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Chopper units recorded in the cochlear nucleus of the awake cat
Neuroscience Letters, 7 (1977) 261--265 © Elsevier/North-Holland Scientific Publishers Ltd.
261
CHOPPER UNITS RECORDED IN THE COCHLEAR NUCLEUS OF THE AWAKE CAT i
W.R. WEBSTER Neuropsychology Laboratory Psychology Department, Monash University, Clayton, Vic. (Australia) (Received January 5th, 1978) (Accepted January 9th, 1978)
SUMMARY
Thirty-six of 120 units recorded in the cochlem' nucleus of awake cal~s had average response histograms which showed a chopper pattern consisting of regular peaks in the initial part of the histogram. Many of the chopper units show,.*d the chopper pattern over most of the excitatory response area with the pattern being strongest at best frequency..~alysis of interval distributions of driven and spontaneous activity indicated that copper units ~ired more regularly than primarylike units. Both the nature of the chopper pattern and the frequency of its occurrence in the awake animal were similar to that observed in animals under barbiturate anaestheti~.
Most extracellular studies of neurones in the cochlear nucleus have been carried out in animals anaesthetized with barbiturate anaesthetic [2--9,11]. When short tone bursts at best frequency are used as stimuli, the most common response pattern in anaesthetized animals is one of sustained firing throughout the stimulus duration. Units showing sustained firing have been clearly divided into 2 major classes on the basis of average response (AR) histogr~ams. One class, called primarylike unii; s, have response characteristics which are very similar to those of auditory nerve fibres. Their AR histograms have an initial peak followed by a monotor~ic decay to a rate of sustained firing which continues while the tone is presented. The other class, ¢~alled chopper units, also have an AR histogram which shows a monotonic decay to a steady level of firing, but the initial part of the AR histogram l~as a series of well defined peaks. The chopper pattern becomes clear at 10--20 dB above threshold: at higher intensities the spacing between peaks decreases and the amplitude and number of peaks increases [ 5,6,9]. Primarylike urdts are recorded mainly in the ventral cochlear nucleus whereal~ chopper units are found in all divisions of the cochlear nucleus [ 9]. Recording in the dorsal cochlear nucleus of the u'nanaesthetized decerebrated
262
cat, Young and Brownell [12] reported that the chopper pattern was very infrequently observed. They suggested that the presence of anaesthetic might potentiate the chopper pattern. This suggestion is intriguing since Young and Bl~wnell also found that inhibition was more often observed in their preparation and when they injected barbiturate anaesthetic these, inhibitory responses were abolished. Single units were recorded from all divisions of the cochlear nucleus in 10 awake cats using techniques already described [1 ]. A metal chamber was positioned over a defect in the skull above the cochlear nucleus, which was ~sualized ~ t e r a small section of the cerebellum has been aspirated. After the animal recovered from the operation, a microdrive driven by a small stepping motor was inserted in the chamber. Glass coated tungsten electrodes were advanced into the cochlear nucleus. A NOVA-2/10 computer controlled stimulus presentation and both tuning curves and response areas were obtained under computer control. Thirty-six eut of 120 units recorded in all divisions of the cochlear nucleus, had the chopper pattern. These proportions are similar to those reported in the barbiturate anaesthetized cat [ 5,6]. Godfrey, Kiang and Norris [ 5] recording from the posteroventral cochlear nucleus (PVCN) observed that 50% of the units had a chopper response pattern at best frequency. Similar results were obtained in the present