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Auditory orienting and detection in rats following lesions of the superior colliculus
293
Behavioural Brain Research, 37 (1990) 293-296 Elsevier BBR 01025
Short Communication
Auditory orienting and detection in rats following lesions of the superior colliculus A. D a v i d M i l n e r a n d M a r k J. T a y l o r Department of Psychology, University of St. Andrews, Fife, Scotland (U.K.) (Received 30 June 1989) (Accepted 12 October 1989)
Key words: Superior colliculus; Auditory; Orienting; Detection; Dissociation; Rat
Rats were trained to run towards a lighted target following either bilateral lesions of the superior colliculus (SC) or control lesions of the overlying cortex. At 4 months post-surgery, the animals were tested for the disruptive effects of an auditory tone. An increase in running times was found in both groups, attributable to frequent freezing reactions in all animals. However, only the control rats made orienting reactions to the tones. It is argued that the freezing responses show that the SC lesions did not impair sensory detection; consequently, the orienting failure cannot be attributed to a sensory deficit.
It has been argued by some authors in recent years that the well-documented disorder of visual orienting that follows lesions of the superior colliculus ( S C ) 4'16 c a n be attributed to a specific detection deficit 2. The orienting failures tend to be most obvious in relation to transient or intermittent stimuli in the peripheral visual field, and the loss of SC cells that respond to such stimuli is specifically assumed to be responsible for the detection deficit. That there is a detection loss seems clear from the work ofOverton et al. 13: rats that had been trained to turn and run towards a light in the peripheral field failed even to disengage from the central water tube following collicular lesions. It would be astonishing indeed if such a detection disorder did not occur; almost all the rat's retinal ganglion cells project to the SC 9, far more than project to other retinofugal targets ~°.
However a detection deficit cannot account for all the observed failures to orient to visual stimuli. In a task requiring running towards a prominent target in an open field, there is initially neither orienting nor freezing in response to a novel peripheral light flash following SC ablations 5'6. However, if the rats are not tested until some 3 months postoperatively, freezing reactions, but not orienting responses, have been found to be reinstated ~2. Yet rats tested in the same apparatus after only 1 postoperative month showed both deficits. This suggests that there may be at least two dissociable disorders when the SC is damaged: one of visual detection, which may show a variable degree of recovery over timel,8; and one of orienting, which may be permanent. In any event, no purely sensory account of the clear orienting deficit that was seen in the 3-month
Correspondence: A.D. Milner, Psychological Laboratory, The University, St. Andrews, Fife KY16 9JU, Scotland, U.K. 0166-4328/90/$03.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)
294 animals can readily explain how freezing responses could have been made by the same animals to the s a m e stimuli. In the present report, a comparable question was asked concerning the auditory modality. The SC receives a substantial auditory input via both mesencephalic and cortical routes 3 and many SC cells are responsive to or are modulated by auditory stimuli 14A7. Goodale and Murison 5 showed that SC lesions abolished the normal disruptive effect of a loud 5-s train of clicks presented during visually-guided running by their rats, just as was found with visual distractors; the animals neither froze nor oriented. Their procedure was repeated in the present study, with minor modifications, but the rats were not tested until 14 weeks had elapsed after surgery. Twelve male hooded Lister rats, housed individually on a 12/12 h light/dark cycle with ad libitum water, served as subjects. They were tested on a 22-h food deprivation schedule, their weights being maintained at not less than 85 ~o of their ad libitum values. The animals had a mean weight of 274 g and a mean age of 84 days at surgery, and were allocated randomly to an experimental group (n = 6) and a sham control group (n = 6). Animals of the experimental group received bilateral radiofrequency ablations of the SC in the standard manner used in this laboratory 12. The control group received small bilateral aspiration lesions of the