severed, is attending to visual stimulation. Oatman suggested that a central inhibitory mechanism terminating in the bundle suppressed click-evoked potentials at the receptor level in the unanesthetized animal during attention to visual stimulation. However, those results were obtained to click stimuli presented at a single intensity, 90 db SPL (re 0.0002 microbar). To establish the generality of Oatman’s results, it is necessary to examine the amount of suppression in the auditory pathway to different click-stimuli intensities. The aim of the present study was to determine the amount of attenuation of the auditory evoked potentials as a function of increased stimulus intensity while the animals, whose middle-ear muscles have been severed, are attending to visual stimulation. METHODS Subjects and Sztrgical Procedure. Four female cats, each weighing approximately 2.5 kg, had electrodes placed on the round window and bilaterally in the cochlear nucleus and auditory cortex under sodium pentobarbital anesthesia (0.5 cc/kg at a concentration of 65 mg/cc). The
VISUAL
ATTENTION
AND
EVOKED
RESPONSE
43
cochlear nucleus electrodes were stereotaxically implanted through small holes bored in the skull according to coordinates in the stereotaxic atlas of Snider and Niemer (23). The electrodes were concentric and were made of 0.0254-cm Formvar-coated stainless-steel wire inserted into 25-gauge hypodermic stock. Both the wire and the hypodermic stock were insulated with vinyl coating (Stoner-Mudge) up to 1 mm from the tip; the tips were 1 mm apart. The auditory cortex electrodes were flattened monopolar silver-ball electrodes placed on the dura over the auditory cortex. The round window electrode was a 0.0254-cm ball-tipped stainless-steel wire in polyethylene tubing. The indifferent electrode was a stainless-steel screw over the frontal sinus, and another stainless-steel screw at the posterior part of the skull was used as an internal ground for the animal. After the electrodes were fixed to the skull with dental cement, the cat was removed from the stereotaxic apparatus and placed into a head holder where a stainless-steel ball electrode was implanted on the round window of each cat. After the electrode was in place and anchored to the wall of the bulla, it was led under the skin to the top of the head, where all electrodes were terminated in a 1Ppin Amphenol connector on the vertex of the skull. The assembly was fixed to the skull with dental cement. At the time of the round window implantation, the tendons of the stapedius and tensor tympani muscles were cut. Histology. At the end of the experiment, the cats were killed with an overdose of Lethane administered intravenously. Electrolytic lesions were produced at the recording sites of each concentric electrode. The lesion current was 1 mA for 15 sec. The brain was removed and placed in formalin and potassium ferrocyanide for 24 hr. All placements were verified histologically using unstained, frozen sections (22). For all four cats the histology slides confirmed that the electrodes were placed in the cochlear nucleus. Middle ears were examined with a Bausch and Lomb stereozoom seven dissecting microscope to determine that the middle-ear muscle tendons had been completely severed. I/&al and Acoustic Stimulation. The tests were made in a soundattenuating chamber which had a visual display mounted on one end wall, a response key and a liquid food dipper mounted in the floor, and a driver, with sound tube attached, mounted in the top of the box. The cats’ task was to learn the visual discrimination for food reinforcement, They were gradually deprived of food until they were on a 22-hour deprivation schedule. Then they learned the visual discrimination task, with Purina tuna mixed with water as food reinforcement. All cats received either 100 trials or 50 food reinforcements, each day of training until they reached a criterion of 20 consecutive correct responses. After testing, the cats were given free access to Purina cat chow for 1 hr.
44
LYNN
C. OATMAN
t, -
n
-FIG.
1. Schematic
diagram
of the stimulus
presentation.
The visual stimuli consisted of concentric rings presented successively for discrimination. The large outer ring was 0.3185 cm wide and had a diameter of 2.54 cm, and the small inner ring was 0.3185 cm wide with a diameter of 1.905 cm. Luminance measurements were made on the stimulus figures with a Pritchard spectrophotometer (model 1970-PR). The luminance was 7.17 ft-L for the outer ring and 8.47 it-L for the inner ring. Figure 1 shows a schematic diagram of the stimulus presentation. The large outer ring was presented first, which served as a warning stimulus for the cat to attend to the stimuli. Then the smaller inner ring was presented. The cat had to respond to the onset of the small inner ring to receive food reward. If the cat responded between the onset of the large outer ring and the onset of the small inner ring, it received no reinforcement and the onset of the next trial was delayed 25 sec. To increase the cats’ attentiveness and avoid temporal conditioning, the temporal interval (tl) between onset of the large and small concentric rings was varied randomly between 1 and 6 sec. The exposure duration of the small inner concentric ring was 4 set and the time between trials was 25 sec. Auditory clicks were presented continuously at a rate of l/set during presentation of the successive visual discrimination tasks, but they were not synchronized with onset of the visual display. The auditory clicks were generated by a 90-psec square-wave pulse (Tektronix type 162 and 163). The pulses were led through a high-pass filter (Allison Laboratories model Z-B, 4800 Hz), and through a decade attenuator (General Radio type GR-1450) and a power amplifier (Dynakit Mark III) to a highfrequency driver (University model HF-206). Clicks were presented through a sound-tube system which terminated at the entrance to the cat’s external meatus. The sound tube was not fastened to the pinna but was held firmly in place by a bracket attached to the electrode plug (IS). Clicks were presented at a rate of l/set at each lo-db intensity step from 45 to 135 db SPL (re 0.0002 microbar j . Sound pressure measurements were made in the sound-attenuating cubicle, where a calibrated
VISUAL
ATTENTION
AND
EVOKED
45
RESPONSE
0.635-cm condenser microphone (Briiel and Kjaer type 4135) was placed perpendicular to and just in front of the end of the sound tube. Movements of the sound tube to different positions within the cubicle did not change the output voltage from the microphone. Data Collection and Procedure. Simultaneous recordings were obtained from the round window (cochlear microphonics and auditory nerve responses), the cochlear nucleus, and the auditory cortex to click stimuli. Recordings were obtained from unrestrained animals via a Microdot shielded cable connected to an electroencephalograph (Grass model 7) placed outside the sound-attenuating cubicle. At the same time, the clickevoked potentials were recorded on a 14-channel FM tape recorder (Sangamo 4700) from which they were led into a signal averager (FabriTek model 1074) and written on an X-Y plotter (Hewlett-Packard 7035B). Four weeks after operation, the cats were placed into the cubicle and the electrodes were checked. Figure 2 shows an example of the clickevoked responses from the round window (CM and N1-N2), cochlear nucleus and auditory cortex and indicates how the peak-to-peak measurement was made for each electrode placement. Peak-to-peak amplitudes of the averaged evoked responses were measured by ruler to the nearest 5 pV. Evoked potentials influenced by bodily movement as observed in the EEG were discarded from the data. After the electrodes were checked, the data were collected in recording sessions consisting of a control period, an experimental period, and a control period, which were designed to alter the attentive state of the animals. The data were collected under three different attentive states: (i) a pretest control in which the cat was awake, relaxed, and not attentive to any identifiable stimuli, (ii) an experimental period during presenta-
25 MSEC
WINDOW FIG.
