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Role of visual attention on auditory evoked potentials in unanesthetized cats
EXPERIMENTAL
Role
iKEUROLOGY
of
32,
Visual
Potentials
341-356 (1971)
Attention
E~~giwering
Auditory
in Unanesthetized LYNN
Human
on
C.
Evoked Cats
OATMAN~
Laboratories, USA Aberdeen Research and Devr/opme?kt Aberdecrk Prozlkng Ground, Maryla?kd 21005 Rcceivcd
May
Center,
8. 1971
Click-evoked potentials were recorded from unanesthetized cats with electrodes chronically implanted in the auditory cortex, cochlear nucleus, and round window. 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. The mean peak-topeak amplitudes of averaged click-evoked responses from six adult female cats were significantly smaller during attention to the visual discrimination stimuli when compared with the prediscrimination and control periods. This relationship was present at all electrode placements for five experimental animals with middle ear muscles cut as well as one control animal with middle ear muscles intact. The results suggest that during attention, a central inhibitory mechanism, independent of middle ear muscles, modified click-evoked responses possibly via the olivocochlear bundle which terminates on the hair cells in the cochlea. introduction
The effect of attention on afferent sensory information has been shown to produce a variety of behavioral and neurophysiological results (5, 11, 12, 14, 22). Wh en an organism is engaged in attentive behavior, a selective process occurs within the central nervous system where relevant sensory stimuli are perceived while irrelevant stimuli are rejected (11). Some stimuli are suppressed at very early stages in the afferent auditory pathways (12, 14) and sensory information is transmitted to the auditory cortex only after having been subjected to a “filtering” at a peripheral level. Worden (22) discussed two neurophysiological systems which could be responsible for filtering auditory information at the peripheral level. One system, a reticular feedback system, involves the regulation of auditory 1 This work is a portion of that submitted in partial fulfillment of requirements for the degree of Doctor of Philosophy at the University of Delaware, Newark, Delaware. In conducting the research described herein, the investigator adhered to the Guide for Laboratory Animal Facilities for Laboratory Animal Resources, National Academy of Sciences, National Research Council, Washington, D.C. 341
342
OATMAN
stimuli through middle ear muscle contractions. The other system, an extrareticular feedback system, involves the regulation of auditory stimuli through the action of the olivocochlear bundle (OCB). 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 (16, 17)) and represents the terminal neural path that originates at the cortex, descends parallel to the classical ascending auditory fibers, and makes synaptic connections in all of the auditory nuclei. Electrical stimulation of the OCB in the region of the fourth ventricle results in suppression of the auditory nerve action potential as recorded from the round window (4, 6-S). This evidence has led to the belief that the OCB performs an inhibitory function which controls auditory stimuli to the central nervous system at the peripheral level. The purpose of the present study was to investigate whether the OCB performs an inhibitory function in the unanesthetized unrestrained animal during attentive behavior. The study was designed to determine if clickevoked potentials along the auditory pathway are suppressed in amplitude while an animal, whose middle ear muscles have been severed, is attending to visual stimulation. Although auditory stimuli can be affected by middle ear muscle activity, as a result of bodily movement (20) and reticular influences (13), it was thought that the extrareticular descending system terminating in the OCB would suppress click-evoked potentials at the peripheral levels in the unanesthetized animal during attention to visual stimulation. This would be consistent with the results of Starr (20) and of clickMoushegian et al., ( 15) who observed a decrease in amplitude evoked responses at the cortex that could not be accounted for by middle ear muscle activity. Methods
Sur$cal Procedure. Six female cats weighing approximately 2.5 kg had electrodes placed on the round window (RW) and bilaterally in the cochlear anesnucleus (CN) and auditory cortex (AC) under sodium pentobarbital thesia. The deep electrodes were stereotaxically implanted through small holes bored in the skull according to coordinates in the stereotaxic atlas of Snider and Niemer (19). The deep electrodes were concentric and were made of O.OlO-inch Formvar-coated stainless-steel wire inserted into 25gauge 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 cortical electrodes were flattened monopolar silver-ball electrodes placed on the dura over the auditory cortex. The round-window electrode was a O.OlO-inch stainless-steel wire with a ball tip in polyethylene tubing. The indifferent electrode was a stainless-steel
AUDITORY
POTENTIAL
313
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. each 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. After the electrode was placed on the round window and anchored to the wall of the bulla, it was led under the skin to the top of the head, where all of the electrodes were terminated in a 19-pin 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 in five of the experimental animals and were left intact in the sixth. About a month after recovery from the brain and round-window implant, another operation was performed on the opposite ear, and the stapes was removed in each cat to render them monaural. 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 ferrocynnide for 24 hr. All placements were verified histologically using unstained, frozen sections (18). Figure 1 shows the histological results for all sis cats which confirmed the electrode placements in the cochlear nucleus and Fig. 2 shows the electrode placements on the auditory cortex. 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. Vis& a& dcousfic Sfhdafion. The tests were made in a sound-attenuating 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 (Fig. 3). The cats’ task was to learn the visual discrimination for food reinforcement. The cats were gradually deprived of food until they were on a 22..hr 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. The visual stimuli consisted of concentric rings presented successively for discrimination. The large outer ring was vs inch wide and had a diameter of 1 inch, and the small imler ring was xy inch with a diameter of VJ inch. Luminance measurements were made on the stimulus figures with a Pritchard spectrophotometer (model 1970-PR). The luminance was 7.17
344
OATMAN
FIG. 1. Sketch of a frontal histological section through showing the locations of the cochlear nucleus electrodes. cats used in the present experiment.