study. Average response histograms of one PVCN trait .are shown in Fig. 1. These histograms which were taken only from the excitatory response area of the unit illustrate some features characteristic of many choppers recorded in the present study. Firstly, t~e chopper response pattern is present over most of the response area. At best frequency (13 kHz), the chopper pattern becomes clear at 20 dB (threshold 5 dB). As intensity increases the number of peaks increases and the duration between peaks decreases. A similar pattern is present at frequencies on either side of the best frequency. If histograms are examined across any one intensity, it is clear that fewer peaks are•seen on either side of best frequency. Secondly, over the whole of the excitatory response area, the number of spikes is a monotonic increasing function of stimulus intensity at any one frequency. (~11wunit also had an inhibitory sideband which extended from 17.0 to 28,0 kHz.) Thirdly, at high iutensities, the firing rate is very high, but even then the chopper pattern is still present. Not all chopper units had such consistent chopper responses at frequencies other than best frequency and these units usually had non-monotonic spike functions wi~h intensity. Interval histograms have been used to demonstrate that chopper v~its fire more regularIy than primarylike units under barbiturate anaesthetic. The histograms of chopper units have bell shaped or symmetrical distributions whereas primarylike units have asymmetrical distributions that approximate an exponential distribution with dead time [ 4,10]. In the latter case, the mean of the interval distribution tends to be equal tc the standard deviation of the dis, tribution. For all chopper uni~ recorded in the pre~ent study, interval distributions
263 CWl-UNIT 18, I..E. 50/10. 30S CHOPPER 7.0
FREQUENCY (kHz) 12 O
11.0
13.0
14.0
F N,993
[ N=526
80
0
35
70 0
35
70 0
25 r SPON
m20!
N-469
N,'41
N
i~
E
L! , ~ 1 1
0
-
.~ . . . .1 . .
35 MSEC
o
P
i. . . . . . . . . . .
70 0 2.5 20
35
70 0
35
_,
35
[
+"
[
L N-540
; N=559
! N=301
![
~ " .
si }
'70 0
+!, i ..
t
ulO i
o c
35
[
.
.
.
.
"/0 0
' N-345
!
'm .
35
N=417
,
"
i
:t
,
70 '1
35
?0
r
.
'
+
70 0
.N--441
35
70
~
70
N=336
"o
40
5 0
0
35 MSEC
70 0
35
25 t 2O N-127
35
70 ,0
70 o
F i N-322
ri N-49
20
II
0
35
?0 0
:~5
,
?O 0
Ii i
35
i+
70
MSEC Fig. 1. Average ~ ~sponse histograms of a chopper unit CWl-unit 18 recorded in the posteroventral eocnlear ]mcleus for a range of frequencies and intensities. Each histogram is based en 30 presentations of a 50 msee tone burst with rise and fall times of 5.0 msec given at a rate o f 101see. The best frequency of the unit is 13.0 kHz. The number above each histogram is the spik~ count calculated during the 30 stimulus presentations. A histogram of spontaneous acti, tity (SPON) ha~ a spike count (N = 41) over the equivalent time of presentation.
approximated a symmetrical distribution and the standard deviation was much Yess than the m ean. Interval distributions were constructed for both driven and spontaneous artivity for unit CW1-18 and s t a n d a ~ deviations plotted as a function of mean interval (Fig. 2). A number of implications can be drawn from them data. When the unit is excited either by a tone or a white noise
264 CW1-18. AWAKE CAT CHOPPER ."50/10.30S, LE /
4Oi ---4 Emtoim7 SOmsectoneImrd~ o---o InlhilstorySQmmctone burtt$ SW~Ot ~ o~tN~y ~ Whitenoise 50nw4c m
0
•
tn
0
~G
10
20
30
°
0
40
50
60
MEAN INTERVAL( McM[C)
Fig. 2. Standard deviations of interval distributions plotted as a functior~ of the corresponding mean interval of the distribution for chopper unit C W l - u n i t 18. Each interval distribution was calculated for 30 presentations of 50 nmec bursts of tone or white :noise with a rise and fall time of 5.0 msec. Line of best fit superimposed on the data by hand. Similar distributions were calculated for spontaneous activity.