nucleus, phonics to-peak
NUCLEUS
AUDITORY CORTEX
2. Averaged click-evoked responses recorded from the round window, cochlear and auditory cortex. (The round window wave form shows cochlear micro(CM) and auditory nerve (N,-N,) responses to a single click. The peakconventions used to quantify the evoked potentials are noted.)
46
LYNN
C.
OATMAN
tion of the visual discrimination stimuli between the concentric rings when the cat was attentive, and (iii) a posttest control period similar to the pretest control period. The evoked responses to clicks were averaged on the signal averager for each of the three different attentive states, i.e., while the cat was relaxed, while attending to the visual discrimination, and when relaxed again. The click-evoked responses, averaged while the cat was attending to the visual discrimination, included only those evoked potentials presented between the onset of the large outer concentric ring and the presentation of the small inner concentric ring when appropriate behavioral responses were obtained to the visual stimuli (Fig. 1). Evoked responses for each of the three different attentive states were then collected at each IO-db intensity step in an ascending order of presentation from 4.5 to 13.5 db SPL (re 0.0002 microbar). RESULTS The data consist of averages of 64 click-evoked potentials from three electrode locations : round window (cochlear microphonics and auditory nerve), cochlear nucleus, and auditory cortex. The data plotted in Figs. 3 through 6 are averages obtained from 256 measurements from each elec-
o/.’
M a)- - - m-0
PRETEST CONTROL EXPERlMENTAL
-
POSTTEST
INTENSITY
AUDITORY FIG. 3. The mean peak-to-peak amplitude microvolts as a function of intensity (db)
CONTROL
( d B)
CORTEX
of auditory and attentive
cortex state.
evoked
potentials
in
VISUAL
ATTENTION
AND
EVOKED
RESPONSE
47
INTENSITY Cd 8)
COCHLEAR
NUCLEUS
FIG. 4. The mean peak-to-peak amplitude of cochlear nucleus evoked potentials in microvolts as a function of intensity (db) and attentive state.
trode placement recorded on each of four cats. These figures show the average peak-to-peak amplitudes of the auditory responses plotted as a function of intensity for each of the three attentive states: pretest-control group (cat nonattentive, relaxed but awake), experimental group (during visual discrimination, cat very attentive), and posttest-control group (cat nonattentive, relaxed but awake). Figure 3 shows that the mean peak-to-peak amplitudes of click-evoked potentials recorded from auditory cortex were of a smaller amplitude when the cats were very attentive to the visual discrimination than when they were nonattentive. An analysis of variance (4) indicated significant differences between the pretest-control group and the experimental group (F = 44.81, df = l/60) and between the posttest-control group and the
experimental group (F =41.84, df = l/60). An analysis of variance indicated no significant differences between the pretest-control group and the posttest-control group (F < 1). The data (Fig. 3) show that, although the amplitudes of the auditory cortex evoked potentials are suppressed at all intensities during visual attention, much greater suppression occurred at low auditory intensities than at the high intensities. Whereas analysis of variance between the
pretest-control group and the experimental group was significant for the
48
LYNN
C.
OATMAN
AUDITORY
NERVE
FIG. 5. The mean peak-to-peak amplitude of auditory nerve (N,) microvolts as a function of intensity (db) and attentive state.
responses in
intensities 45 to 135 db SPL, an analysis of variance showed no significant differences between the pretest-control group and the experimental group for intensities 105 to 135 db SPL (F = 3.40, df = l/24). The mean peak-to-peak amplitudes of the cochlear nucleus responsesas a function of attentive state and increased intensity appear in Fig. 4. Figure 4 shows that when the attention of the animals was focused on the visual discrimination, mean peak-to-peak amplitudes of the cochlear nucleus were also reduced. Analysis of variance indicated significant differences between the pretest-control group and the experimental group (F = 25.53, df = l/60) and between the posttest-control group and the experimental group, (F = 30.10, df = l/60), but no significant differences between the (F < 1) pretest-control group and the posttest-control group. Figure 4 also shows that greater reduction in evoked potentials occurred at low auditory intensities than at the higher auditory intensities. The analysis of variance between the pretest-control group and the experimental group was significant for the intensities 45 to 135 db SPL, however, an analysis of variance indicated no significant differences between the pretest-control group and experimental group for intensities 95 to 135
db SPL (F = 3.31, df = l/30).
