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Binaural response characteristics of single neurons in the medial superior olivary nucleus of the albino rat
Brain Research 210 (1981) 361-366 © Elsevier/North-Holland Biomedical Press
361
Binaural response characteristics of single neurons in the medial superior olivary nucleus of the albino rat
STEVEN B. INBODY and ALBERT S. FENG* Department of Physiology and Biophysics, University of Illinois at Urbana-Champaign, Urbana, IlL 61081 (U.S.A.)
(Accepted November 13th, 1980) Key words: binaural response - - medial superior olivary neuron - - ear dominance
Binaural response properties of single neurons in the medial superior olivary nucleus (MSO) were investigated in the anesthetized rat. Stimulus parameters studied included interaural time difference and interaural intensity difference. In the present study, of the two cell types observed in the rat MSO nucleus, EE and El, variations in the binaural response properties of the MSO neurons permitted further subclassifications, which may be related to the dendritic dominance of the MSO neurons. Behavioral and physiological studies have shown that the mammalian medial superior olivary nucleus (MSO) is an important neural center for the processing of binaural cues for sound localizationl,a,6,9,10,1L Neurons in the central portion of the nucleus possess bipolar dendritic processes extending primarily medially and laterally, receiving separate inputs from the contralateral and the ipsilateral anterior ventral cochlear nucleus (AVCN), respectively14,15. A recent developmental study showed that 3 subtypes of bipolar neurons existed in the rat MSO depending on the dominance of the two lateral dendritic branches, i.e. left, right or equal dominance 3. Earlier physiological studies4,5,6,7,s,9,12,13 have revealed that two classes of MSO neurons could be recognized on the basis of their binaural response properties: excitatory--excitatory (EE) cells receiving excitatory input from each ear, and excitatory--inhibitory (El) cells receiving excitatory input from one ear, and inhibitory input from the other ear. The present investigation addresses the following question: are the varying morphological cell types correlated with the two primary physiological classes of neurons or possibly with subclasses of these neurons ? Evidence is presented that on the basis of the relative effectiveness of an individual ear in exciting or inhibiting the neural responses further classification could be made for each of the two primary categories of EE and El ceils which may correlate with the cell morphology. Albino rats (200-325 g) were anesthetized by i.p. injections of equithesine (0.33 ml/100 g) during the surgery and the recording session. Each animal was placed in a * To whom correspondence should be addressed.
362 stereotaxic device ( K o p f 1430) and maintained at about 37 "~C. Earphone housing with hollow ear bars were inserted into the ear canals. A craniotomy was performed and the dura mater removed. The central part of the cerebellum was then aspirated to reveal the floor of the fourth ventricle which was used as a guide for medial/lateral coordinants. Anterior/posterior coordinants were taken from lambda and bregma. During recordings, the animal was placed in a sound proof room and the electrode was positioned stereotaxically. ]'he electrode advance was later controlled with a remote hydraulic microdrive ( K o p f 1207). Indium-filled micropipettes (tip size of 7-10 #m) were used to record the activity of single cells, primarily from cell bodiesT, 8. Small lesions ( ~ 80 #m) in the brain were produced by passing radiofrequency current (10 kHz, 10 V peak to peak for 8 rain) through them at the end of each electrode track. Following each recording session, the rat was perfused with saline and 10~o formalin. The brain was extracted, embedded in gelatin and cut into frozen sections which were then stained with cresylecht violet to verify the position of the recording locus. Acoustical stimuli, consisting of binaural noise bursts and tone bursts (250 msec duration, 5 msec rise/fall time), were delivered through two independent earphone (Beyer D T 48) systems at a rate of one per 1.5 sec. Detailed instrumentation has been given elsewhere 2. For tone bursts, the phase was identical in the two channels, and in one channel it remained the same (at zero crossing) with each repeated stimulus. The onset times of the stimuli at the two ears, however, were