burst, the standard deviation of the interval distribution is always less than half the value of the corresponding mean interval. The fact that this reIation~ip applies also to white noise stimuli and that chopper AR histograms are produced by short bursts of white noise, indicates that the chopper pattern is not related to a specific tone frequency. A line of best fit superimposed on the data (Fig. 2) also reveals that both spontaneous activity and activity less than the spontaneous level (inhibition) have similar relationships. It is also clear that longer mean intervals show more divergence from the line of best fit, but this is to be expected as the number of intervals in a distribution decreases as the mean interval increases. It is striking, however, that under all stimulus conditions the unit is firing more regularly at any given mean interval than any primarylike unit recorded in the present study. Similar relationships between mean and standard deviation am seen in t h e chopper units recorded under barbiturate anaesthetic. The present data clearly show that the transformation of firing pattern taking place at a chopper unit is not basically chan~ed by the absence of barbiturate anaesthetic. ,: A number of models have been proposed to account for the regularity of firing of chopper units [4,10], all of which suggest thatthe chopper pattern might be produced by a cell which .receivesauditory nerve input through m a n y sm'allsynaptic endings. None of these models r~quims an inhibitory mechanism in the generation of the chopper pattern; the most likely hypothesis postulates temporal integration of depolarization in postsynaptic structures [4]. The resolution of the problems of h o w the chopper pattern is generated and the type of cell involved~awaits intracellularrecording and marking of these ubiquitous cochlear nucleus units. ~. . . . . . ~ •. :, .
.
265 ACKNOWL:~DGF.~I~!T
This work has been supported by grants from the Australian Research Grants Committee. REFERENCES 1 Bock, G.R., Webster, W.R. and Aitkin, L.M., Discharge patterns of single units in inferior colliculus of the alert cat, J. Neurophysiol., 35 (1972) 265--277. 2 Gisbergen, J.A.M. Van, Grashu~s, J.L., Johannesma, P.I.M, and Vendrik, A.J.H., Spectral and temporal characteristics of activation and suppression units in the cochlear nuclei of the anaesthetized cat, Exp. Brain Res., 23 (1975) 367--386. 3 Gisbergen, J.A.M. Van, Grashuis, J.L., Johannesma, P.I.M. and Vendrik, A.J.H., Neurones in the cochlear nucleus in'vestigated with tone and noise stimuli, Exp. Brain Res., 23 (1975) 387--406. 4 Gisbergen, J.A.M. Van, Gra~uis, J.L., Johannesma, P.I.M. and Vendrik, A.J.H., Statistical analysis and interpretation of the initial response of cochlear nucleus neurones to tone burets. Exp. Brain Res., 23 (1975) 407--423. 5 Godfrey, D.A., Kiang, N.Y.S. and Norris. B.E., Single unit activity in the pos~eroventral cochlear nucleus of the cat, J. Comp. Neurol., 162 (1975) 247--268. 6 Godfrey, D.A. Ki~ng, N.Y.S. and Norris, B.E., Single unit activity in the dorsal cochlear nuc!eus of the cat, J. Comp. Neurol., 162 (1975) 269--254. 7 Goldberg, J.M. and Brownell, W.E., Discharge characteristics of neurones in anteroventral and dorsal cochlear nuclei of cat, Brain Res., 64 (1973) 35--54. 8 Goldberg, J.M. and Greenwood, D.D., Response of neurones of the dorsal and posteroventral cochlear nuclei of the cat to acoustic stimuli of long duration. J. Neurophysiol., 29 (1966) 72--93. 9 Kiang, N.Y.S., Stimulus representation in the discharge patterns of auditory neurons. In D.B. Tower (Ed.), The Nervous System, Vol. 3. Human Communication and Its Disorders, Raven Preu, New York, 1975, pp. 8 1 - 9 6 . 10 Molnar, C.E. and Pfeiffer, R.R., Interpretation of spontaneous spike discharge patterns of neurons in the cochlear nucleus, Proc. IEEE, 56 (1968) 993--1004. 11 Pfeiffer, R.R., Classification of response patterns of spike discharges for units in the cochlear nucleus of unan~thetized cats, J. Neurophysiol., 19 (1976) 9.82--300. 12 Young, E.D. and Brownell, W.E., Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats, J. Neurophysiol, 19 (1976) 28~',--300.