VISUAL
ATTENTION
I
*
45
AND
EVOKED
I
I
I
I
55
55
75
85
INTENSITY
6. The mean peak-to-peak as a function of intensity (db) FIG.
I
95
49
RESPONSE
I
I
105
115 125 135
I
,
t dB)
COCHLEAR
MICROPHONIC
amplitude and attentive
of cochlear state.
microphonics
in
microvolts
Figure 5 shows the mean peak-to-peak amplitudes of the N1 responses as a function of increased intensity and attentive state. Again the mean peak-to-peak N1 responseswere reduced in amplitude when the animals were attentive to the visual discrimination task. Analysis of variance indicated significant differences between the pretest-control group and the experimental group (F = 91.47, df = l/60) and the posttest-control and the experimental group (F = 101.67, df = l/60) ; however, no significant differences were found between the pretest-control group and the posttest-control group (F = 1.36, df = l/60). Figure 5 shows a greater reduction in amplitudes of the auditory nerve responsesat low auditory intensities than at the higher auditory intensities. Analysis of variance between the pretest-control group and the experimental group indicated significant differences for the intensities 45 to 135 db SPL, but, no significant differences for the intensities 115 to 13.5 db SPL (F = 1.27, df = l/18). The mean peak-to-peak amplitudes of the cochlear microphonic responses as a function of attentive state and increased intensity appear in Fig. 6, which shows that the mean peak-to-peak cochlear microphonic responseswere not changed in amplitude when the animals were attentive to the visual discrimination task. Analysis of variance indicated no significant differences between the pretest-control group and the experimental group (F < 1) or between the posttest-control and the experimental group (F < 1).
50
LYNN
C.
OATMAN
DISCUSSION The results indicate that the attentive state of the animal significantly affects the amplitude of click-evoked responses recorded along the auditory pathway. It is apparent that when cats were attentive to the visual discrimination, the amplitudes of click-evoked potentials recorded from the auditory cortex, cochlear nucleus, and auditory nerve (N1) were significantly smaller than when the cats were nonattentive. These data are consistent with the electrophysiological evidence of Galambos (10) and Desmedt (6), who have shown that electrical stimulation of the crossed olivocochlear bundle suppressed the Nr responses to clicks, and the findings of Starr (25) and Moushegian et al. (17)) who observed a decrease in amplitude of click-evoked responses at the cortex with middle-ear muscles cut. These data are also consistent with the previous findings of Oatman (19)) who observed that when the cats’ attention was focused on the visual discrimination stimuli, amplitudes of the auditory cortex, cochlear nucleus, and Nr responses were suppressed. The data suggest that the changes in amplitude as a function of increased attention are due to a central inhibitory mechanism which influences Nr responses at the hair-cell level in the cochlea, but does not influence the cochlear microphonic. Presumably, attention to the visual discrimination task activates a central inhibitory mechanism which suppresses auditory stimuli by the olivo-cochlear bundle. This suggestion is supported by Igarashi et al. ( 15), who observed that elimination of the crossed olivocochlear bundle resulted in a significant increase in white noise distraction during a visual detection task in the cat. In the present experiment the data also indicate that when the animals are attentive to the visual discrimination stimuli, the amount of suppression of the auditory evoked potentials changes as a function of increased auditory intensity. In this experiment a greater reduction in the amplitude of click-evoked potentials recorded from auditory cortex, cochlear nucleus, and auditory nerve (Nr) was observed at low auditory intensities than at the high auditory intensities. This finding is in agreement with Sohmer (24) and Wiederhold and Peake (28)) who have demonstrated that electrical stimulation of the crossed olivocochlear bundle in anesthetized cats reduces the amplitude of N1 responses for low auditory intensities, but the same stimulation did not diminish the amplitudes of N1 responses for the high auditory intensities. The control procedures used in the present study were designed to insure a constant stimulus input to the auditory system (30), to eliminate the effects of the middle-ear muscles (5, 14, 25), and to obtain visual attention in the cats. A constant stimulus input to the auditory system was
VISUAL
ATTENTION
AND
EVOKED
RESPONSE
51
accomplished by running a sound tube adjacent to the recording cable and terminating the sound in the entrance of the auditory meatus. Examination of the cochlear microphonics in Fig, 6 reveals little change in the amplitude of the cochlear microphonic between the different attentive states. Since the microphonics show little change in amplitude as a function of increased attention, the obtained results could not be attributed to differences in the intensity of the auditory stimulus during the different attentive states. In the past little regard has been given to the procedure used in getting an animal to attend to a visual stimulus. Visual attention has been defined as the introduction of mice in a bottle (10, 13), the experimenter distracting the cat in one way or another (17), or the use of novel light flashes (27). The attention span may be very short, and perhaps the problem with previous attention-getting techniques may be that they were too long for the animals’ attention span. To obtain better control over attentive behavior, a successive visual discrimination task was used in this experiment during the attentive condition. The cats were assumed to be exhibiting attentive behavior when they responded appropriately in the visual discrimination task. Baust, Berlucchi, and Moruzzi (1) and Berlucchi, Munson, and Rizzolatti (2) observed that in cats with middle-ear muscles cut, the evoked responses to clicks recorded from the round window (Nl) and the cochlear nucleus remain unchanged to different arousal levels observed in sleeping and waking cycles. However, Wickelgren (26) observed that auditory cortex click-evoked potentials were decreased during similar arousal conditions in animals with middle-ear muscles cut. These present findings have added to a long-standing controversy regarding the interpretation of reductions in auditory evoked responses during attention experiments. In these experiments, when an animal is conditioned to become attentive to a specific stimulus, the animal’s general level of arousal may increase simultaneously. The controversy then becomes whether reductions in click-evoked responses at the auditory cortex are due to selective attention or to changes in arousal. This experiment was not designed to However, the descending inhibition of the investigate this controversy. olivocochlear bundle could fully account for the reduction in amplitudes of the auditory nerve, cochlear nucleus, and auditory cortex. It is more parsimonious to assume the amplitude reductions at the auditory cortex are due to auditory nerve and cochlear nucleus reductions than due to independent cortical and peripheral arousal systems. The observed results in this experiment are thought to be due entirely to possible olivocochlear inhibition as a result of visual attention rather than to shifts in general level of arousal as seen in sleeping and waking states.