cerebral hemispheres at those same horizontal (AP and L) coordinates, designed to duplicate the damage inevitably sustained to overlying tissue during SC surgery. As the previous study 12, the rats were trained postoperatively to run between two 90 cm × 90 cm x 40 cm-high boxes connected by a short tunnel. Passage through a photocell beam located 30 cm from the back of a given box caused a 6-V light to be illuminated behind a single door set centrally in the far wall of the other box. (The other doors used in the previous study were blocked.) The light was extinguished 3 s after a push on the illuminated door, during which time a condensed milk reward was available there. Extraneous noises were masked by an external white noise generator (65 dB at a central point in either box). Running times (between crossing the photo-
cell beam in the current box and response to the target door) were measured to the nearest 10 ms, and the behaviour of each animal was recorded through an overhead video camera. A laboratory computer controlled the experiment and logged the running times, which were averaged on nontest trials using harmonic means. Starting 5 weeks after surgery, several stages of pretraining was given for 8 days, followed by 16 training days of 40 trials, after which various visual distraction tests were administered (not reported here). There were 4 auditory test sessions, given at 14 weeks post-surgery. On trial 39 of these sessions a novel tone was presented through one of 2 speakers each located on a side wall 30 cm above the floor and 30 cm forwards from the back wall in one box. The speaker used alternated between left and right (LRRL or RLLR, balanced across rats) over the 4 trials. The tone was presented at a frequency of 4 kHz, oscillating on/offat 5 Hz, with a mean intensity of 77 dB; it was triggered by the animal's breaking the photobeam in that box, and ended after 5 s or when the correct door was pushed. After the completion of behavioural testing, the brains were sectioned at 40 ~tm and every other section saved. Half of these were stained with Cresyl violet. In some brains, the alternate sections were stained for acetylcholinesterase, and in others for H R P histochemistry following ocular injection. A reconstruction of a typical SC lesion (animal SC3) is shown in Fig. 1. The lesions removed most of the SC bilaterally in all 6 rats, with some inevitable damage sustained posteriorly in the inferior colliculi (4 rats), anteriorly in the pretectal nuclei (3 rats), and dorsally in the cortex (all 6 rats). The cortex was damaged to a comparable extent in the control group; in addition there was very slight damage to the superficial SC in 2 animals (SH4 and SH5). In both groups the cortical damage was located almost exclusively in the medial area R S G of Zilles 19, although there was slight damage in some cases to the medial subiculum (CA1). The log-transformed running times were subjected to 3-way ANOVA, in which the factors were groups, sessions, and trials (training mean versus test). Main effects were found only for
295
. .'~
.~'
',.,/
[
';
~,
Fig. 1. A representatwe midbrain lesion (SC3). The extent of the ablation is indicated on standard cross-sections taken from the KOnig and Klippel 7 atlas.
trials ( F = 6 9 . 7 3 , d f = 1.10, P < 0 . 0 0 0 1 ) and sessions ( F = 7.87, d f = 3.30, P < 0 . 0 0 1 ) , the groups not differing overall ( F > 1). The trials effect reveals a substantial disruption of running by the tone in both groups. As shown in Fig. 2, the sessions effect resolved into the interaction with trials (F = 8.11, df = 3.30, P < 0.001), reflecting a
HAM
15
SC LESION
50 2o~ C ~OZ --4
F---.lo Z 'E) e~o.5
clear habituation effect to the tones over the 4 sessions. The lack of a significant groups by trials interaction (P > 0.10) provided no evidence for a differential effect of the tones on the running speeds of the 2 groups. Both the interaction between groups and sessions ( F = 3.13, df = 3.30, P < 0.05) and the 3-way interaction
100
q o
2
3
4 TEST SESSIONS
Fig. 2. Running times recorded in the 4 auditory test sessions: means and standard errors for the 6 rats in each group. The times for the standard training trials (squares) are based on the harmonic mean for each session, and are given along with the times for the auditory 'distraction' trials (circles).
Freezeor Headturn retreat (n.s.) (P' ~ =.oo2) ~T~
Long run times
SH
SH
n.si
5o
SC
SH
SC
SC
Fig. 3. Behavioural reactions made to the auditory distractors: means and standard errors, calculated across the 6 rats in each group.