the The
brain stem of the cat numbers refer to the
ft-L for the outer ring and 8.47 ft-L for the inner ring. Figure 4 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. In order to increase the cats’ attentiveness and avoid temporal conditioning, the temporal interval (tI) between the
FIG, 2. Sketch of the left tions of the auditory cortex present experiment.
and right hemispheres of the cat brain showing the locaelectrodes. The numbers refer to the cats used in the
AUDITORY
345
POTENTIAL
1-VISUAL
DISPLAY
+20------l L36 FIG.
3. Diagram
I
of the sound-attenuating
onset of the large 1 and 6 sec. The 4 set and the time Auditory clicks
chamber
; see text.
and small concentric rings was varied randomly between exposure duration of the small inner concentric ring was between trials was 25 sec. were presented continuously at a rate of l/set during the
r
OUTER
t,
P
INNER
l-l
\
FIG.
1
4. Schematic
1
1
diagram
1
1
1
1
of the stimulus
1
1
1
presentation
RING
RING
BEHAVIORAL
1
AUDITORY
; see text.
RESPONSE
CLICKS
346
OATMAN
presentation of the successive visual discrimination task, but they were not synchronized with the onset of the visual display. The auditory clicks were generated by a 90-psec square-wave pulse obtained from Tektronix waveform (type 162) and pulse generators (type 163). The filtered pulses were led through a decade attenuator (General Radio, GR-1450), and a Dynakit power amplifier (Mark III, 60 W) to a hypersonic driver (University T50). The clicks were presented through a sound-tube system which terminated at the entrance to the external auditory meatus of the cat, however the tube was not fastened to the pinna. The clicks were presented at a peak intensity of 90 db SPL (re 0.0002 microbar). The click intensity was measured with a calibrated condenser microphone (Bruel and Kjaer type 4135). The sound-pressure measurements were made in the sound-attenuated cubicle, where the condenser microphone 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. The voltage output from the microphone was observed oscilloscopically, and the decade attenuator was used to obtain the necessary sound levels. The highest wave was measured from base line to peak to calculate the sound intensity. The sound pressure was calibrated at 1 dyne/cm2, and other sound pressures for different intensities were inferred from that intensity, since the output from the speaker was linear through 120 db. Data Collection and Procedure. Simultaneous recordings were obtained from the round window (cochlear microphonics and N,-- N, responses), the cochlear nucleus, and the auditory cortex to click stimuli. Recordings were obtained from the unrestrained animals via a Microdot shielded cable connected to an electroencephalograph (Grass model 7) located outside the sound-attenuating cubicle. At the same time, the click-evoked potentials were recorded on a lCchanne1 FM tape recorder (Sangamo 4iOO). From the FM tape recorder the click-evoked potentials were fed into a Bio-Data variance computer (model 204), averaged with a computer of average transients (Technical Measurement Corporation, CAT 1000) and displayed on a Tektronix storage oscilloscope (type 564) or plotted on an X-Y plotter (Mosley model 7000 AM ) . 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 four different attentive states : (a) a pre-test control in which the cat was awake, relaxed, and not attentive to any identifiable stimuli; (b) a p re d’rscrimination period during the test which was just prior to the onset of the visual discrimination when the cat was mildly attentive, anticipating the onset of the visual discrimination ;
AUDITORY
POTENTIAL
347
(c) during the presentation of the visual discrimination stimuli which was between the concentric rings when the cat was attentive since appropriate behavioral responses were obtained to the visual stimuli ; and (d) a posttest control period similar to the pretest control period. The evoked responses to 50 clicks were averaged on the computer of average transients for each of the four different attentive states, i.e., while the cat was relaxed, while the cat was anticipating the onset of the visual discrimination, while the cat was attending to the visual discrimination, and while the cat was relaxed again. The 50 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 (Fig. 4). Results
The data consist of plots of the averages of 50 click-evoked potentials from the three electrode locations: round window (LRW) ; cochlear nucleus (LCN) : and auditory cortex (LAC). The peak-to-peak (first largest positive to first largest negative) amplitude of these averaged evoked responses was measured by ruler to the nearest millimeter and then converted into microvolts. Evoked potentials influenced by bodily movement were discarded from the data as were those responses obtained on discrimination trials in which the cat failed to respond and received no food reinforcement. No attempt was made to analyze the different components of the evoked response. Figure 5 shows an example of representative averaged auditory evoked potentials for cat No. 28 for each of the four attentive states: pre-test control (cat nonattentive, relaxed but awake) : prediscrimination (cat alert, somewhat attentive) ; during discrimination (cat very attentive) ; and posttest control (cat nonattentive, relaxed but awake). The figure shows that the mean peak-to-peak amplitude of click-evoked potentials recorded from the auditory pathway were of a smaller amplitude when the cats were very attentive than when they were nonattentive. This reduction in amplitude occurred at all three electrode locations. All six cats showed that with a mild degree of attention (prediscrimination) the amplitudes of the clickevoked potentials at the cochlear nucleus and the auditory cortex were reduced when compared to the control periods. However, when the attention of the animals was focused upon the visual discrimination, the amplitudes of these evoked potentials were further reduced. The top wave forms in Fig. S show the cochlear microphonic (CM) and N,-NZ responses to a single click. Likewise, when the animal was very attentive (during discrimination), the amplitudes of the N,- N,, responses of the auditory nerre (LRW) were reduced when compared with the control periods.