52
LYNN
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OATMAN
In summary, the results of the present experiment are due to the attentive state of the animal. Apparently, the role of attention in sensory perception is to initiate within the central nervous system a gating mechanism in which the evoked potentials of irrelevant sensory stimuli are inhibited. This gating mechanism involves at least two inhibitory systems which participate in modifying sensory input at the peripheral stages in the afferent auditory pathways. One system, a reticular feedback system, suppresses irrelevant auditory stimuli through middle-ear muscle contractions. The other system suppresses irrelevant auditory stimuli presumably via the olivocochlear bundle, affecting the auditory nerve responses but not the cochlear microphonics at the hair-cell level in the cochlea. This system may be either an extrareticular feedback system or a presently unknown reticular system capable of functioning with the middle-ear muscles severed. REFERENCES 1. BAUST, W.. C. BERLUCCHI, and G. MOR~ZZI. 1964. Changes in the auditory input in wakefulness and during the synchronized and desynchronized stages of sleep. Arch. Ital. Biol. 102: 657-674. 2. BERLUCCHI, G., J. B. MUNSON, and G. RIZZOLATTI. 1967. Changes in clickevoked responses in the auditory system and the cerebellum of free-moving cats during sleep and waking. Arclt. Ifal. Biol. 105: 118-135. 3. B~No, W., R. VELLUTI, P. HANDLER, and E. GARCIA-AUSST. 1966. Neural control of the cochlear input in the wakeful free guinea pig. Physiol. and Behav. 1: 23-35. 4. BUTLER, D. H., A. S. KAMLET, and R. A. MONTY. 1969. A multipurpose analysis of variance FORTRAN IV computer program. Psychon. Monograph S21pp. 2 : 301-319. 5. CARMEL, P. W., and A. STARR. 1963. Acoustic and non-acoustic factors modifying middle-ear muscle activity in waking cats. J. Nezlrophysiol. 26: 598-616. 6. DESMEDT, J. E. 1962. Auditory-evoked potentials from cochlea to cortex as influenced by activation of the efferent olivo-cochlear bundle. J. ACOUS~. Sot. Am. 34: 1478-1496. 7. DUNLOP, C. W., W. R. WEBSTER, and L. A. SIMONS. 1965. Effect of attention on evoked responses in the classical auditory pathway. Nature 206: 1048-1050. 8. FEX, J. 1959. Augmentation of cochlear microphonics by stimulation of efferent fibers to the cochlea. Arfa Ofolaryng. 50: 540-541. 9. FEX, J. 1962. Auditory activity in centrifugal and centripetal cochlear fibers in cat. Acfa Physiol. Stand., 55: .Sufipl. 189, l-68. 10. GALAMBOS, R. 1956. Suppression of the auditory nerve activity by stimulation of efferent fibers to cochlea. .I. Nezrrophysiol. 19: 424-437. 11. GUZMAN-FLORES, C., and M. ALCARAZ. 1963. Funcion de la cintilla olivo coclear en el fenomeno de distraction a estimulos acusticos. Nota preliminar. Bol. Inst. Esfzld. Med. Biol. 21: 87-92. 12. HERNANDEZ-PEON, R. 1966. Physiological mechanisms in attention, pp. 121-144. In “Frontiers in Physiological Psychology.” R. W, Russell [Ed.]. Academic Press, New York, New York.
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13. HERNANDEZ-PEON, R., H. SCHERRER, and M. JOUVET. 1956. Modification of electrical activity in cochlear nucleus during “attention” in unanesthetized cats. Science 123 : 331-332. 14. HUGELIN, A., S. DUMONT, and N. PAILLAS. 1960. Tympanic muscles and control of auditory input during arousal. Science 131: 1371-1372. 15. IGARASHI, M., B. R. ALFORD, W. P. GORDON, and Y. NAKAI. 1974. Behavioral auditory function after transection of crossed olivocochlear bundle in the cat. Acta Otolaryftg. 77 : 311-317. 16. JOUVET, M., and R. HERNANDEZ-PEON. 1957. Mechanismes neurophysiologiques concernant I’habituation, l’attention, et le conditionment. Electroenceph. Clin. Newophysiol. 6 : 39-49. 17. MOUSHEGIAN, G., A. RUPERT, J. T. MARSH, and R. GALAMBOS. 1961. Evoked cortical potentials in absence of middle-ear muscles. Science 133: 582-583. 18. OATMAN, L. C. 1%8. The effect of attention on auditory evoked
NEUROLOGY
51,
41-53 (1976)
Effects of Visual Attention on the Intensity of Auditory Evoked Potentials LYNN II. S. Amy Aberdeen Receiwd
October
Human Proving 1,1975,
C. OATMAN~ Esgineering Laboratory, Maryland 21005
G~ozltzd,
revisio?t
rrceizlcd Decmzber
9,1975
Click-evoked potentials were recorded from the round window (cochlear microphonic and auditory nerve), cochlear nucleus, and auditory cortex of unanesthetized cats during periods of visual attention and increased auditory intensity. The clicks (irrelevant stimuli) were presented continuously as background before, during, and after the presentation of a visual discrimination task (relevant stimuli) which attempted to alter the attentive state of the animals. At all electrode sites, the mean peak-to-peak amplitudes of click-evoked potentials were significantly smaller during attention to the visual discrimination stimuli when compared with the pretest and posttest control periods. Although the amplitudes of the click-evoked potentials were suppressed at all intensities during visual attention, much greater suppression occurred at low auditory intensities than at high auditory intensities. The results suggest that during attention, a central inhibitory mechanism suppresses irrelevant auditory stimuli presumably via the olivo-cochlear bundle at the peripheral stages in the afferent auditory pathways.