296
( F = 3 . 1 8 , d f = 3.30, P < 0 . 0 5 ) were however marginally significant, presumably reflecting a slightly different habituation rate to the tones in the 2 groups. Behavioural reactions to the tones were categorized non-exclusively as freezing, orienting (head-turn), and retreating (into the tunnel). As Fig. 3 shows, the incidence of freezing and retreating was not dissimilar in the 2 groups, and paralleled the occurrence of long running times (i.e. those outside the range of training trial latencies for that session). However, there was a clear difference between the 2 groups in the frequency of orienting reactions (Mann-Whitney test: U = 0, P < 0.001). It is clear that the rats of both groups detected the tones, since their running was disrupted by them to a similar extent. Consequently the failure of the SC-lesioned rats to orient to the tones cannot be attributed to a sensory loss. In the auditory modality, therefore, the SC clearly does not play a purely sensory role, but does seem (in rats: there may be a difference in cats TM) to be crucially involved in the mediation of overt orienting acts. This conclusion tends to strengthen the similar conclusion reached for the visual modality elsewhere TM. Precisely what role the SC plays in the orienting process is unclear: it could be that its crucial contribution is in localizing the auditory stimulus ~5 rather than in organizing the motor act. However, it should be noted that covert orienting, i.e. such attentional realignment as may be a prerequisite for any adaptive response to an external stimulus, seems not to have been impaired by the SC lesions; freezing and fleeing are entirely appropriate responses in our test setting, and these were not significantly impaired. For auditory stimuli, at least, it therefore seems that such non-orienting responses to novel stimuli can be mediated by other structures. REFERENCES 1 Albano, J.E., Mishkin, M., Westbrook, L.E. and Wurtz, R.H., Visuomotor deficits following ablation of monkey superior colliculus, J. Neurophysiol., 48 (1982) 338-350.
2 Dean, P, and Redgrave, P., The superior colliculus and visual neglect in rat and hamster. I. Bebavioural evidence, Brain Res. Rev., 8 (1984) 129-141. 3 Druga, R. and Syka, J., Projection from auditory structures to the superior colliculus in the rat, Neurosci. Lett., 45 (1984) 247-252. 4 Goodale, M.A. and Milner, A.D., Fractionating orientation behavior in the rodent. In D. Ingle, M.A. Goodale and R.J.W. Mansfield (Eds.), The Analysis of Visual Behavior, M.I.T. Press, Cambridge MA, 1982, pp. 267-299. 5 Goodale, M.A. and Murison, R.C.C., The effects of lesions of the superior colliculus on locomotor orientation and the orienting reflex in the rat, Brain Res., 88 (1975) 243-261. 6 Goodale, M.A., Foreman, N.P. and Milner, A.D., Visual orientation in the rat: a dissociation of the deficits following cortical and collicular lesions, Exp. Brain Res., 31 (1978) 445-457. 7 K0nig, J.F.R. and Klippel, R.A., The Rat Brain: A Stereotaxic Atlas of the Forebrain and Lower Parts of the Brain Stem, Williams and Wilkins, Baltimore MD, 1963. 8 Latto, R. and Cowey, A., Visual field defects after frontal eye field lesions in monkeys. Brain Res., 30 (1971) 1-24. 9 Linden, P. and Perry, V.H., Massive retinotectal projection in rats, Brain Res., 272 (1983) 145-149. 10 Martin, P.R., The projection of different retinal ganglion cell classes to the dorsal lateral geniculate nucleus in the hooded rat, Exp. Brain Res., 62 (1986) 77-88. 11 Midgley, G.C., Wilkie, D.M. and Tees, R.C., Effects of superior colliculus lesions on rats' orienting and detection of neglected visual cues, Behav. Neurosci., 102 (1988) 93-100. 12 Milner, A.D., Lines, C.R. and Migdal, B., Visual orientation and detection following lesions of the superior colliculus in rats, Exp. Brain Res., 56 (1984) 106-114. 13 Overton, P., Dean, P. and Redgrave, P., Detection of visual stimuli in far periphery by rats: possible role of superior colliculus, Exp. Brain Res., 59 (1985) 559-569. 14 Peck, C.K., Visual-auditory interactions in cat superior colliculus: their role in the control of gaze, Brain Res., 420 (1987) 162-166. 15 Schneider, G.E., Two visual systems, Science, 163 (1969) 895-902. 16 Sprague, J.M., The superior colliculus and pretectum in visual behavior, Invest. Ophthalmol., 11 (1972) 473-482. 17 Stein, B.E., Multimodal representation in the superior colliculus and optic tectum. In H. Vanegas (Ed.) Comparative Neurology of the Optic Tectum, Plenum, New York, 1984, pp. 819-841. 18 Thompson, G.C. and Masterton, R.B., Brainstem auditory pathways involved in reflexive head orientation to sound, J. Neurophysiol., 41, (1978) 1183-1202. 19 Zilles, K., The Cortex of the Rat, A Stereotaxic Atlas, Springer, New York, 1985.