348
OATMAN
OJ
, CLICK
I CLICK
I CLICK
CLlCI
I
FIG. 5. Averaged evoked potentials recorded from the left round window the left cochlear nucleus (LCN), and the left auditory cortex (LAC) for attentive states. Top waveforms from LRW show cochlear microphonics and responses to a single click. Calibration: 50 gv per 1.5 division and 500 ysec sion. Cat PC-28 with middle ear muscles cut.
(LRW), different N,-N, per divi-
AUDITORY
POTENTIAL
349
Although the N, -N, responses were reduced in amplitude when the cats were very attentive (during discrimination), little or no change occurred in the amplitude of the CM. It was necessary to increase the number of responses to 100 in order to obtain the maximum resolution of the N, -N? responses from the computer of average transients. Therefore, the missing data of the prediscrimination condition at the round window (LRW) resulted from an insufficient number of evoked responses during that condition. The variance of the 50 averaged responses is presented below the mean for the cochlear nucleus and auditory cortex in Fig. 5. The variance for the round-window response was discarded since the computer could not be properly calibrated in the variance mode. The figure shows that the evoked potentials become more variable with increased attention at the auditory cortex. The highest variance occurred when the cats were most attentive, whereas the lowest variance occurred during the control periods when the cats were nonattentive. Differences in variance also occurred between the cochlear nucleus and the auditory cortex. For all of the attentive states, the variance in the cochlear nucleus was much lower than the variance in the auditory cortex. All of the data are summarized in Figs. 6-9. The figures show the mean peak-to-peak amplitude in microvolts as a function of increased attention for the five cats with middle ear muscles cut and the cat with muscles intact. The columns in the graphs represent different attentive states ; the pretest and posttest were control periods, with the cat relased, awake, and nonattentive. The experimental period consisted of two parts: (a) prediscrimination (cat mildly attentive, prior to the visual discrimination) : (b) during discrimination (cat very attentive, onset of outer and inner rings). The number (N) below each column refers to the number of averages upon which the condition means were based. The limits around each mean for the cochlear nucleus and the auditory tortes represent 95% confidence levels. No confidence levels are included for the round-window means since the variance could not be obtained from the computer. At the auditory cortex (Fig. 6) the mean peak-to-peak amplitudes decreased as a function of increased attention for cats with middle ear muscles cut as well as for the cat with its middle ear muscles intact. In the cats with middle ear muscles cut, comparing the prediscrimination period with the period during discrimination, the figure shows that the mean amplitude was reduced 300/o, which was significant at the 0.02 level (tz2.34, df=4065). The mean amplitude reduced in the cat with the middle ear muscles intact was not different from the cats with their muscles cut. The percentage of amplitude reduction between the prediscrimination period and
350
OATMAN
50
Yl-
-+ T 2 z P
40
30
f 4 ; : : :
20
10
0
AUDITORY
CORTEX
FIG. 6. The mean peak-to-peak amplitude of auditory cortex evoked potentials in microvolts as a function of increased attention for cats with middle ear muscles cut (left) and intact (right). The numbers (N) refer to the number of data plots where each plot was a mean based on 50 evoked potentials. The limits around each mean represent 95% confidence levels. that during discrimination was 29% which was significant at the 0.01 level (t=2.64, df=684). At the cochlear nucleus (Fig. 7) in cats with the middle ear muscles cut, the mean amplitude of the prediscrimination period as compared with the period during discrimination was reduced 26% which was significant at the 0.01 level (t = 21.01, df = 3232). Although there was an overall reduction in amplitude between the cats with the middle ear muscles cut and the cat with the middle ear muscles intact, the amplitude reduction reflects a poor electrode placement in cat PC-29 rather than any action on the part of the middle ear muscles. Cat PC-29 had the least sensitivity of the six cats. The percentage of amplitude reduction for the cat with the middle ear muscles intact was 20% between the periods before discrimination and during discrimination, which was significant at the 0.01 level (t = 7.87, df = 930). At the round window (Fig. 8) in cats with middle ear muscles cut, the mean amplitude of the N, response in the period during discrimination was reduced 46% when compared with the pretest period. Since the variance was not available for this electrode placement, a t test was not applied to the two mean amplitudes. However, it may be assumed that a distribution of evoked responses around the means would be similar to the distribution observed in the cochlear nucleus and that the two means would be significantly different in amplitude. The percentage of amplitude reduc-
AUDITORY
POTENTIAL
351
300
200
100
0
FIG. 7. The mean peak-to-peak amplitude of cochlear nucleus evoked potentials in microvolts as a function of increased attention for cats with middle ear muscles cut (left) and intact (right). The numbers (N) refer to the number of data plots where each plot was a mean based on 50 evoked potentials. The limits around each mean represent 95% confidence levels.