INTRODUCTION The effect of attention on afferent sensory information has been shown to produce a variety of behavioral and neurophysiological results (7, 12, 13, 16, 30). When an organism is engaged in attentive behavior, a selective process occurs within the central nervous system where relevant sensory stimuli are perceived and irrelevant stimuli are rejected (12). Some stimuli are suppressedat very early stages in the afferent auditory pathways (13, 16) and sensory information is transmitted to the auditory cortex only after having been subjected to a “filtering” at a peripheral level. described herein, the investigator adhered to the for Laboratovy Animal Resources, National Academy of Sciences, National Research Council, Washington, D.C. The author and the gratefully acknowledges the electronic assistance of Joseph Mazurczak assistance of Janet L. Makarevich and Timothy G. Coughlin in reducing the data. 1 In conducting
Guide
for
Laboratory
the research A&au1
Facilities
41 Copyright All rights
0 1976 by Academic Press, of reproduction in any form
Inc. reserved.
42
LYNN
C.
OATMAN
Auditory evoked potentials can be attenuated by peripheral processes which regulate auditory stimuli either through middle-ear muscle contractions (5, 14, 25) or through the action of the olivo-cochlear bundle (3). The existence of a descending neural pathway from the region of the superior olivary nuclei to the hair cells in the cochlea has been firmly established anatomically (20,21) , Electrical stimulation of the olivo-cochlear bundle in the region of the fourth ventricle results in suppression of the auditory nerve action potential as recorded from the round window (6, S-10) and decreases the firing rate of single fibers of the auditory nerve (9, 29). This evidence has led to the notion that the bundle performs an inhibitory function which controls auditory stimuli to the central nervous system at the peripheral level. Guzman-Flores and Alcaraz (11) showed that lesion of the olivocochlear bundle abolishes the attenuation of cochlear nucleus evoked potentials during attentive behavior to a visual stimulus, which suggests that the auditory and visual systems are connected via the bundle. Burro et al. (3) h ave presented the first direct evidence that the olivocochlear bundle inhibits auditory input at the receptor level. They reported that in unanesthetized guinea pigs, both the cochlear microphonic and auditory nerve (N1) amplitudes recorded from the round window were decreased during habituation and distraction experiments. However, these changes associated with habituation and distraction were not observed after sectioning the crossed olivocochlear bundle. Oatman (19) observed that auditory evoked potentials at the receptor level and the cortical level are suppressed in amplitude while an animal, whose middle-ear muscles have been severed, is attending to visual stimulation. Oatman suggested that a central inhibitory mechanism terminating in the bundle suppressed click-evoked potentials at the receptor level in the unanesthetized animal during attention to visual stimulation. However, those results were obtained to click stimuli presented at a single intensity, 90 db SPL (re 0.0002 microbar). To establish the generality of Oatman’s results, it is necessary to examine the amount of suppression in the auditory pathway to different click-stimuli intensities. The aim of the present study was to determine the amount of attenuation of the auditory evoked potentials as a function of increased stimulus intensity while the animals, whose middle-ear muscles have been severed, are attending to visual stimulation. METHODS Subjects and Sztrgical Procedure. Four female cats, each weighing approximately 2.5 kg, had electrodes placed on the round window and bilaterally in the cochlear nucleus and auditory cortex under sodium pentobarbital anesthesia (0.5 cc/kg at a concentration of 65 mg/cc). The
VISUAL
ATTENTION
AND
EVOKED
RESPONSE
43
cochlear nucleus electrodes were stereotaxically implanted through small holes bored in the skull according to coordinates in the stereotaxic atlas of Snider and Niemer (23). The electrodes were concentric and were made of 0.0254-cm Formvar-coated stainless-steel wire inserted into 25-gauge hypodermic stock. Both the wire and the hypodermic stock were insulated with vinyl coating (Stoner-Mudge) up to 1 mm from the tip; the tips were 1 mm apart. The auditory cortex electrodes were flattened monopolar silver-ball electrodes placed on the dura over the auditory cortex. The round window electrode was a 0.0254-cm ball-tipped stainless-steel wire in polyethylene tubing. The indifferent electrode was a stainless-steel screw over the frontal sinus, and another stainless-steel screw at the posterior part of the skull was used as an internal ground for the animal. After the electrodes were fixed to the skull with dental cement, the cat was removed from the stereotaxic apparatus and placed into a head holder where a stainless-steel ball electrode was implanted on the round window of each cat. After the electrode was in place and anchored to the wall of the bulla, it was led under the skin to the top of the head, where all electrodes were terminated in a 1Ppin Amphenol connector on the vertex of the skull. The assembly was fixed to the skull with dental cement. At the time of the round window implantation, the tendons of the stapedius and tensor tympani muscles were cut. Histology. At the end of the experiment, the cats were killed with an overdose of Lethane administered intravenously. Electrolytic lesions were produced at the recording sites of each concentric electrode. The lesion current was 1 mA for 15 sec. The brain was removed and placed in formalin and potassium ferrocyanide for 24 hr. All placements were verified histologically using unstained, frozen sections (22). For all four cats the histology slides confirmed that the electrodes were placed in the cochlear nucleus. Middle ears were examined with a Bausch and Lomb stereozoom seven dissecting microscope to determine that the middle-ear muscle tendons had been completely severed. I/&al and Acoustic Stimulation. The tests were made in a soundattenuating chamber which had a visual display mounted on one end wall, a response key and a liquid food dipper mounted in the floor, and a driver, with sound tube attached, mounted in the top of the box. The cats’ task was to learn the visual discrimination for food reinforcement, They were gradually deprived of food until they were on a 22-hour deprivation schedule. Then they learned the visual discrimination task, with Purina tuna mixed with water as food reinforcement. All cats received either 100 trials or 50 food reinforcements, each day of training until they reached a criterion of 20 consecutive correct responses. After testing, the cats were given free access to Purina cat chow for 1 hr.
44
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t, -
n
-FIG.
1. Schematic
diagram
of the stimulus
presentation.