261
CHOPPER UNITS RECORDED IN THE COCHLEAR NUCLEUS OF THE AWAKE CAT i
W.R. WEBSTER Neuropsychology Laboratory Psychology Department, Monash University, Clayton, Vic. (Australia) (Received January 5th, 1978) (Accepted January 9th, 1978)
SUMMARY
Thirty-six of 120 units recorded in the cochlem' nucleus of awake cal~s had average response histograms which showed a chopper pattern consisting of regular peaks in the initial part of the histogram. Many of the chopper units show,.*d the chopper pattern over most of the excitatory response area with the pattern being strongest at best frequency..~alysis of interval distributions of driven and spontaneous activity indicated that copper units ~ired more regularly than primarylike units. Both the nature of the chopper pattern and the frequency of its occurrence in the awake animal were similar to that observed in animals under barbiturate anaestheti~.
Most extracellular studies of neurones in the cochlear nucleus have been carried out in animals anaesthetized with barbiturate anaesthetic [2--9,11]. When short tone bursts at best frequency are used as stimuli, the most common response pattern in anaesthetized animals is one of sustained firing throughout the stimulus duration. Units showing sustained firing have been clearly divided into 2 major classes on the basis of average response (AR) histogr~ams. One class, called primarylike unii; s, have response characteristics which are very similar to those of auditory nerve fibres. Their AR histograms have an initial peak followed by a monotor~ic decay to a rate of sustained firing which continues while the tone is presented. The other class, ¢~alled chopper units, also have an AR histogram which shows a monotonic decay to a steady level of firing, but the initial part of the AR histogram l~as a series of well defined peaks. The chopper pattern becomes clear at 10--20 dB above threshold: at higher intensities the spacing between peaks decreases and the amplitude and number of peaks increases [ 5,6,9]. Primarylike urdts are recorded mainly in the ventral cochlear nucleus whereal~ chopper units are found in all divisions of the cochlear nucleus [ 9]. Recording in the dorsal cochlear nucleus of the u'nanaesthetized decerebrated
262
cat, Young and Brownell [12] reported that the chopper pattern was very infrequently observed. They suggested that the presence of anaesthetic might potentiate the chopper pattern. This suggestion is intriguing since Young and Bl~wnell also found that inhibition was more often observed in their preparation and when they injected barbiturate anaesthetic these, inhibitory responses were abolished. Single units were recorded from all divisions of the cochlear nucleus in 10 awake cats using techniques already described [1 ]. A metal chamber was positioned over a defect in the skull above the cochlear nucleus, which was ~sualized ~ t e r a small section of the cerebellum has been aspirated. After the animal recovered from the operation, a microdrive driven by a small stepping motor was inserted in the chamber. Glass coated tungsten electrodes were advanced into the cochlear nucleus. A NOVA-2/10 computer controlled stimulus presentation and both tuning curves and response areas were obtained under computer control. Thirty-six eut of 120 units recorded in all divisions of the cochlear nucleus, had the chopper pattern. These proportions are similar to those reported in the barbiturate anaesthetized cat [ 5,6]. Godfrey, Kiang and Norris [ 5] recording from the posteroventral cochlear nucleus (PVCN) observed that 50% of the units had a chopper response pattern at best frequency. Similar results were obtained in the present study. Average response histograms of one PVCN trait .are shown in Fig. 1. These histograms which were taken only from the excitatory response area of the unit illustrate some features characteristic of many choppers recorded in the present study. Firstly, t~e chopper response pattern is present over most of the response area. At best frequency (13 kHz), the chopper pattern becomes clear at 20 dB (threshold 5 dB). As intensity increases the number of peaks increases and the duration between peaks decreases. A similar pattern is present at frequencies on either side of the best frequency. If histograms are examined across any one intensity, it is clear that fewer peaks are•seen on either side of best frequency. Secondly, over the whole of the excitatory response area, the number of spikes is a monotonic increasing function of stimulus intensity at any one frequency. (~11wunit also had an inhibitory sideband which extended from 17.0 to 28,0 kHz.) Thirdly, at high iutensities, the firing rate is very high, but even then the chopper pattern is still present. Not all chopper units had such consistent chopper responses at frequencies other than best frequency and these units usually had non-monotonic spike functions wi~h intensity. Interval histograms have been used to demonstrate that chopper v~its fire more regularIy than primarylike units under barbiturate anaesthetic. The histograms of chopper units have bell shaped or symmetrical distributions whereas primarylike units have asymmetrical distributions that approximate an exponential distribution with dead time [ 4,10]. In the latter case, the mean of the interval distribution tends to be equal tc the standard deviation of the dis, tribution. For all chopper uni~ recorded in the pre~ent study, interval distributions
263 CWl-UNIT 18, I..E. 50/10. 30S CHOPPER 7.0
FREQUENCY (kHz) 12 O
11.0
13.0
14.0
F N,993
[ N=526
80
0
35
70 0
35
70 0
25 r SPON
m20!