of the N, response was 40% between the pretest period and the period during discrimination, and this reduction is similar to that of cats with middle ear muscles severed. Figure 9 shows the cochlear microphonic response recorded at the round window for cats with middle ear muscles cut, as well as for the cat with middle ear muscles intact. The graph shows the mean peak-to-peak amplitude of the cochlear microphonic in microvolts as a function of increased attention. No significant differences were found between the pretest or posttest periods and the period during discrimination for the cats with middle ear muscles cut and intact. tion
Discussion
The results indicate that the attentive state of the animal significantly affects the amplitude of click-evoked responses recorded all along the auditory pathway. The present evidence suggests that the response modifications are due to a central inhibitory mechanism which influences N, -iv, responses at the hair-cell level in the cochlea but does not influence the cochlear microphonic. These data are consistent with the findings of Starr (20) and Moushegian et al. (15) who observed a decrease in amplitude
352
OATMAN
ROUND
FIG. 8. The attention for numbers (N) on 100 evoked
WINDOW
mean peak-to-peak amplitude of N, in microvolts as a function of cats with middle ear muscles cut (left) and intact (right). The refer to the number of data plots, where each plot was a mean based responses.
of click-evoked responses at the cortex with middle ear muscles cut. The data are also consistent with the electrophysiological evidence of Galambos (8) and Desmedt (4) who have shown that electrical stimulation of the crossed OCB suppressed the N1-iV2 responses to clicks. The control procedures used in the present study were designed to insure a constant stimulus input to the auditory system (22), to eliminate the effects of the middle ear muscles (3, 13, 20), and to obtain visual attention in the cats. A constant stimulus input to the auditory system was 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. 5 reveals little change in the amplitude of the CM between the different attentive states. Since CM 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. Both the tensor tympani and stapedius muscles were severed in the present experiment, however, the results show no differences between cats with middle ear muscles cut and the cat with middle ear muscles intact. It was concluded that the middle ear muscles are not a factor in the inhibition
Al~DJTORY
353
I’OTENTIAL
40-
30-
lo-
0
PRE-
TEST N-74
I
I1
DURING
POST
PRE-
DURING
POST
DISCRIM
TEST
TEST
DISCRIM
TEST
N=lS
N=20
N=l7
N=76
N=80
COCHLEAR
MICROPHONIC
FIG. 9. The mean peak-to-peak amplitude of cochlear microphonics in microvolts as a function of increased attention for cats with middle ear muscles cut (left) and intact (right). The number (N) refers to the number of measureable individual responses evoked by a single click.
shown in this experiment. This conclusion can he supported by noting frequency and amplitude of the CM in Fig. 5. The frequency of the to the 90-psec click is approximately 16,000 Hz. Middle-ear muscle tractions in cat PC-29 would not severely attenuate the amplitude of a high frequency (16,000 Hz) stimulus, since Galambos and Rupert
the
CM consuch
(9) have shown in the cat that the ear muscles attenuate transmission tones
primarily
between
500 and 3000 Hz. In addition,
if the middle
ear muscles
contract and attenuate sound transmission, an attenuation would appear in the amplitude of the CM. Since little change in the amplitude of the CM can be observed in cat PC-29 (Fig. 9) as a function of increased attentiveness, it is not likely that middle-ear muscle contractions are a factor in this experiment. 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 (8, 12)) the experimenter distracting the cat in one way or another (15), or the use of novel light flashes (21). The attention span may be very short, and perhaps the problem with previous attention getting techniques. may he that they were too long for the animal’s attention span. To obtain better control over attentive behavior, a successivevisual 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.
354
OATMAN
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 (N,) and the cochlear nucleus remain unchanged durin g sleep and waking cycles. It is therefore unlikely that the results of the present experiment can be interpreted as reflecting shifts in general level of arousal as seen in sleep and waking states. It might also be argued that any changes in amplitude of the clickevoked responses which occur in the present study during the experimental period could be the result of conditioning procedures per se rather than any interaction of the visual system upon the auditory system. For example, the requirement of making the conditioned response and the central concomitants of such responses might themselves be distracting. The present experiment tried to avoid this possibility by making all measures before the movements of the conditioned response began. This possibility also seems unlikely in light of the studies done on the rat by Hall and Mark (10) on acoustically evoked potentials in the auditory cortex during conditioning. These authors concluded that establishing a discriminative stimulus with positive reinforcement procedures does not change the amplitude of evoked potentials recorded from the primary auditory cortex. Since no differences were observed at the cortex, it would seem unlikely that changes would occur at lower stations in the auditory pathways and not be reflected in the cortical responses. I conclude that 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 selective process in which the evoked potentials of irrelevant sensory stimuli are inhibited. This selection process involves at least two inhibitory systems which participate in modifying sensory input at very early 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 OCB, effecting the N,-N, responses but not the CM 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 W., G. BERLUCCHI, in wakefulness and during
1.
BAUST,
2.