The visual stimuli consisted of concentric rings presented successively for discrimination. The large outer ring was 0.3185 cm wide and had a diameter of 2.54 cm, and the small inner ring was 0.3185 cm wide with a diameter of 1.905 cm. Luminance measurements were made on the stimulus figures with a Pritchard spectrophotometer (model 1970-PR). The luminance was 7.17 ft-L for the outer ring and 8.47 it-L for the inner ring. Figure 1 shows a schematic diagram of the stimulus presentation. The large outer ring was presented first, which served as a warning stimulus for the cat to attend to the stimuli. Then the smaller inner ring was presented. The cat had to respond to the onset of the small inner ring to receive food reward. If the cat responded between the onset of the large outer ring and the onset of the small inner ring, it received no reinforcement and the onset of the next trial was delayed 25 sec. To increase the cats’ attentiveness and avoid temporal conditioning, the temporal interval (tl) between onset of the large and small concentric rings was varied randomly between 1 and 6 sec. The exposure duration of the small inner concentric ring was 4 set and the time between trials was 25 sec. Auditory clicks were presented continuously at a rate of l/set during presentation of the successive visual discrimination tasks, but they were not synchronized with onset of the visual display. The auditory clicks were generated by a 90-psec square-wave pulse (Tektronix type 162 and 163). The pulses were led through a high-pass filter (Allison Laboratories model Z-B, 4800 Hz), and through a decade attenuator (General Radio type GR-1450) and a power amplifier (Dynakit Mark III) to a highfrequency driver (University model HF-206). Clicks were presented through a sound-tube system which terminated at the entrance to the cat’s external meatus. The sound tube was not fastened to the pinna but was held firmly in place by a bracket attached to the electrode plug (IS). Clicks were presented at a rate of l/set at each lo-db intensity step from 45 to 135 db SPL (re 0.0002 microbar j . Sound pressure measurements were made in the sound-attenuating cubicle, where a calibrated
VISUAL
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RESPONSE
0.635-cm condenser microphone (Briiel and Kjaer type 4135) was placed perpendicular to and just in front of the end of the sound tube. Movements of the sound tube to different positions within the cubicle did not change the output voltage from the microphone. Data Collection and Procedure. Simultaneous recordings were obtained from the round window (cochlear microphonics and auditory nerve responses), the cochlear nucleus, and the auditory cortex to click stimuli. Recordings were obtained from unrestrained animals via a Microdot shielded cable connected to an electroencephalograph (Grass model 7) placed outside the sound-attenuating cubicle. At the same time, the clickevoked potentials were recorded on a 14-channel FM tape recorder (Sangamo 4700) from which they were led into a signal averager (FabriTek model 1074) and written on an X-Y plotter (Hewlett-Packard 7035B). Four weeks after operation, the cats were placed into the cubicle and the electrodes were checked. Figure 2 shows an example of the clickevoked responses from the round window (CM and N1-N2), cochlear nucleus and auditory cortex and indicates how the peak-to-peak measurement was made for each electrode placement. Peak-to-peak amplitudes of the averaged evoked responses were measured by ruler to the nearest 5 pV. Evoked potentials influenced by bodily movement as observed in the EEG were discarded from the data. After the electrodes were checked, the data were collected in recording sessions consisting of a control period, an experimental period, and a control period, which were designed to alter the attentive state of the animals. The data were collected under three different attentive states: (i) a pretest control in which the cat was awake, relaxed, and not attentive to any identifiable stimuli, (ii) an experimental period during presenta-
25 MSEC
WINDOW FIG.
nucleus, phonics to-peak
NUCLEUS
AUDITORY CORTEX
2. Averaged click-evoked responses recorded from the round window, cochlear and auditory cortex. (The round window wave form shows cochlear micro(CM) and auditory nerve (N,-N,) responses to a single click. The peakconventions used to quantify the evoked potentials are noted.)
46
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tion of the visual discrimination stimuli between the concentric rings when the cat was attentive, and (iii) a posttest control period similar to the pretest control period. The evoked responses to clicks were averaged on the signal averager for each of the three different attentive states, i.e., while the cat was relaxed, while attending to the visual discrimination, and when relaxed again. The click-evoked responses, averaged while the cat was attending to the visual discrimination, included only those evoked potentials presented between the onset of the large outer concentric ring and the presentation of the small inner concentric ring when appropriate behavioral responses were obtained to the visual stimuli (Fig. 1). Evoked responses for each of the three different attentive states were then collected at each IO-db intensity step in an ascending order of presentation from 4.5 to 13.5 db SPL (re 0.0002 microbar). RESULTS The data consist of averages of 64 click-evoked potentials from three electrode locations : round window (cochlear microphonics and auditory nerve), cochlear nucleus, and auditory cortex. The data plotted in Figs. 3 through 6 are averages obtained from 256 measurements from each elec-
o/.’
M a)- - - m-0
PRETEST CONTROL EXPERlMENTAL
-
POSTTEST
INTENSITY
AUDITORY FIG. 3. The mean peak-to-peak amplitude microvolts as a function of intensity (db)
CONTROL
( d B)
CORTEX
of auditory and attentive
cortex state.
evoked
potentials
in
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47
INTENSITY Cd 8)
COCHLEAR
NUCLEUS
FIG. 4. The mean peak-to-peak amplitude of cochlear nucleus evoked potentials in microvolts as a function of intensity (db) and attentive state.
trode placement recorded on each of four cats. These figures show the average peak-to-peak amplitudes of the auditory responses plotted as a function of intensity for each of the three attentive states: pretest-control group (cat nonattentive, relaxed but awake), experimental group (during visual discrimination, cat very attentive), and posttest-control group (cat nonattentive, relaxed but awake). Figure 3 shows that the mean peak-to-peak amplitudes of click-evoked potentials recorded from auditory cortex were of a smaller amplitude when the cats were very attentive to the visual discrimination than when they were nonattentive. An analysis of variance (4) indicated significant differences between the pretest-control group and the experimental group (F = 44.81, df = l/60) and between the posttest-control group and the
experimental group (F =41.84, df = l/60). An analysis of variance indicated no significant differences between the pretest-control group and the posttest-control group (F < 1). The data (Fig. 3) show that, although the amplitudes of the auditory cortex evoked potentials are suppressed at all intensities during visual attention, much greater suppression occurred at low auditory intensities than at the high intensities. Whereas analysis of variance between the
pretest-control group and the experimental group was significant for the
48
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AUDITORY
NERVE
FIG. 5. The mean peak-to-peak amplitude of auditory nerve (N,) microvolts as a function of intensity (db) and attentive state.