controlled by two pulse delay units. Sound intensities were adjusted through two independent attenuators. The neural responses of single MSO neurons were displayed on a storage oscilloscope and audio monitored. The firing rate of the single unit, was measured with a gated electronic counter. For each isolated neuron the best excitatory frequency (BEF), i.e. the frequency at which the neuron had the lowest excitation threshold, was noted for each neuron. The intensity-rate function, and the responses to changes in interaural time and intensity differences of the tone bursts at the unit's BEF at 20 dB above threshold were studied. Results were averaged for 20 repetitive stimuli for each stimulus configuration, and expressed as a percentage of the maximum spike count among all acoustic stimulation conditions. For a given unit, this parameter provides a standardized assessment of the relative responsiveness of a neuron to different acoustic stimuli and of different neurons to a specific acoustic stimulus configuration (Fig. 1b). Response properties of 52 neurons identified within the MSO were reported here. Two principal classes of neurons 4-6,9,1,a,13 were distinguishable on the basis of the effects of stimulation of the two ears: EE neurons (52 ~ ) which were excitable by stimulation of either ear, and EI neurons (48 ~ ) which were excitable by stimulating one ear, exclusively by the contralateral ear in our sample, and the contralateral response could be suppressed by ipsilaterat stimulation at a suitable intensity and time. The BEF ranged from 2200 to 6600 Hz and was similar in both neuronal classes. For EE cells the BEFs for both ears were identical, and for the EI cells the BEF from the contralateral ear matched closely with the best inhibitory frequency (BIF) of the ipsilateral ear. Therefore, the unit's BEF was used in subsequent binaural studies. The
363
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Fig. 1A: monaural and binaural responses of an equal dominance EE cell (unit 15-2; BEF = 5.9 kHz). The abscissa represents the sound intensity of monaural or binaural stimuli (zero l i D ) in dB SPL @eft 0.0002 dyne/sq, cm). The ordinate represents the standardized firing rate of the unit in terms of % maximum response. The % maximum response represents a percentage of the maximum spike count among all of the monaural and binaural conditions for a given unit. Maximum response = 3.5 spikes/stimulus. The monaural responses to ipsilateral (IL) and contralateral (CL) ear stimulation are shown in empty and filled circles, respectively, and the binaural response at zero l i D is shown in squares. B: responses of the same neuron in terms of its absolute firing rate showing the variability of one trial to the next. The abscissa is the same as described in A above. The ordinate represents the average spike count of the first trial (20 presentations; solid line) and the second trial (20 presentations, broken line) for any given stimulus configuration. Data with circles and squares are for the responses to ipsilateral monaural stimulation and binaural stimulation, respectively. The average responses from the two trials are used to plot the figure in A. Unit 15-2 had a BEF of 5.9 kHz. C: monaural and binaural responses of a contralaterally dominated EE cell (unit 5-4; BEF = 5.7 kHz). Maximum response = 5.2 spikes/stimulus. D: monaural and binaural responses of an ipsilateraily dominated EE cell (unit 18-3; BEF = 6.2 kHz). Maximum response = 1.4 spikes/stimulus. Vertical bars, ranges of average firing rates.
t h r e s h o l d s o f responses o f the rat M S O n e u r o n s ranged f r o m 50 to 90 dB SPL, w h i c h are higher than t h o s e reported in other species6, 7. T h i s m a y be attributed to the p o o r e r hearing t h r e s h o l d s o f the a l b i n o rat at l o w frequencies n or effects o f anesthetic. A m o n g the 27 E E cells studied, subclassification c o u l d be m a d e o n the basis o f the r e s p o n s e d o m i n a n c e o f the i n d i v i d u a l ear as also s h o w n in the dog's M S O S , 6. In o n e subclass (n : equal monaural
6), the equal d o m i n a n c e E E cells, b o t h ears h a d a p p r o x i m a t e l y response t h r e s h o l d s
(within ±
4 dB) a n d similar i n t e n s i t y - r a t e
f u n c t i o n s . B i n a u r a l s t i m u l a t i o n w i t h e q u a l intensities at the t w o ears p r o d u c e d a higher firing rate than m o n a u r a l s t i m u l a t i o n s (unit 1 5 - 2 in Fig. la).