BERLUCCHI,
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102 :
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G., J. B. MUNSON,
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responses in the auditory sleep and waking. Arch.
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STARR,
Role
iKEUROLOGY
of
32,
Visual
Potentials
341-356 (1971)
Attention
E~~giwering
Auditory
in Unanesthetized LYNN
Human
on
C.
Evoked Cats
OATMAN~
Laboratories, USA Aberdeen Research and Devr/opme?kt Aberdecrk Prozlkng Ground, Maryla?kd 21005 Rcceivcd
May
Center,
8. 1971
Click-evoked potentials were recorded from unanesthetized cats with electrodes chronically implanted in the auditory cortex, cochlear nucleus, and round window. 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. The mean peak-topeak amplitudes of averaged click-evoked responses from six adult female cats were significantly smaller during attention to the visual discrimination stimuli when compared with the prediscrimination and control periods. This relationship was present at all electrode placements for five experimental animals with middle ear muscles cut as well as one control animal with middle ear muscles intact. The results suggest that during attention, a central inhibitory mechanism, independent of middle ear muscles, modified click-evoked responses possibly via the olivocochlear bundle which terminates on the hair cells in the cochlea. introduction
The effect of attention on afferent sensory information has been shown to produce a variety of behavioral and neurophysiological results (5, 11, 12, 14, 22). Wh en an organism is engaged in attentive behavior, a selective process occurs within the central nervous system where relevant sensory stimuli are perceived while irrelevant stimuli are rejected (11). Some stimuli are suppressed at very early stages in the afferent auditory pathways (12, 14) and sensory information is transmitted to the auditory cortex only after having been subjected to a “filtering” at a peripheral level. Worden (22) discussed two neurophysiological systems which could be responsible for filtering auditory information at the peripheral level. One system, a reticular feedback system, involves the regulation of auditory 1 This work is a portion of that submitted in partial fulfillment of requirements for the degree of Doctor of Philosophy at the University of Delaware, Newark, Delaware. In conducting the research described herein, the investigator adhered to the Guide for Laboratory Animal Facilities for Laboratory Animal Resources, National Academy of Sciences, National Research Council, Washington, D.C. 341
342
OATMAN
stimuli through middle ear muscle contractions. The other system, an extrareticular feedback system, involves the regulation of auditory stimuli through the action of the olivocochlear bundle (OCB). 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 (16, 17)) and represents the terminal neural path that originates at the cortex, descends parallel to the classical ascending auditory fibers, and makes synaptic connections in all of the auditory nuclei. Electrical stimulation of the OCB in the region of the fourth ventricle results in suppression of the auditory nerve action potential as recorded from the round window (4, 6-S). This evidence has led to the belief that the OCB performs an inhibitory function which controls auditory stimuli to the central nervous system at the peripheral level. The purpose of the present study was to investigate whether the OCB performs an inhibitory function in the unanesthetized unrestrained animal during attentive behavior. The study was designed to determine if clickevoked potentials along the auditory pathway are suppressed in amplitude while an animal, whose middle ear muscles have been severed, is attending to visual stimulation. Although auditory stimuli can be affected by middle ear muscle activity, as a result of bodily movement (20) and reticular influences (13), it was thought that the extrareticular descending system terminating in the OCB would suppress click-evoked potentials at the peripheral levels in the unanesthetized animal during attention to visual stimulation. This would be consistent with the results of Starr (20) and of clickMoushegian et al., ( 15) who observed a decrease in amplitude evoked responses at the cortex that could not be accounted for by middle ear muscle activity. Methods
Sur$cal Procedure. Six female cats weighing approximately 2.5 kg had electrodes placed on the round window (RW) and bilaterally in the cochlear anesnucleus (CN) and auditory cortex (AC) under sodium pentobarbital thesia. The deep electrodes were stereotaxically implanted through small holes bored in the skull according to coordinates in the stereotaxic atlas of Snider and Niemer (19). The deep electrodes were concentric and were made of O.OlO-inch Formvar-coated stainless-steel wire inserted into 25gauge 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 cortical electrodes were flattened monopolar silver-ball electrodes placed on the dura over the auditory cortex. The round-window electrode was a O.OlO-inch stainless-steel wire with a ball tip in polyethylene tubing. The indifferent electrode was a stainless-steel
AUDITORY
POTENTIAL
313
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. each 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. After the electrode was placed on the round window and anchored to the wall of the bulla, it was led under the skin to the top of the head, where all of the electrodes were terminated in a 19-pin 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 in five of the experimental animals and were left intact in the sixth. About a month after recovery from the brain and round-window implant, another operation was performed on the opposite ear, and the stapes was removed in each cat to render them monaural. 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 ferrocynnide for 24 hr. All placements were verified histologically using unstained, frozen sections (18). Figure 1 shows the histological results for all sis cats which confirmed the electrode placements in the cochlear nucleus and Fig. 2 shows the electrode placements on the auditory cortex. 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. Vis& a& dcousfic Sfhdafion. The tests were made in a sound-attenuating 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 (Fig. 3). The cats’ task was to learn the visual discrimination for food reinforcement. The cats were gradually deprived of food until they were on a 22..hr 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. The visual stimuli consisted of concentric rings presented successively for discrimination. The large outer ring was vs inch wide and had a diameter of 1 inch, and the small imler ring was xy inch with a diameter of VJ inch. Luminance measurements were made on the stimulus figures with a Pritchard spectrophotometer (model 1970-PR). The luminance was 7.17
344
OATMAN
FIG. 1. Sketch of a frontal histological section through showing the locations of the cochlear nucleus electrodes. cats used in the present experiment.