N-469
N,'41
N
i~
E
L! , ~ 1 1
0
-
.~ . . . .1 . .
35 MSEC
o
P
i. . . . . . . . . . .
70 0 2.5 20
35
70 0
35
_,
35
[
+"
[
L N-540
; N=559
! N=301
![
~ " .
si }
'70 0
+!, i ..
t
ulO i
o c
35
[
.
.
.
.
"/0 0
' N-345
!
'm .
35
N=417
,
"
i
:t
,
70 '1
35
?0
r
.
'
+
70 0
.N--441
35
70
~
70
N=336
"o
40
5 0
0
35 MSEC
70 0
35
25 t 2O N-127
35
70 ,0
70 o
F i N-322
ri N-49
20
II
0
35
?0 0
:~5
,
?O 0
Ii i
35
i+
70
MSEC Fig. 1. Average ~ ~sponse histograms of a chopper unit CWl-unit 18 recorded in the posteroventral eocnlear ]mcleus for a range of frequencies and intensities. Each histogram is based en 30 presentations of a 50 msee tone burst with rise and fall times of 5.0 msec given at a rate o f 101see. The best frequency of the unit is 13.0 kHz. The number above each histogram is the spik~ count calculated during the 30 stimulus presentations. A histogram of spontaneous acti, tity (SPON) ha~ a spike count (N = 41) over the equivalent time of presentation.
approximated a symmetrical distribution and the standard deviation was much Yess than the m ean. Interval distributions were constructed for both driven and spontaneous artivity for unit CW1-18 and s t a n d a ~ deviations plotted as a function of mean interval (Fig. 2). A number of implications can be drawn from them data. When the unit is excited either by a tone or a white noise
264 CW1-18. AWAKE CAT CHOPPER ."50/10.30S, LE /
4Oi ---4 Emtoim7 SOmsectoneImrd~ o---o InlhilstorySQmmctone burtt$ SW~Ot ~ o~tN~y ~ Whitenoise 50nw4c m
0
•
tn
0
~G
10
20
30
°
0
40
50
60
MEAN INTERVAL( McM[C)
Fig. 2. Standard deviations of interval distributions plotted as a functior~ of the corresponding mean interval of the distribution for chopper unit C W l - u n i t 18. Each interval distribution was calculated for 30 presentations of 50 nmec bursts of tone or white :noise with a rise and fall time of 5.0 msec. Line of best fit superimposed on the data by hand. Similar distributions were calculated for spontaneous activity.