responses in
intensities 45 to 135 db SPL, an analysis of variance showed no significant differences between the pretest-control group and the experimental group for intensities 105 to 135 db SPL (F = 3.40, df = l/24). The mean peak-to-peak amplitudes of the cochlear nucleus responsesas a function of attentive state and increased intensity appear in Fig. 4. Figure 4 shows that when the attention of the animals was focused on the visual discrimination, mean peak-to-peak amplitudes of the cochlear nucleus were also reduced. Analysis of variance indicated significant differences between the pretest-control group and the experimental group (F = 25.53, df = l/60) and between the posttest-control group and the experimental group, (F = 30.10, df = l/60), but no significant differences between the (F < 1) pretest-control group and the posttest-control group. Figure 4 also shows that greater reduction in evoked potentials occurred at low auditory intensities than at the higher auditory intensities. The analysis of variance between the pretest-control group and the experimental group was significant for the intensities 45 to 135 db SPL, however, an analysis of variance indicated no significant differences between the pretest-control group and experimental group for intensities 95 to 135
db SPL (F = 3.31, df = l/30).
VISUAL
ATTENTION
I
*
45
AND
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I
I
I
I
55
55
75
85
INTENSITY
6. The mean peak-to-peak as a function of intensity (db) FIG.
I
95
49
RESPONSE
I
I
105
115 125 135
I
,
t dB)
COCHLEAR
MICROPHONIC
amplitude and attentive
of cochlear state.
microphonics
in
microvolts
Figure 5 shows the mean peak-to-peak amplitudes of the N1 responses as a function of increased intensity and attentive state. Again the mean peak-to-peak N1 responseswere reduced in amplitude when the animals were attentive to the visual discrimination task. Analysis of variance indicated significant differences between the pretest-control group and the experimental group (F = 91.47, df = l/60) and the posttest-control and the experimental group (F = 101.67, df = l/60) ; however, no significant differences were found between the pretest-control group and the posttest-control group (F = 1.36, df = l/60). Figure 5 shows a greater reduction in amplitudes of the auditory nerve responsesat low auditory intensities than at the higher auditory intensities. Analysis of variance between the pretest-control group and the experimental group indicated significant differences for the intensities 45 to 135 db SPL, but, no significant differences for the intensities 115 to 13.5 db SPL (F = 1.27, df = l/18). The mean peak-to-peak amplitudes of the cochlear microphonic responses as a function of attentive state and increased intensity appear in Fig. 6, which shows that the mean peak-to-peak cochlear microphonic responseswere not changed in amplitude when the animals were attentive to the visual discrimination task. Analysis of variance indicated no significant differences between the pretest-control group and the experimental group (F < 1) or between the posttest-control and the experimental group (F < 1).
50
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DISCUSSION The results indicate that the attentive state of the animal significantly affects the amplitude of click-evoked responses recorded along the auditory pathway. It is apparent that when cats were attentive to the visual discrimination, the amplitudes of click-evoked potentials recorded from the auditory cortex, cochlear nucleus, and auditory nerve (N1) were significantly smaller than when the cats were nonattentive. These data are consistent with the electrophysiological evidence of Galambos (10) and Desmedt (6), who have shown that electrical stimulation of the crossed olivocochlear bundle suppressed the Nr responses to clicks, and the findings of Starr (25) and Moushegian et al. (17)) who observed a decrease in amplitude of click-evoked responses at the cortex with middle-ear muscles cut. These data are also consistent with the previous findings of Oatman (19)) who observed that when the cats’ attention was focused on the visual discrimination stimuli, amplitudes of the auditory cortex, cochlear nucleus, and Nr responses were suppressed. The data suggest that the changes in amplitude as a function of increased attention are due to a central inhibitory mechanism which influences Nr responses at the hair-cell level in the cochlea, but does not influence the cochlear microphonic. Presumably, attention to the visual discrimination task activates a central inhibitory mechanism which suppresses auditory stimuli by the olivo-cochlear bundle. This suggestion is supported by Igarashi et al. ( 15), who observed that elimination of the crossed olivocochlear bundle resulted in a significant increase in white noise distraction during a visual detection task in the cat. In the present experiment the data also indicate that when the animals are attentive to the visual discrimination stimuli, the amount of suppression of the auditory evoked potentials changes as a function of increased auditory intensity. In this experiment a greater reduction in the amplitude of click-evoked potentials recorded from auditory cortex, cochlear nucleus, and auditory nerve (Nr) was observed at low auditory intensities than at the high auditory intensities. This finding is in agreement with Sohmer (24) and Wiederhold and Peake (28)) who have demonstrated that electrical stimulation of the crossed olivocochlear bundle in anesthetized cats reduces the amplitude of N1 responses for low auditory intensities, but the same stimulation did not diminish the amplitudes of N1 responses for the high auditory intensities. The control procedures used in the present study were designed to insure a constant stimulus input to the auditory system (30), to eliminate the effects of the middle-ear muscles (5, 14, 25), and to obtain visual attention in the cats. A constant stimulus input to the auditory system was
VISUAL
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51
accomplished by running a sound tube adjacent to the recording cable and terminating the sound in the entrance of the auditory meatus. Examination of the cochlear microphonics in Fig, 6 reveals little change in the amplitude of the cochlear microphonic between the different attentive states. Since the microphonics show little change in amplitude as a function of increased attention, the obtained results could not be attributed to differences in the intensity of the auditory stimulus during the different attentive states. In the past little regard has been given to the procedure used in getting an animal to attend to a visual stimulus. Visual attention has been defined as the introduction of mice in a bottle (10, 13), the experimenter distracting the cat in one way or another (17), or the use of novel light flashes (27). The attention span may be very short, and perhaps the problem with previous attention-getting techniques may be that they were too long for the animals’ attention span. To obtain better control over attentive behavior, a successive visual discrimination task was used in this experiment during the attentive condition. The cats were assumed to be exhibiting attentive behavior when they responded appropriately in the visual discrimination task. Baust, Berlucchi, and Moruzzi (1) and Berlucchi, Munson, and Rizzolatti (2) observed that in cats with middle-ear muscles cut, the evoked responses to clicks recorded from the round window (Nl) and the cochlear nucleus remain unchanged to different arousal levels observed in sleeping and waking cycles. However, Wickelgren (26) observed that auditory cortex click-evoked potentials were decreased during similar arousal conditions in animals with middle-ear muscles cut. These present findings have added to a long-standing controversy regarding the interpretation of reductions in auditory evoked responses during attention experiments. In these experiments, when an animal is conditioned to become attentive to a specific stimulus, the animal’s general level of arousal may increase simultaneously. The controversy then becomes whether reductions in click-evoked responses at the auditory cortex are due to selective attention or to changes in arousal. This experiment was not designed to However, the descending inhibition of the investigate this controversy. olivocochlear bundle could fully account for the reduction in amplitudes of the auditory nerve, cochlear nucleus, and auditory cortex. It is more parsimonious to assume the amplitude reductions at the auditory cortex are due to auditory nerve and cochlear nucleus reductions than due to independent cortical and peripheral arousal systems. The observed results in this experiment are thought to be due entirely to possible olivocochlear inhibition as a result of visual attention rather than to shifts in general level of arousal as seen in sleeping and waking states.