364
A % MAX RESPONSE
I0
8
IL>CL
6
4.
2
0
2
4
AI (dB)
6
8
I0
CL>IL
B % MAX. RESPONSE
IL LEAD
AT (msec)
CL L E A D
Fig. 2A: effect of interaural intensity difference (liD) on the responses of 3 E1 cells. The abscissa represents liD in dB, with the contralateral (CL) stimulus intensity kept at 20 dB above threshold. The ordinate represents the standardized firing rate of the unit in per cent maximum response. The ipsilateral (IL) stimulus intensityranged between ÷ 10 dB (IL)- CL) to --10 dB (IL > CL) relative to the contralateral stimulus intensity. The curve with triangles represents the responses of unit 17-6 (BEF at 6.6 kHz) exhibiting weak ipsilateral inhibition. Squares represent the responses of unit 5-2 (BEF of 6.6 kHz), which exhibited strong ipsilateral inhibition. Circles represent the responses of unit 17-9 (BEF at 4.5 kHz) which exhibited intermediate ipsilateral inhibition. Maximum response = 4.8, 0.7, 0.8 spikes/stimulus for units 17-6, 5-2 and 17-9, respectively. B: effect of interaural time difference (ITD) on the responses of 3 EI cells. The abscissa represents ITD (or AT) between the two stimuli, and the ordinate represents the standardized firing rate of the unit in per cent maximum response. Unit 18-2 (BEF of 2.5 kHz) exhibited strong ipsilateral inhibitionwhereas unit 14-1 (BEF of 2.6 kHz) exhibited weak ipsilateral inhibition. Unit 18-4 (BEF of 2.4 kHz) exhibited ipsilateral inhibitionintermediate in its response between the other two units. Maximum response - 1.0, 2.1, 2.8 spikes/stimulus for unit 18-2, 14-1, and 18-4, respectively, Vertical bars, ranges of average firing rates. The majority of EE ceils encountered were d o m i n a t e d by one ear. A n example of contralaterally d o m i n a t e d n e u r o n s (n == 19) is shown in Fig. lc ( U n i t 5-4). The threshold for ipsilateral stimulation was 4-5 dB higher t h a n that for contralateral stimulation a n d that the firing rate at any intensity level was lower for ipsilateral t h a n it was for contralateral stimulation. Binaural stimulation generally elicited stronger responses t h a n either m o n a u r a l responses.
365 In two EE neurons, the opposite was true, i.e. the ipsilateral ear dominated the contralateral ear as exemplified by the responses of unit 18-3 in Fig. ld. It did not appear that the subclassification was related to the unit's BEF or response threshold. Interestingly, the EI neurons in the rat MSO could also be subdivided into 3 classes depending on the dominance of the two inputs. Responses to interaural intensity difference (liD), for example, could show strong, weak or intermediate ipsilateral inhibition as shown in Fig. 2a. For unit 5-2 (strongly inhibited) the eontralateral response (100 % max. response) was suppressed even when the intensity of the contralateral excitatory tone was higher than that of the ipsilateral inhibitory tone. Suppression reached a 50 % level, and was complete when the contralateral stimulus intensity was 8 dB and 2dB stronger than the ipsilateral stimulus intensity, respectively. This cell then, seemed to be dominated by ipsilateral inhibitory input. Unit 17-6 (weakly inhibited), on the other hand, was characterized by dominant contralateral excitatory input. Suppression of the contralateral response was not clearly evidenced and did not reach a 50 % level until the ipsilateral inhibitory stimulus intensity was larger than the contralateral stimulus intensity. Furthermore, complete suppression did not occur in the studied I I D range. Unit 17-9 was intermediate in its response between the above two types of neurons in that neither the contralateral nor the ipsilateral ear dominated the response. The l i D response of this neuron was graded over the ~_~- 10 dB range studied. Subclassification of E1 cells could also be made on the basis of the responses to interaural time difference (ITD). Strong, weak and intermediate ipsilateral inhibition is seen in Fig. 2b for units 18-2 (BEF : 2.5 kHz), 14-1 (BEF : 2.6 kHz), and 18-4 (BEF : 2.4 kHz), respectively. With the exception of two units, subclassification of single E1 cells always agreed whether it was based on the response to I I D or I T D when both sets of data were obtained (Table I). It seemed clear that for both EE and EI cell types, either the left or right ear could dominate the unit's response, or neither was dominant. Ear dominance, therefore, did not depend on the synaptic sign. It seems that these physiological variations of the two primary neuronal classes
TABLE I Distribution o f various cell types in the rat M S O Class
Response type
Number o f neurons
EE EE EE
Dominated by contralateral excitation Dominated by ipsilateral excitation Equally dominated
EI EI EI
Total Weak ipsilateral inhibition (or strong contralateral excitation) Strong ipsilateral inhibition (or weak contralateral excitation) Intermediate ipsilateral inhibition Total
19 2 6 27 7 (0)* 4 (2)* 11 (4)* 22 (6)
* Number of neurons indicated in the bracket based on the neural response to interaural intensity difference only.
