Methodological considerations
Both the limitations and the strengths of this study concern the use of the magnetic search coil. The technique is restrictive for measuring pinna movements because (1) the structure moves in three dimensions, whereas our coil system measures movements around two axes only; and (2) the position of the coil on the pinna places it outside of the linear range of the system. On the other hand, with the system interfaced to a computer that allows fast sampling rates, pinna movements can be recorded with a time resolution not available with conventional video.
Coil calibration
As described in Materials and Methods, the magnetic search coil system is optimal when the coil is positioned in the coronal plane. Anatomical considerations, however, prevent the pinna coils from being implanted in that position. Therefore, we took advantage of the cat's habit of orienting the pinnae in a standard position while fixating an LED at the primary position and made our calibrations about that position. Such a procedure is essential for proper calibration. Previous measurements of cat pinna movements using the search coil technique by Hartline et al. (1995)
have not mentioned any calibration procedure so it is difficult to determine how they converted the voltage output of the coil system to degrees.
Pinna movements and two-dimensional movement recordings
The limitations of the calibration procedure, coupled with the uncertainty along which axis the pinna is moving, limit our interpretation of the measurements to relative changes in pinna position along the yaw and pitch axes. The simultaneous recordings of pinna movements with the magnetic search coil and videotape indicate that the main aspects of the movements are nevertheless recorded.
On the other hand, we are confident of our measurements of the timing of pinna movements. In this case, the actual position of the coil, not quite in the coronal plane, worked to our advantage, because rolling (lateral) movements of the pinna also produce movement components of yaw and pitch, which we can detect. Thus it is unlikely that we missed any pinna movements, although we cannot claim to determine their precise type.
Pinna movements during sound localization
The primary goal of this study was to characterize the behavior of the cat's pinna during sound localization. When the cat anticipated that the start of a trial was imminent, it looked toward the center and moved its pinnae to a ready position. A similar behavior has been reported by May and Huang (1996) in the conditioned head-free cat before the presentation of a target and by Heffner and Heffner (1982) in an elephant trained in a left-right discrimination task. Just before starting a trial, the elephant extended its pinnae perpendicularly to its head, to return them to their resting position while executing the response with its trunk. Significantly, this pinna behavior was not observed during threshold experiments conducted before and after the discrimination experiment, suggesting that it was specific to the task that required a localization judgment.
The extent to which the behavior of the cats of May and Huang (1996) and the elephant of Heffner and Heffner (1982) is analogous to the behavior of our cat's pinnae is debatable given the differences between the species and experimental paradigms, but the similarities are intriguing. It appears as if both species, as they prepared to localize sound, pulled their pinnae to a position that provided some acoustical advantage. Bringing the pinnae to a standard position when certain of having to localize the source of a sound could be a simplifying strategy that could facilitate localization (Young et al., 1996).
The question, therefore, arises as to whether a standard pinna position is required for accurate localization. Our sound localization data show that cats are able to localize acoustic targets starting from different fixation positions (Populin, 1996; Populin and Yin, 1997b) that are associated with different pinna positions, thus indicating that a standard pinna position is not required for accurate localization. Furthermore, the amplitude of pinna movements in our data range up to ~20°, which is within the range of different ear positions studied by Young et al. (1996). Therefore, we would expect that our cats experienced similar changes in acoustic input from stationary sources as illustrated in their study.
Neural mechanisms of pinna control
Pinna movements to auditory targets are stereotyped and consistent, goal-oriented, and have shorter latencies than to corresponding visual targets. They consist of two parts: a short-latency component time-locked to the onset of the sound and a second long-latency component that is highly correlated with the eye movement and may be part of the animal's general orientation behavior (Schaefer, 1970; Stein and Clamann, 1981; Hartline et al., 1995).
The distinct characteristics of each component of pinna movement suggest that they may be controlled separately. The close association between eye and pinna movements to visual targets is consistent with electrical stimulation of the SC, which evokes coordinated movements of the eyes, pinna, and whiskers (Stein and Clamann, 1981). These movements could be mediated by the tectoreticular-facial pathway or the tectoparalemniscal-facial pathways (May et al., 1990). The paralemniscal area, in the lateral midbrain tegmentum of the cat (Henkel and Edwards, 1978; Henkel, 1981), supplies a large and elaborate network of monosynaptic excitatory and inhibitory inputs to the medial aspect of the facial nucleus (May et al., 1990), where the motoneurons that innervate the muscles of the pinna are located (Kume et al., 1978; Populin and Yin, 1995).
The role of the SC in the control of the short-latency component described above is not as clear, however. The average latency with which the right pinna begins to move in response to acoustic stimuli presented on the frontal hemifield (Fig. 7) is 23.5 msec. This time seems too short to include the intermediate and deep SC, the units of which respond to acoustic stimuli with an average first spike latency of 19 msec in the same preparation performing the same sensory probe task (Populin and Yin, 1997b). Longer auditory SC latencies have also been reported in the behaving cat (Peck et al., 1995) and monkey (Jay and Sparks, 1987) (median, 50 msec; mean, 44.8 msec, respectively). Latency measurements of electrically evoked pinna movements, which could shed some light onto this issue, are not reported in the literature.
If the SC were not involved in the generation of the short-latency component of pinna movements, then what pathways could underlie this behavior? The goal-oriented nature of the short-latency component suggests that the paralemniscal zone may be involved. Auditory inputs to this area seem to be limited to the nucleus sagulum (Henkel, 1981), which is considered part of the auditory system but has not been studied physiologically. Alternatively, it is possible that auditory inputs reaching the medial aspects of the facial nucleus, bypassing the paralemniscal zone, could drive these movements. Pinna movement-related activity has been demonstrated in units in the pontomedullary reticular formation of the cat (Siegel et al., 1980). Stapedius motoneurons are located near the facial nucleus and receive direct inputs from the medial superior olive (Borg, 1973; Joseph et al., 1985). Thus auditory information does reach the vicinity of the facial nucleus, but the existence of the required synaptic contacts to complete the short-latency pinna movement circuit remains to be demonstrated.
Summary and conclusions
The results of this study show that cat pinna movements during sound localization consist of a short-latency component, time-locked to the onset of the stimulus, and a second component that accompanies the eye movement to the target. The consistency of the behaviors observed and the changes in acoustics that can result from them (Phillips et al., 1982; Musicant et al., 1990; Rice et al., 1992; Young et al., 1996) raise the question of what the cat accomplishes by moving its pinna. The two different types of pinna movements observed suggest that various roles could be fulfilled. With the short-latency component the cat could (1) obtain multiple samples of an acoustic object within a short period, which could help in localization (Thurlow and Runge, 1967), and (2) separate the spectrum of a sound source from the HRTF (Young et al., 1996). On the other hand, the larger pinna movements observed during an orientation response could help improve signal-to-noise ratio by focusing the acoustic axis of the pinna on a particular area of space (Phillips et al., 1982).
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