the The
brain stem of the cat numbers refer to the
ft-L for the outer ring and 8.47 ft-L for the inner ring. Figure 4 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. In order to increase the cats’ attentiveness and avoid temporal conditioning, the temporal interval (tI) between the
FIG, 2. Sketch of the left tions of the auditory cortex present experiment.
and right hemispheres of the cat brain showing the locaelectrodes. The numbers refer to the cats used in the
AUDITORY
345
POTENTIAL
1-VISUAL
DISPLAY
+20------l L36 FIG.
3. Diagram
I
of the sound-attenuating
onset of the large 1 and 6 sec. The 4 set and the time Auditory clicks
chamber
; see text.
and small concentric rings was varied randomly between exposure duration of the small inner concentric ring was between trials was 25 sec. were presented continuously at a rate of l/set during the
r
OUTER
t,
P
INNER
l-l
\
FIG.
1
4. Schematic
1
1
diagram
1
1
1
1
of the stimulus
1
1
1
presentation
RING
RING
BEHAVIORAL
1
AUDITORY
; see text.
RESPONSE
CLICKS
346
OATMAN
presentation of the successive visual discrimination task, but they were not synchronized with the onset of the visual display. The auditory clicks were generated by a 90-psec square-wave pulse obtained from Tektronix waveform (type 162) and pulse generators (type 163). The filtered pulses were led through a decade attenuator (General Radio, GR-1450), and a Dynakit power amplifier (Mark III, 60 W) to a hypersonic driver (University T50). The clicks were presented through a sound-tube system which terminated at the entrance to the external auditory meatus of the cat, however the tube was not fastened to the pinna. The clicks were presented at a peak intensity of 90 db SPL (re 0.0002 microbar). The click intensity was measured with a calibrated condenser microphone (Bruel and Kjaer type 4135). The sound-pressure measurements were made in the sound-attenuated cubicle, where the condenser microphone 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. The voltage output from the microphone was observed oscilloscopically, and the decade attenuator was used to obtain the necessary sound levels. The highest wave was measured from base line to peak to calculate the sound intensity. The sound pressure was calibrated at 1 dyne/cm2, and other sound pressures for different intensities were inferred from that intensity, since the output from the speaker was linear through 120 db. Data Collection and Procedure. Simultaneous recordings were obtained from the round window (cochlear microphonics and N,-- N, responses), the cochlear nucleus, and the auditory cortex to click stimuli. Recordings were obtained from the unrestrained animals via a Microdot shielded cable connected to an electroencephalograph (Grass model 7) located outside the sound-attenuating cubicle. At the same time, the click-evoked potentials were recorded on a lCchanne1 FM tape recorder (Sangamo 4iOO). From the FM tape recorder the click-evoked potentials were fed into a Bio-Data variance computer (model 204), averaged with a computer of average transients (Technical Measurement Corporation, CAT 1000) and displayed on a Tektronix storage oscilloscope (type 564) or plotted on an X-Y plotter (Mosley model 7000 AM ) . 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 four different attentive states : (a) a pre-test control in which the cat was awake, relaxed, and not attentive to any identifiable stimuli; (b) a p re d’rscrimination period during the test which was just prior to the onset of the visual discrimination when the cat was mildly attentive, anticipating the onset of the visual discrimination ;
AUDITORY
POTENTIAL
347
(c) during the presentation of the visual discrimination stimuli which was between the concentric rings when the cat was attentive since appropriate behavioral responses were obtained to the visual stimuli ; and (d) a posttest control period similar to the pretest control period. The evoked responses to 50 clicks were averaged on the computer of average transients for each of the four different attentive states, i.e., while the cat was relaxed, while the cat was anticipating the onset of the visual discrimination, while the cat was attending to the visual discrimination, and while the cat was relaxed again. The 50 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 (Fig. 4). Results
The data consist of plots of the averages of 50 click-evoked potentials from the three electrode locations: round window (LRW) ; cochlear nucleus (LCN) : and auditory cortex (LAC). The peak-to-peak (first largest positive to first largest negative) amplitude of these averaged evoked responses was measured by ruler to the nearest millimeter and then converted into microvolts. Evoked potentials influenced by bodily movement were discarded from the data as were those responses obtained on discrimination trials in which the cat failed to respond and received no food reinforcement. No attempt was made to analyze the different components of the evoked response. Figure 5 shows an example of representative averaged auditory evoked potentials for cat No. 28 for each of the four attentive states: pre-test control (cat nonattentive, relaxed but awake) : prediscrimination (cat alert, somewhat attentive) ; during discrimination (cat very attentive) ; and posttest control (cat nonattentive, relaxed but awake). The figure shows that the mean peak-to-peak amplitude of click-evoked potentials recorded from the auditory pathway were of a smaller amplitude when the cats were very attentive than when they were nonattentive. This reduction in amplitude occurred at all three electrode locations. All six cats showed that with a mild degree of attention (prediscrimination) the amplitudes of the clickevoked potentials at the cochlear nucleus and the auditory cortex were reduced when compared to the control periods. However, when the attention of the animals was focused upon the visual discrimination, the amplitudes of these evoked potentials were further reduced. The top wave forms in Fig. S show the cochlear microphonic (CM) and N,-NZ responses to a single click. Likewise, when the animal was very attentive (during discrimination), the amplitudes of the N,- N,, responses of the auditory nerre (LRW) were reduced when compared with the control periods.