366 can be correlated, m o r e readily t h a n the two classes itself with the r e p o r t e d 3 m o r p h o l o g i c a l l y different b i p o l a r l y projecting rat M S O n e u r o n s : left, right and equal d o m i n a n t dendritic trees a. However, this correlation c a n n o t be unequivocally m a d e w i t h o u t identifying the m o r p h o l o g y o f the recorded cell. The a n a t o m i c a l study reveals t h a t in the n o r m a l rat there is a n a p p r o x i m a t e l y equal n u m b e r o f neurons with d o m i n a n t left or right dendritic trees and a low percentage o f neurons with equaW d o m i n a n t dendritic trees. D i s t r i b u t i o n o f these cell types is in variance with the d i s t r i b u t i o n o f the various subcategories of EE cells a n d o f EI cells from the physiological study. These discrepancies are p r o b a b l y a t t r i b u t e d to r a n d o m sampling o f the r e c o r d i n g electrode and inclusion o f d a t a from m u l t i p o l a r neurons or differences in the criteria chosen for n e u r o n a l classification, lntracellular recording and staining techniques will be necessary to correlate the binaural response properties of a M S O n e u r o n with its dendritic m o r p h o l o g y . W e t h a n k Z. Fuzessery a n d B. A. R o g o w s k i for their c o m m e n t s on the manuscript. S u p p o r t e d by the Research B o a r d o f the University o f Illinois, Biomedical Research G r a n t s , and N . I . H . G r a n t s NS 14488 to A . S . F .
1 Casseday, J. H. and Neff, W. D., Auditory localization: role of auditory pathways in brainstem of the cat, J. Neurophysiol., 38 (1975) 842-858. 2 Feng, A. S., Directional characteristics of the acoustic receiver of the leopard frog (Ranapipiens) : a study of eighth nerve auditory responses, J. acoust. Soc. Amer., 68 (1980) 1107-1114. 3 Feng, A. S. and Rogowski, B. A., Effects of monaural and binaural occlusion on the morphology of neurons in the medial superior olivary nucleus of the rat, Brain Research, 189 (1980) 530-534. 4 Galambos, R., Schwartzkopff, J. and Rupert, A. R., Microelectrode study of superior olivary nuclei, Amer J. Physiol., 197 (1959) 527-536. 5 Goldberg, J. M. and Brown, P. B., Functional organization of the dog superior olivary complex: An anatomical and electrophysiological study, J. Neurophysiol., 31 (1968) 639-656. 6 Goldberg, J. M. and Brown, P. B., Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli : some physiological mechanisms of sound localization, J. Neurophysiol., 32 (1969) 613-636. 7 Guinan, J. J., Guinan, S. S. and Norris, B. E. Single auditory units in the superior olivary complex. I: responses to sounds and classification based on physiological properties, Int. J. Neurosci., 4 (1972) 101-120. 8 Guinan, J. J., Guinan, S. S. and Norris, B. E., Single auditory units in the superior olivary complex II. Locations of units, categories and tonotopic organization, Int. J. Neurosci., 4 (1972) 147-166. 9 Hall, J. L., Binaural interaction in the accessory superior olivary nucleus of the cat, J. acoust. Soc. Arner., 37 (1965) 814-823. 10 Harrison, J. M. and Irving, R., Visual and nonvisual auditory systems in mammals, Science, 154 (1965) 738-743. 11 Kelly, J. B. and Masterton, R. B., Auditory sensitivity of the albino rat, J. comp. physiol. Psychol., 91 (1977) 930-936. 