Behavioural Brain Research, 37 (1990) 293-296 Elsevier BBR 01025
Short Communication
Auditory orienting and detection in rats following lesions of the superior colliculus A. D a v i d M i l n e r a n d M a r k J. T a y l o r Department of Psychology, University of St. Andrews, Fife, Scotland (U.K.) (Received 30 June 1989) (Accepted 12 October 1989)
Key words: Superior colliculus; Auditory; Orienting; Detection; Dissociation; Rat
Rats were trained to run towards a lighted target following either bilateral lesions of the superior colliculus (SC) or control lesions of the overlying cortex. At 4 months post-surgery, the animals were tested for the disruptive effects of an auditory tone. An increase in running times was found in both groups, attributable to frequent freezing reactions in all animals. However, only the control rats made orienting reactions to the tones. It is argued that the freezing responses show that the SC lesions did not impair sensory detection; consequently, the orienting failure cannot be attributed to a sensory deficit.
It has been argued by some authors in recent years that the well-documented disorder of visual orienting that follows lesions of the superior colliculus ( S C ) 4'16 c a n be attributed to a specific detection deficit 2. The orienting failures tend to be most obvious in relation to transient or intermittent stimuli in the peripheral visual field, and the loss of SC cells that respond to such stimuli is specifically assumed to be responsible for the detection deficit. That there is a detection loss seems clear from the work ofOverton et al. 13: rats that had been trained to turn and run towards a light in the peripheral field failed even to disengage from the central water tube following collicular lesions. It would be astonishing indeed if such a detection disorder did not occur; almost all the rat's retinal ganglion cells project to the SC 9, far more than project to other retinofugal targets ~°.
However a detection deficit cannot account for all the observed failures to orient to visual stimuli. In a task requiring running towards a prominent target in an open field, there is initially neither orienting nor freezing in response to a novel peripheral light flash following SC ablations 5'6. However, if the rats are not tested until some 3 months postoperatively, freezing reactions, but not orienting responses, have been found to be reinstated ~2. Yet rats tested in the same apparatus after only 1 postoperative month showed both deficits. This suggests that there may be at least two dissociable disorders when the SC is damaged: one of visual detection, which may show a variable degree of recovery over timel,8; and one of orienting, which may be permanent. In any event, no purely sensory account of the clear orienting deficit that was seen in the 3-month
Correspondence: A.D. Milner, Psychological Laboratory, The University, St. Andrews, Fife KY16 9JU, Scotland, U.K. 0166-4328/90/$03.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)
294 animals can readily explain how freezing responses could have been made by the same animals to the s a m e stimuli. In the present report, a comparable question was asked concerning the auditory modality. The SC receives a substantial auditory input via both mesencephalic and cortical routes 3 and many SC cells are responsive to or are modulated by auditory stimuli 14A7. Goodale and Murison 5 showed that SC lesions abolished the normal disruptive effect of a loud 5-s train of clicks presented during visually-guided running by their rats, just as was found with visual distractors; the animals neither froze nor oriented. Their procedure was repeated in the present study, with minor modifications, but the rats were not tested until 14 weeks had elapsed after surgery. Twelve male hooded Lister rats, housed individually on a 12/12 h light/dark cycle with ad libitum water, served as subjects. They were tested on a 22-h food deprivation schedule, their weights being maintained at not less than 85 ~o of their ad libitum values. The animals had a mean weight of 274 g and a mean age of 84 days at surgery, and were allocated randomly to an experimental group (n = 6) and a sham control group (n = 6). Animals of the experimental group received bilateral radiofrequency ablations of the SC in the standard manner used in this laboratory 12. The control group received small bilateral aspiration lesions of the cerebral hemispheres at those same horizontal (AP and L) coordinates, designed