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In summary, the results of the present experiment are due to the attentive state of the animal. Apparently, the role of attention in sensory perception is to initiate within the central nervous system a gating mechanism in which the evoked potentials of irrelevant sensory stimuli are inhibited. This gating mechanism involves at least two inhibitory systems which participate in modifying sensory input at the peripheral stages in the afferent auditory pathways. One system, a reticular feedback system, suppresses irrelevant auditory stimuli through middle-ear muscle contractions. The other system suppresses irrelevant auditory stimuli presumably via the olivocochlear bundle, affecting the auditory nerve responses but not the cochlear microphonics at the hair-cell level in the cochlea. This system may be either an extrareticular feedback system or a presently unknown reticular system capable of functioning with the middle-ear muscles severed. REFERENCES 1. BAUST, W.. C. BERLUCCHI, and G. MOR~ZZI. 1964. Changes in the auditory input in wakefulness and during the synchronized and desynchronized stages of sleep. Arch. Ital. Biol. 102: 657-674. 2. BERLUCCHI, G., J. B. MUNSON, and G. RIZZOLATTI. 1967. Changes in clickevoked responses in the auditory system and the cerebellum of free-moving cats during sleep and waking. Arclt. Ifal. Biol. 105: 118-135. 3. B~No, W., R. VELLUTI, P. HANDLER, and E. GARCIA-AUSST. 1966. Neural control of the cochlear input in the wakeful free guinea pig. Physiol. and Behav. 1: 23-35. 4. BUTLER, D. H., A. S. KAMLET, and R. A. MONTY. 1969. A multipurpose analysis of variance FORTRAN IV computer program. Psychon. Monograph S21pp. 2 : 301-319. 5. CARMEL, P. W., and A. STARR. 1963. Acoustic and non-acoustic factors modifying middle-ear muscle activity in waking cats. J. Nezlrophysiol. 26: 598-616. 6. DESMEDT, J. E. 1962. Auditory-evoked potentials from cochlea to cortex as influenced by activation of the efferent olivo-cochlear bundle. J. ACOUS~. Sot. Am. 34: 1478-1496. 7. DUNLOP, C. W., W. R. WEBSTER, and L. A. SIMONS. 1965. Effect of attention on evoked responses in the classical auditory pathway. Nature 206: 1048-1050. 8. FEX, J. 1959. Augmentation of cochlear microphonics by stimulation of efferent fibers to the cochlea. Arfa Ofolaryng. 50: 540-541. 9. FEX, J. 1962. Auditory activity in centrifugal and centripetal cochlear fibers in cat. Acfa Physiol. Stand., 55: .Sufipl. 189, l-68. 10. GALAMBOS, R. 1956. Suppression of the auditory nerve activity by stimulation of efferent fibers to cochlea. .I. Nezrrophysiol. 19: 424-437. 11. GUZMAN-FLORES, C., and M. ALCARAZ. 1963. Funcion de la cintilla olivo coclear en el fenomeno de distraction a estimulos acusticos. Nota preliminar. Bol. Inst. Esfzld. Med. Biol. 21: 87-92. 12. HERNANDEZ-PEON, R. 1966. Physiological mechanisms in attention, pp. 121-144. In “Frontiers in Physiological Psychology.” R. W, Russell [Ed.]. Academic Press, New York, New York.
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13. HERNANDEZ-PEON, R., H. SCHERRER, and M. JOUVET. 1956. Modification of electrical activity in cochlear nucleus during “attention” in unanesthetized cats. Science 123 : 331-332. 14. HUGELIN, A., S. DUMONT, and N. PAILLAS. 1960. Tympanic muscles and control of auditory input during arousal. Science 131: 1371-1372. 15. IGARASHI, M., B. R. ALFORD, W. P. GORDON, and Y. NAKAI. 1974. Behavioral auditory function after transection of crossed olivocochlear bundle in the cat. Acta Otolaryftg. 77 : 311-317. 16. JOUVET, M., and R. HERNANDEZ-PEON. 1957. Mechanismes neurophysiologiques concernant I’habituation, l’attention, et le conditionment. Electroenceph. Clin. Newophysiol. 6 : 39-49. 17. MOUSHEGIAN, G., A. RUPERT, J. T. MARSH, and R. GALAMBOS. 1961. Evoked cortical potentials in absence of middle-ear muscles. Science 133: 582-583. 18. OATMAN, L. C. 1%8. The effect of attention on auditory evoked