12 Moushegian, G. A., Rupert, A. and Gidds, J., Functional characteristics of superior olivary neurons to binaural stimuli, J. Neurophysiol., 38 (1975) 1037-1048. 13 Moushegian, G., Rupert, A. and Whitcomb, M. A., Medial superior olivary-unit response patterns to monaural and binaural clicks, J. acoust. Soc. Amer, 36 (1964) 196-202. 14 Perkins, R. E., An electron microscopic study of synaptic organization in the medial superior olive of normal and experimental chinchillas, J. comp. Neurol., 148 (1973) 387-416. 15 Stotler, W. A., An experimental study of the cells and connections of the superior olivary complex of the cat, J. comp. Neurol., 98 (1953) 401-432.
361
Binaural response characteristics of single neurons in the medial superior olivary nucleus of the albino rat
STEVEN B. INBODY and ALBERT S. FENG* Department of Physiology and Biophysics, University of Illinois at Urbana-Champaign, Urbana, IlL 61081 (U.S.A.)
(Accepted November 13th, 1980) Key words: binaural response - - medial superior olivary neuron - - ear dominance
Binaural response properties of single neurons in the medial superior olivary nucleus (MSO) were investigated in the anesthetized rat. Stimulus parameters studied included interaural time difference and interaural intensity difference. In the present study, of the two cell types observed in the rat MSO nucleus, EE and El, variations in the binaural response properties of the MSO neurons permitted further subclassifications, which may be related to the dendritic dominance of the MSO neurons. Behavioral and physiological studies have shown that the mammalian medial superior olivary nucleus (MSO) is an important neural center for the processing of binaural cues for sound localizationl,a,6,9,10,1L Neurons in the central portion of the nucleus possess bipolar dendritic processes extending primarily medially and laterally, receiving separate inputs from the contralateral and the ipsilateral anterior ventral cochlear nucleus (AVCN), respectively14,15. A recent developmental study showed that 3 subtypes of bipolar neurons existed in the rat MSO depending on the dominance of the two lateral dendritic branches, i.e. left, right or equal dominance 3. Earlier physiological studies4,5,6,7,s,9,12,13 have revealed that two classes of MSO neurons could be recognized on the basis of their binaural response properties: excitatory--excitatory (EE) cells receiving excitatory input from each ear, and excitatory--inhibitory (El) cells receiving excitatory input from one ear, and inhibitory input from the other ear. The present investigation addresses the following question: are the varying morphological cell types correlated with the two primary physiological classes of neurons or possibly with subclasses of these neurons ? Evidence is presented that on the basis of the relative effectiveness of an individual ear in exciting or inhibiting the neural responses further classification could be made for each of the two primary categories of EE and El ceils which may correlate with the cell morphology. Albino rats (200-325 g) were anesthetized by i.p. injections of equithesine (0.33 ml/100 g) during the surgery and the recording session. Each animal was placed in a * To whom correspondence should be addressed.