348
OATMAN
OJ
, CLICK
I CLICK
I CLICK
CLlCI
I
FIG. 5. Averaged evoked potentials recorded from the left round window the left cochlear nucleus (LCN), and the left auditory cortex (LAC) for attentive states. Top waveforms from LRW show cochlear microphonics and responses to a single click. Calibration: 50 gv per 1.5 division and 500 ysec sion. Cat PC-28 with middle ear muscles cut.
(LRW), different N,-N, per divi-
AUDITORY
POTENTIAL
349
Although the N, -N, responses were reduced in amplitude when the cats were very attentive (during discrimination), little or no change occurred in the amplitude of the CM. It was necessary to increase the number of responses to 100 in order to obtain the maximum resolution of the N, -N? responses from the computer of average transients. Therefore, the missing data of the prediscrimination condition at the round window (LRW) resulted from an insufficient number of evoked responses during that condition. The variance of the 50 averaged responses is presented below the mean for the cochlear nucleus and auditory cortex in Fig. 5. The variance for the round-window response was discarded since the computer could not be properly calibrated in the variance mode. The figure shows that the evoked potentials become more variable with increased attention at the auditory cortex. The highest variance occurred when the cats were most attentive, whereas the lowest variance occurred during the control periods when the cats were nonattentive. Differences in variance also occurred between the cochlear nucleus and the auditory cortex. For all of the attentive states, the variance in the cochlear nucleus was much lower than the variance in the auditory cortex. All of the data are summarized in Figs. 6-9. The figures show the mean peak-to-peak amplitude in microvolts as a function of increased attention for the five cats with middle ear muscles cut and the cat with muscles intact. The columns in the graphs represent different attentive states ; the pretest and posttest were control periods, with the cat relased, awake, and nonattentive. The experimental period consisted of two parts: (a) prediscrimination (cat mildly attentive, prior to the visual discrimination) : (b) during discrimination (cat very attentive, onset of outer and inner rings). The number (N) below each column refers to the number of averages upon which the condition means were based. The limits around each mean for the cochlear nucleus and the auditory tortes represent 95% confidence levels. No confidence levels are included for the round-window means since the variance could not be obtained from the computer. At the auditory cortex (Fig. 6) the mean peak-to-peak amplitudes decreased as a function of increased attention for cats with middle ear muscles cut as well as for the cat with its middle ear muscles intact. In the cats with middle ear muscles cut, comparing the prediscrimination period with the period during discrimination, the figure shows that the mean amplitude was reduced 300/o, which was significant at the 0.02 level (tz2.34, df=4065). The mean amplitude reduced in the cat with the middle ear muscles intact was not different from the cats with their muscles cut. The percentage of amplitude reduction between the prediscrimination period and
350
OATMAN
50
Yl-
-+ T 2 z P
40
30
f 4 ; : : :
20
10
0
AUDITORY
CORTEX
FIG. 6. The mean peak-to-peak amplitude of auditory cortex evoked potentials in microvolts as a function of increased attention for cats with middle ear muscles cut (left) and intact (right). The numbers (N) refer to the number of data plots where each plot was a mean based on 50 evoked potentials. The limits around each mean represent 95% confidence levels. that during discrimination was 29% which was significant at the 0.01 level (t=2.64, df=684). At the cochlear nucleus (Fig. 7) in cats with the middle ear muscles cut, the mean amplitude of the prediscrimination period as compared with the period during discrimination was reduced 26% which was significant at the 0.01 level (t = 21.01, df = 3232). Although there was an overall reduction in amplitude between the cats with the middle ear muscles cut and the cat with the middle ear muscles intact, the amplitude reduction reflects a poor electrode placement in cat PC-29 rather than any action on the part of the middle ear muscles. Cat PC-29 had the least sensitivity of the six cats. The percentage of amplitude reduction for the cat with the middle ear muscles intact was 20% between the periods before discrimination and during discrimination, which was significant at the 0.01 level (t = 7.87, df = 930). At the round window (Fig. 8) in cats with middle ear muscles cut, the mean amplitude of the N, response in the period during discrimination was reduced 46% when compared with the pretest period. Since the variance was not available for this electrode placement, a t test was not applied to the two mean amplitudes. However, it may be assumed that a distribution of evoked responses around the means would be similar to the distribution observed in the cochlear nucleus and that the two means would be significantly different in amplitude. The percentage of amplitude reduc-
AUDITORY
POTENTIAL
351
300
200
100
0
FIG. 7. The mean peak-to-peak amplitude of cochlear nucleus evoked potentials in microvolts as a function of increased attention for cats with middle ear muscles cut (left) and intact (right). The numbers (N) refer to the number of data plots where each plot was a mean based on 50 evoked potentials. The limits around each mean represent 95% confidence levels.