burst, the standard deviation of the interval distribution is always less than half the value of the corresponding mean interval. The fact that this reIation~ip applies also to white noise stimuli and that chopper AR histograms are produced by short bursts of white noise, indicates that the chopper pattern is not related to a specific tone frequency. A line of best fit superimposed on the data (Fig. 2) also reveals that both spontaneous activity and activity less than the spontaneous level (inhibition) have similar relationships. It is also clear that longer mean intervals show more divergence from the line of best fit, but this is to be expected as the number of intervals in a distribution decreases as the mean interval increases. It is striking, however, that under all stimulus conditions the unit is firing more regularly at any given mean interval than any primarylike unit recorded in the present study. Similar relationships between mean and standard deviation am seen in t h e chopper units recorded under barbiturate anaesthetic. The present data clearly show that the transformation of firing pattern taking place at a chopper unit is not basically chan~ed by the absence of barbiturate anaesthetic. ,: A number of models have been proposed to account for the regularity of firing of chopper units [4,10], all of which suggest thatthe chopper pattern might be produced by a cell which .receivesauditory nerve input through m a n y sm'allsynaptic endings. None of these models r~quims an inhibitory mechanism in the generation of the chopper pattern; the most likely hypothesis postulates temporal integration of depolarization in postsynaptic structures [4]. The resolution of the problems of h o w the chopper pattern is generated and the type of cell involved~awaits intracellularrecording and marking of these ubiquitous cochlear nucleus units. ~. . . . . . ~ •. :, .
.
265 ACKNOWL:~DGF.~I~!T
This work has been supported by grants from the Australian Research Grants Committee. REFERENCES 1 Bock, G.R., Webster, W.R. and Aitkin, L.M., Discharge patterns of single units in inferior colliculus of the alert cat, J. Neurophysiol., 35 (1972) 265--277. 2 Gisbergen, J.A.M. Van, Grashu~s, J.L., Johannesma, P.I.M, and Vendrik, A.J.H., Spectral and temporal characteristics of activation and suppression units in the cochlear nuclei of the anaesthetized cat, Exp. Brain Res., 23 (1975) 367--386. 3 Gisbergen, J.A.M. Van, Grashuis, J.L., Johannesma, P.I.M. and Vendrik, A.J.H., Neurones in the cochlear nucleus in'vestigated with tone and noise stimuli, Exp. Brain Res., 23 (1975) 387--406. 4 Gisbergen, J.A.M. Van, Gra~uis, J.L., Johannesma, P.I.M. and Vendrik, A.J.H., Statistical analysis and interpretation of the initial response of cochlear nucleus neurones to tone burets. Exp. Brain Res., 23 (1975) 407--423. 5 Godfrey, D.A., Kiang, N.Y.S. and Norris. B.E., Single unit activity in the pos~eroventral cochlear nucleus of the cat, J. Comp. Neurol., 162 (1975) 247--268. 6 Godfrey, D.A. Ki~ng, N.Y.S. and Norris, B.E., Single unit activity in the dorsal cochlear nuc!eus of the cat, J. Comp. Neurol., 162 (1975) 269--254. 7 Goldberg, J.M. and Brownell, W.E., Discharge characteristics of neurones in anteroventral and dorsal cochlear nuclei of cat, Brain Res., 64 (1973) 35--54. 8 Goldberg, J.M. and Greenwood, D.D., Response of neurones of the dorsal and posteroventral cochlear nuclei of the cat to acoustic stimuli of long duration. J. Neurophysiol., 29 (1966) 72--93. 9 Kiang, N.Y.S., Stimulus representation in the discharge patterns of auditory neurons. In D.B. Tower (Ed.), The Nervous System, Vol. 3. Human Communication and Its Disorders, Raven Preu, New York, 1975, pp. 8 1 - 9 6 . 10 Molnar, C.E. and Pfeiffer, R.R., Interpretation of spontaneous spike discharge patterns of neurons in the cochlear nucleus, Proc. IEEE, 56 (1968) 993--1004. 11 Pfeiffer, R.R., Classification of response patterns of spike discharges for units in the cochlear nucleus of unan~thetized cats, J. Neurophysiol., 19 (1976) 9.82--300. 12 Young, E.D. and Brownell, W.E., Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats, J. Neurophysiol, 19 (1976) 28~',--300.