362 stereotaxic device ( K o p f 1430) and maintained at about 37 "~C. Earphone housing with hollow ear bars were inserted into the ear canals. A craniotomy was performed and the dura mater removed. The central part of the cerebellum was then aspirated to reveal the floor of the fourth ventricle which was used as a guide for medial/lateral coordinants. Anterior/posterior coordinants were taken from lambda and bregma. During recordings, the animal was placed in a sound proof room and the electrode was positioned stereotaxically. ]'he electrode advance was later controlled with a remote hydraulic microdrive ( K o p f 1207). Indium-filled micropipettes (tip size of 7-10 #m) were used to record the activity of single cells, primarily from cell bodiesT, 8. Small lesions ( ~ 80 #m) in the brain were produced by passing radiofrequency current (10 kHz, 10 V peak to peak for 8 rain) through them at the end of each electrode track. Following each recording session, the rat was perfused with saline and 10~o formalin. The brain was extracted, embedded in gelatin and cut into frozen sections which were then stained with cresylecht violet to verify the position of the recording locus. Acoustical stimuli, consisting of binaural noise bursts and tone bursts (250 msec duration, 5 msec rise/fall time), were delivered through two independent earphone (Beyer D T 48) systems at a rate of one per 1.5 sec. Detailed instrumentation has been given elsewhere 2. For tone bursts, the phase was identical in the two channels, and in one channel it remained the same (at zero crossing) with each repeated stimulus. The onset times of the stimuli at the two ears, however, were controlled by two pulse delay units. Sound intensities were adjusted through two independent attenuators. The neural responses of single MSO neurons were displayed on a storage oscilloscope and audio monitored. The firing rate of the single unit, was measured with a gated electronic counter. For each isolated neuron the best excitatory frequency (BEF), i.e. the frequency at which the neuron had the lowest excitation threshold, was noted for each neuron. The intensity-rate function, and the responses to changes in interaural time and intensity differences of the tone bursts at the unit's BEF at 20 dB above threshold were studied. Results were averaged for 20 repetitive stimuli for each stimulus configuration, and expressed as a percentage of the maximum spike count among all acoustic stimulation conditions. For a given unit, this parameter provides a standardized assessment of the relative responsiveness of a neuron to different acoustic stimuli and of different neurons to a specific acoustic stimulus configuration (Fig. 1b). Response properties of 52 neurons identified within the MSO were reported here. Two principal classes of neurons 4-6,9,1,a,13 were distinguishable on the basis of the effects of stimulation of the two ears: EE neurons (52 ~ ) which were excitable by stimulation of either ear, and EI neurons (48 ~ ) which were excitable by stimulating one ear, exclusively by the contralateral ear in our sample, and the contralateral response could be suppressed by ipsilaterat stimulation at a suitable intensity and time. The BEF ranged from 2200 to 6600 Hz and was similar in both neuronal classes. For EE cells the BEFs for both ears were identical, and for the EI cells the BEF from the contralateral ear matched closely with the best inhibitory frequency (BIF) of the ipsilateral ear. Therefore, the unit's BEF was used in subsequent binaural studies. The
363
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80
82
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INTENSITY
90 (dB SPL) 88
92
Fig. 1A: monaural and binaural responses of an equal dominance EE cell (unit 15-2; BEF = 5.9 kHz). The abscissa represents the sound intensity of monaural or binaural stimuli (zero l i D ) in dB SPL @eft 0.0002 dyne/sq, cm). The ordinate represents the standardized firing rate of the unit in terms of % maximum response. The % maximum response represents a percentage of the maximum spike count among all of the monaural and binaural conditions for a given unit. Maximum response = 3.5 spikes/stimulus. The monaural responses to ipsilateral (IL) and contralateral (CL) ear stimulation are shown in empty and filled circles, respectively, and the binaural response at zero l i D is shown in squares. B: responses of the same neuron in terms of its absolute firing rate showing the variability of one trial to the next. The abscissa is the same as described in A above. The ordinate represents the average spike count of the first trial (20 presentations; solid line) and the second trial (20 presentations, broken line) for any given stimulus configuration. Data with circles and squares are for the responses to ipsilateral monaural stimulation and binaural stimulation, respectively. The average responses from the two trials are used to plot the figure in A. Unit 15-2 had a BEF of 5.9 kHz. C: monaural and binaural responses of a contralaterally dominated EE cell (unit 5-4; BEF = 5.7 kHz). Maximum response = 5.2 spikes/stimulus. D: monaural and binaural responses of an ipsilateraily dominated EE cell (unit 18-3; BEF = 6.2 kHz). Maximum response = 1.4 spikes/stimulus. Vertical bars, ranges of average firing rates.