of the N, response was 40% between the pretest period and the period during discrimination, and this reduction is similar to that of cats with middle ear muscles severed. Figure 9 shows the cochlear microphonic response recorded at the round window for cats with middle ear muscles cut, as well as for the cat with middle ear muscles intact. The graph shows the mean peak-to-peak amplitude of the cochlear microphonic in microvolts as a function of increased attention. No significant differences were found between the pretest or posttest periods and the period during discrimination for the cats with middle ear muscles cut and intact. tion
Discussion
The results indicate that the attentive state of the animal significantly affects the amplitude of click-evoked responses recorded all along the auditory pathway. The present evidence suggests that the response modifications are due to a central inhibitory mechanism which influences N, -iv, responses at the hair-cell level in the cochlea but does not influence the cochlear microphonic. These data are consistent with the findings of Starr (20) and Moushegian et al. (15) who observed a decrease in amplitude
352
OATMAN
ROUND
FIG. 8. The attention for numbers (N) on 100 evoked
WINDOW
mean peak-to-peak amplitude of N, in microvolts as a function of cats with middle ear muscles cut (left) and intact (right). The refer to the number of data plots, where each plot was a mean based responses.
of click-evoked responses at the cortex with middle ear muscles cut. The data are also consistent with the electrophysiological evidence of Galambos (8) and Desmedt (4) who have shown that electrical stimulation of the crossed OCB suppressed the N1-iV2 responses to clicks. The control procedures used in the present study were designed to insure a constant stimulus input to the auditory system (22), to eliminate the effects of the middle ear muscles (3, 13, 20), and to obtain visual attention in the cats. A constant stimulus input to the auditory system was 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. 5 reveals little change in the amplitude of the CM between the different attentive states. Since CM 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. Both the tensor tympani and stapedius muscles were severed in the present experiment, however, the results show no differences between cats with middle ear muscles cut and the cat with middle ear muscles intact. It was concluded that the middle ear muscles are not a factor in the inhibition
Al~DJTORY
353
I’OTENTIAL
40-
30-
lo-
0
PRE-
TEST N-74
I
I1
DURING
POST
PRE-
DURING
POST
DISCRIM
TEST
TEST
DISCRIM
TEST
N=lS
N=20
N=l7
N=76
N=80
COCHLEAR
MICROPHONIC
FIG. 9. The mean peak-to-peak amplitude of cochlear microphonics in microvolts as a function of increased attention for cats with middle ear muscles cut (left) and intact (right). The number (N) refers to the number of measureable individual responses evoked by a single click.
shown in this experiment. This conclusion can he supported by noting frequency and amplitude of the CM in Fig. 5. The frequency of the to the 90-psec click is approximately 16,000 Hz. Middle-ear muscle tractions in cat PC-29 would not severely attenuate the amplitude of a high frequency (16,000 Hz) stimulus, since Galambos and Rupert
the
CM consuch
(9) have shown in the cat that the ear muscles attenuate transmission tones
primarily
between
500 and 3000 Hz. In addition,
if the middle
ear muscles
contract and attenuate sound transmission, an attenuation would appear in the amplitude of the CM. Since little change in the amplitude of the CM can be observed in cat PC-29 (Fig. 9) as a function of increased attentiveness, it is not likely that middle-ear muscle contractions are a factor in this experiment. 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 (8, 12)) the experimenter distracting the cat in one way or another (15), or the use of novel light flashes (21). The attention span may be very short, and perhaps the problem with previous attention getting techniques. may he that they were too long for the animal’s attention span. To obtain better control over attentive behavior, a successivevisual 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.
354
OATMAN
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 (N,) and the cochlear nucleus remain unchanged durin g sleep and waking cycles. It is therefore unlikely that the results of the present experiment can be interpreted as reflecting shifts in general level of arousal as seen in sleep and waking states. It might also be argued that any changes in amplitude of the clickevoked responses which occur in the present study during the experimental period could be the result of conditioning procedures per se rather than any interaction of the visual system upon the auditory system. For example, the requirement of making the conditioned response and the central concomitants of such responses might themselves be distracting. The present experiment tried to avoid this possibility by making all measures before the movements of the conditioned response began. This possibility also seems unlikely in light of the studies done on the rat by Hall and Mark (10) on acoustically evoked potentials in the auditory cortex during conditioning. These authors concluded that establishing a discriminative stimulus with positive reinforcement procedures does not change the amplitude of evoked potentials recorded from the primary auditory cortex. Since no differences were observed at the cortex, it would seem unlikely that changes would occur at lower stations in the auditory pathways and not be reflected in the cortical responses. I conclude that 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 selective process in which the evoked potentials of irrelevant sensory stimuli are inhibited. This selection process involves at least two inhibitory systems which participate in modifying sensory input at very early 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 OCB, effecting the N,-N, responses but not the CM 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 W., G. BERLUCCHI, in wakefulness and during
1.
BAUST,
2.
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