to duplicate the damage inevitably sustained to overlying tissue during SC surgery. As the previous study 12, the rats were trained postoperatively to run between two 90 cm × 90 cm x 40 cm-high boxes connected by a short tunnel. Passage through a photocell beam located 30 cm from the back of a given box caused a 6-V light to be illuminated behind a single door set centrally in the far wall of the other box. (The other doors used in the previous study were blocked.) The light was extinguished 3 s after a push on the illuminated door, during which time a condensed milk reward was available there. Extraneous noises were masked by an external white noise generator (65 dB at a central point in either box). Running times (between crossing the photo-
cell beam in the current box and response to the target door) were measured to the nearest 10 ms, and the behaviour of each animal was recorded through an overhead video camera. A laboratory computer controlled the experiment and logged the running times, which were averaged on nontest trials using harmonic means. Starting 5 weeks after surgery, several stages of pretraining was given for 8 days, followed by 16 training days of 40 trials, after which various visual distraction tests were administered (not reported here). There were 4 auditory test sessions, given at 14 weeks post-surgery. On trial 39 of these sessions a novel tone was presented through one of 2 speakers each located on a side wall 30 cm above the floor and 30 cm forwards from the back wall in one box. The speaker used alternated between left and right (LRRL or RLLR, balanced across rats) over the 4 trials. The tone was presented at a frequency of 4 kHz, oscillating on/offat 5 Hz, with a mean intensity of 77 dB; it was triggered by the animal's breaking the photobeam in that box, and ended after 5 s or when the correct door was pushed. After the completion of behavioural testing, the brains were sectioned at 40 ~tm and every other section saved. Half of these were stained with Cresyl violet. In some brains, the alternate sections were stained for acetylcholinesterase, and in others for H R P histochemistry following ocular injection. A reconstruction of a typical SC lesion (animal SC3) is shown in Fig. 1. The lesions removed most of the SC bilaterally in all 6 rats, with some inevitable damage sustained posteriorly in the inferior colliculi (4 rats), anteriorly in the pretectal nuclei (3 rats), and dorsally in the cortex (all 6 rats). The cortex was damaged to a comparable extent in the control group; in addition there was very slight damage to the superficial SC in 2 animals (SH4 and SH5). In both groups the cortical damage was located almost exclusively in the medial area R S G of Zilles 19, although there was slight damage in some cases to the medial subiculum (CA1). The log-transformed running times were subjected to 3-way ANOVA, in which the factors were groups, sessions, and trials (training mean versus test). Main effects were found only for
295
. .'~
.~'
',.,/
[
';
~,
Fig. 1. A representatwe midbrain lesion (SC3). The extent of the ablation is indicated on standard cross-sections taken from the KOnig and Klippel 7 atlas.
trials ( F = 6 9 . 7 3 , d f = 1.10, P < 0 . 0 0 0 1 ) and sessions ( F = 7.87, d f = 3.30, P < 0 . 0 0 1 ) , the groups not differing overall ( F > 1). The trials effect reveals a substantial disruption of running by the tone in both groups. As shown in Fig. 2, the sessions effect resolved into the interaction with trials (F = 8.11, df = 3.30, P < 0.001), reflecting a
HAM
15
SC LESION
50 2o~ C ~OZ --4
F---.lo Z 'E) e~o.5
clear habituation effect to the tones over the 4 sessions. The lack of a significant groups by trials interaction (P > 0.10) provided no evidence for a differential effect of the tones on the running speeds of the 2 groups. Both the interaction between groups and sessions ( F = 3.13, df = 3.30, P < 0.05) and the 3-way interaction
100
q o
2
3
4 TEST SESSIONS
Fig. 2. Running times recorded in the 4 auditory test sessions: means and standard errors for the 6 rats in each group. The times for the standard training trials (squares) are based on the harmonic mean for each session, and are given along with the times for the auditory 'distraction' trials (circles).
Freezeor Headturn retreat (n.s.) (P' ~ =.oo2) ~T~
Long run times
SH
SH
n.si
5o
SC
SH
SC
SC
Fig. 3. Behavioural reactions made to the auditory distractors: means and standard errors, calculated across the 6 rats in each group.