t h r e s h o l d s o f responses o f the rat M S O n e u r o n s ranged f r o m 50 to 90 dB SPL, w h i c h are higher than t h o s e reported in other species6, 7. T h i s m a y be attributed to the p o o r e r hearing t h r e s h o l d s o f the a l b i n o rat at l o w frequencies n or effects o f anesthetic. A m o n g the 27 E E cells studied, subclassification c o u l d be m a d e o n the basis o f the r e s p o n s e d o m i n a n c e o f the i n d i v i d u a l ear as also s h o w n in the dog's M S O S , 6. In o n e subclass (n : equal monaural
6), the equal d o m i n a n c e E E cells, b o t h ears h a d a p p r o x i m a t e l y response t h r e s h o l d s
(within ±
4 dB) a n d similar i n t e n s i t y - r a t e
f u n c t i o n s . B i n a u r a l s t i m u l a t i o n w i t h e q u a l intensities at the t w o ears p r o d u c e d a higher firing rate than m o n a u r a l s t i m u l a t i o n s (unit 1 5 - 2 in Fig. la).
364
A % MAX RESPONSE
I0
8
IL>CL
6
4.
2
0
2
4
AI (dB)
6
8
I0
CL>IL
B % MAX. RESPONSE
IL LEAD
AT (msec)
CL L E A D
Fig. 2A: effect of interaural intensity difference (liD) on the responses of 3 E1 cells. The abscissa represents liD in dB, with the contralateral (CL) stimulus intensity kept at 20 dB above threshold. The ordinate represents the standardized firing rate of the unit in per cent maximum response. The ipsilateral (IL) stimulus intensityranged between ÷ 10 dB (IL)- CL) to --10 dB (IL > CL) relative to the contralateral stimulus intensity. The curve with triangles represents the responses of unit 17-6 (BEF at 6.6 kHz) exhibiting weak ipsilateral inhibition. Squares represent the responses of unit 5-2 (BEF of 6.6 kHz), which exhibited strong ipsilateral inhibition. Circles represent the responses of unit 17-9 (BEF at 4.5 kHz) which exhibited intermediate ipsilateral inhibition. Maximum response = 4.8, 0.7, 0.8 spikes/stimulus for units 17-6, 5-2 and 17-9, respectively. B: effect of interaural time difference (ITD) on the responses of 3 EI cells. The abscissa represents ITD (or AT) between the two stimuli, and the ordinate represents the standardized firing rate of the unit in per cent maximum response. Unit 18-2 (BEF of 2.5 kHz) exhibited strong ipsilateral inhibitionwhereas unit 14-1 (BEF of 2.6 kHz) exhibited weak ipsilateral inhibition. Unit 18-4 (BEF of 2.4 kHz) exhibited ipsilateral inhibitionintermediate in its response between the other two units. Maximum response - 1.0, 2.1, 2.8 spikes/stimulus for unit 18-2, 14-1, and 18-4, respectively, Vertical bars, ranges of average firing rates. The majority of EE ceils encountered were d o m i n a t e d by one ear. A n example of contralaterally d o m i n a t e d n e u r o n s (n == 19) is shown in Fig. lc ( U n i t 5-4). The threshold for ipsilateral stimulation was 4-5 dB higher t h a n that for contralateral stimulation a n d that the firing rate at any intensity level was lower for ipsilateral t h a n it was for contralateral stimulation. Binaural stimulation generally elicited stronger responses t h a n either m o n a u r a l responses.
365 In two EE neurons, the opposite was true, i.e. the ipsilateral ear dominated the contralateral ear as exemplified by the responses of unit 18-3 in Fig. ld. It did not appear that the subclassification was related to the unit's BEF or response threshold. Interestingly, the EI neurons in the rat MSO could also be subdivided into 3 classes depending on the dominance of the two inputs. Responses to interaural intensity difference (liD), for example, could show strong, weak or intermediate ipsilateral inhibition as shown in Fig. 2a. For unit 5-2 (strongly inhibited) the eontralateral response (100 % max. response) was suppressed even when the intensity of the contralateral excitatory tone was higher than that of the ipsilateral inhibitory tone. Suppression reached a 50 % level, and was complete when the contralateral stimulus intensity was 8 dB and 2dB stronger than the ipsilateral stimulus intensity, respectively. This cell then, seemed to be dominated by ipsilateral inhibitory input. Unit 17-6 (weakly inhibited), on the other hand, was characterized by dominant contralateral excitatory input. Suppression of the contralateral response was not clearly evidenced and did not reach a 50 % level until the ipsilateral inhibitory stimulus intensity was larger than the contralateral stimulus intensity. Furthermore, complete suppression did not occur in the studied I I D range. Unit 17-9 was intermediate in its response between the above two types of neurons in that neither the contralateral nor the ipsilateral ear dominated the response. The l i D response of this neuron was graded over the ~_~- 10 dB range studied. Subclassification of E1 cells could also be made on the basis of the responses to interaural time difference (ITD). Strong, weak and intermediate ipsilateral inhibition is seen in Fig. 2b for units 18-2 (BEF : 2.5 kHz), 14-1 (BEF : 2.6 kHz), and 18-4 (BEF : 2.4 kHz), respectively. With the exception of two units, subclassification of single E1 cells always agreed whether it was based on the response to I I D or I T D when both sets of data were obtained (Table I). It seemed clear that for both EE and EI cell types, either the left or right ear could dominate the unit's response, or neither was dominant. Ear dominance, therefore, did not depend on the synaptic sign. It seems that these physiological variations of the two primary neuronal classes
TABLE I Distribution o f various cell types in the rat M S O Class
Response type
Number o f neurons
EE EE EE
Dominated by contralateral excitation Dominated by ipsilateral excitation Equally dominated
EI EI EI
Total Weak ipsilateral inhibition (or strong contralateral excitation) Strong ipsilateral inhibition (or weak contralateral excitation) Intermediate ipsilateral inhibition Total
19 2 6 27 7 (0)* 4 (2)* 11 (4)* 22 (6)
* Number of neurons indicated in the bracket based on the neural response to interaural intensity difference only.
366 can be correlated, m o r e readily t h a n the two classes itself with the r e p o r t e d 3 m o r p h o l o g i c a l l y different b i p o l a r l y projecting rat M S O n e u r o n s : left, right and equal d o m i n a n t dendritic trees a. However, this correlation c a n n o t be unequivocally m a d e w i t h o u t identifying the m o r p h o l o g y o f the recorded cell. The a n a t o m i c a l study reveals t h a t in the n o r m a l rat there is a n a p p r o x i m a t e l y equal n u m b e r o f neurons with d o m i n a n t left or right dendritic trees and a low percentage o f neurons with equaW d o m i n a n t dendritic trees. D i s t r i b u t i o n o f these cell types is in variance with the d i s t r i b u t i o n o f the various subcategories of EE cells a n d o f EI cells from the physiological study. These discrepancies are p r o b a b l y a t t r i b u t e d to r a n d o m sampling o f the r e c o r d i n g electrode and inclusion o f d a t a from m u l t i p o l a r neurons or differences in the criteria chosen for n e u r o n a l classification, lntracellular recording and staining techniques will be necessary to correlate the binaural response properties of a M S O n e u r o n with its dendritic m o r p h o l o g y . W e t h a n k Z. Fuzessery a n d B. A. R o g o w s k i for their c o m m e n t s on the manuscript. S u p p o r t e d by the Research B o a r d o f the University o f Illinois, Biomedical Research G r a n t s , and N . I . H . G r a n t s NS 14488 to A . S . F .
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