296
( F = 3 . 1 8 , d f = 3.30, P < 0 . 0 5 ) were however marginally significant, presumably reflecting a slightly different habituation rate to the tones in the 2 groups. Behavioural reactions to the tones were categorized non-exclusively as freezing, orienting (head-turn), and retreating (into the tunnel). As Fig. 3 shows, the incidence of freezing and retreating was not dissimilar in the 2 groups, and paralleled the occurrence of long running times (i.e. those outside the range of training trial latencies for that session). However, there was a clear difference between the 2 groups in the frequency of orienting reactions (Mann-Whitney test: U = 0, P < 0.001). It is clear that the rats of both groups detected the tones, since their running was disrupted by them to a similar extent. Consequently the failure of the SC-lesioned rats to orient to the tones cannot be attributed to a sensory loss. In the auditory modality, therefore, the SC clearly does not play a purely sensory role, but does seem (in rats: there may be a difference in cats TM) to be crucially involved in the mediation of overt orienting acts. This conclusion tends to strengthen the similar conclusion reached for the visual modality elsewhere TM. Precisely what role the SC plays in the orienting process is unclear: it could be that its crucial contribution is in localizing the auditory stimulus ~5 rather than in organizing the motor act. However, it should be noted that covert orienting, i.e. such attentional realignment as may be a prerequisite for any adaptive response to an external stimulus, seems not to have been impaired by the SC lesions; freezing and fleeing are entirely appropriate responses in our test setting, and these were not significantly impaired. For auditory stimuli, at least, it therefore seems that such non-orienting responses to novel stimuli can be mediated by other structures. REFERENCES 1 Albano, J.E., Mishkin, M., Westbrook, L.E. and Wurtz, R.H., Visuomotor deficits following ablation of monkey superior colliculus, J. Neurophysiol., 48 (1982) 338-350.
2 Dean, P, and Redgrave, P., The superior colliculus and visual neglect in rat and hamster. I. Bebavioural evidence, Brain Res. Rev., 8 (1984) 129-141. 3 Druga, R. and Syka, J., Projection from auditory structures to the superior colliculus in the rat, Neurosci. Lett., 45 (1984) 247-252. 4 Goodale, M.A. and Milner, A.D., Fractionating orientation behavior in the rodent. In D. Ingle, M.A. Goodale and R.J.W. Mansfield (Eds.), The Analysis of Visual Behavior, M.I.T. Press, Cambridge MA, 1982, pp. 267-299. 5 Goodale, M.A. and Murison, R.C.C., The effects of lesions of the superior colliculus on locomotor orientation and the orienting reflex in the rat, Brain Res., 88 (1975) 243-261. 6 Goodale, M.A., Foreman, N.P. and Milner, A.D., Visual orientation in the rat: a dissociation of the deficits following cortical and collicular lesions, Exp. Brain Res., 31 (1978) 445-457. 7 K0nig, J.F.R. and Klippel, R.A., The Rat Brain: A Stereotaxic Atlas of the Forebrain and Lower Parts of the Brain Stem, Williams and Wilkins, Baltimore MD, 1963. 8 Latto, R. and Cowey, A., Visual field defects after frontal eye field lesions in monkeys. Brain Res., 30 (1971) 1-24. 9 Linden, P. and Perry, V.H., Massive retinotectal projection in rats, Brain Res., 272 (1983) 145-149. 10 Martin, P.R., The projection of different retinal ganglion cell classes to the dorsal lateral geniculate nucleus in the hooded rat, Exp. Brain Res., 62 (1986) 77-88. 11 Midgley, G.C., Wilkie, D.M. and Tees, R.C., Effects of superior colliculus lesions on rats' orienting and detection of neglected visual cues, Behav. Neurosci., 102 (1988) 93-100. 12 Milner, A.D., Lines, C.R. and Migdal, B., Visual orientation and detection following lesions of the superior colliculus in rats, Exp. Brain Res., 56 (1984) 106-114. 13 Overton, P., Dean, P. and Redgrave, P., Detection of visual stimuli in far periphery by rats: possible role of superior colliculus, Exp. Brain Res., 59 (1985) 559-569. 14 Peck, C.K., Visual-auditory interactions in cat superior colliculus: their role in the control of gaze, Brain Res., 420 (1987) 162-166. 15 Schneider, G.E., Two visual systems, Science, 163 (1969) 895-902. 16 Sprague, J.M., The superior colliculus and pretectum in visual behavior, Invest. Ophthalmol., 11 (1972) 473-482. 17 Stein, B.E., Multimodal representation in the superior colliculus and optic tectum. In H. Vanegas (Ed.) Comparative Neurology of the Optic Tectum, Plenum, New York, 1984, pp. 819-841. 18 Thompson, G.C. and Masterton, R.B., Brainstem auditory pathways involved in reflexive head orientation to sound, J. Neurophysiol., 41, (1978) 1183-1202. 19 Zilles, K., The Cortex of the Rat, A Stereotaxic Atlas, Springer, New York, 1985.