Pinna movement data from six different cats were collected while they engaged in sound localization tasks in which they were free to move their ears (Populin and Yin, 1998
). In all figures the 0° on the ordinate scale was arbitrarily set to approximate the position of the pinna at the time the cat fixated the LED at the primary position for that recording session. Thus, the scales measure changes in pinna position rather than absolute position.
Pinna movements to visual targets from two-dimensional video images
We begin with videotaped images of a cat's pinnae to provide a qualitative reference for the pinna movements measured by the search coil method. Shown in Figure 2 are posterior views of Cat08's head illustrating the position of the pinnae during various phases of a downward visual saccade. These images were selected from a video recording of an experimental session. The camera was positioned behind the cat, slightly to the right of the sagittal plane, and above the interaural axis. The gray structure labeled hh in Figure 2 is the head holder, and the circular structure labeled cr is a calibrating ring, both of which are stationary in these images (see Materials and Methods).
To better track pinna position, triangular markers were attached to the tip and medial and lateral edges of each pinna, and a white reference dot was painted on the skin at the center of the implanted coil. Changes in pinna position in these figures (Fig. 1, bottom) are described as changes in yaw (left or right movements around the vertical axis), pitch (up or down movements around the horizontal axis), and roll (movements around the longitudinal axis of the cat).
During a typical behavioral run there was a fixed intertrial interval (5-10 sec) during which the cat was usually licking the reward from the previous trial. When the cat anticipated that the next trial was about to begin, it usually looked near the primary position and pulled its pinnae into a ready position. The Spon image in Figure 2 was taken during this period, which we reserve for spontaneous activity in physiological recordings. The second image (Fig. 2, Fix) was taken while the cat was fixating the LED at the primary position, seen in the figure as a red dot. The third image (Fig. 2, Down) was taken after the cat had made a downward saccade to the LED at (0°,
23°). These images were selected from frames corresponding to each part of the task after the pinna had settled to a new position.
To show the relative movements of the pinna during these three sequences, we superimposed the three images in Figure 2, Composite. This figure was generated by decomposing each of the three images into its red, green, and blue components using Corel Photo Paint, keeping only one of the color components of each image (blue for Spon, red for Fix, and green for Down) and recombining them into a single image. In this way, the parts of the figure that remain stationary in all three images appear in their original color, and those that move appear in the color of the retained image or some combination of colors. The relative changes in pinna position can thus be seen in a single composite image.
Using the blue portion of the image from the spontaneous period as a reference, we will track the changes in pinna position throughout the sequence (Fig. 2). Notice that the dot marking the center of the coil is below the calibrating ring in the Spon period and is seen as a faint blue dot in the Composite image. In the Fix period the right pinna rolled laterally, as can be seen by the triangular markers on the pinna, and pitched slightly downward, as indicated by the shift in the position of the reference dot, which at this point is inside the lower edge of the calibrating ring. The left pinna also rolled laterally, although the details of its movement are obscured by the head holder.
In the last part of the task an LED was presented below the horizontal plane at (0°,23°). The right pinna rolled further to the right and pitched downward, as indicated by the reference dot at the center of the calibrating ring and the almost complete disappearance of the medial triangular marker. The change in position of the left pinna appears to mirror that of the right pinna.
Figure 3 shows composite images analogous to the one in Figure 2 for the other three targets with the same color convention. In Figure 3, top (for a target to the right at 18°,0°) the fixation LED is shown in red, whereas the target LED in green is also visible to the right. As in Figure 2, the right pinna rolled laterally between the spontaneous (blue) and fixation (red) periods. The target LED evoked an outward (yaw) movement to the right, as indicated by the green triangular marker in the medial aspect of the right pinna that has almost disappeared from view, the lateral marker that is more visible, and the medial movement of the reference dot (red to green) inside the calibrating ring. On the other hand, there was little change in the position of the left pinna throughout the entire trial, because the triangular markers are mostly white.
The initial part of the sequence for the
Left target (
18°,0°) (
Fig. 3) started with both pinnae rolled more laterally than in the previous case (
blue image). The red image, taken during the fixation period, shows that the pinnae rolled slightly medially. The magnitude of the displacement is similar in both pinnae. The visual target presented 18° to the left evoked different movements on the two sides; the contralateral right pinna rolled slightly to the left between the fixation and saccade period, as suggested by the almost superimposed red and green markers (which together appear yellow), whereas the left pinna rolled further medially.
The Up target sequence (Fig. 3) shows that the two pinnae moved asymmetrically, although the target was on the midline at 18° above the horizontal. The position of the right pinna changed very little between the spontaneous and fixation periods, as seen by the overlap of the triangular markers. In the last part of the sequence, after the cat saccaded to the target, the lower position of the green reference dot indicates that the pinna pitched upward in the direction of the target. The small change in the position of the triangular markers, compared with the change in the position of the reference dot, indicates that the main rotation was accompanied by displacements that maintained the most distal part of the pinna in a relatively constant position as it pitched upward. The left pinna also showed little movement between the spontaneous and fixation stages but a more pronounced change in pitch in the upward direction of the distal end of the pinna, judging by the amount of downward displacement of the green markers.
These series of images illustrate (1) that the pinna moved in the general direction of the target; (2) that the movements of both pinnae were not necessarily symmetrical for horizontal or vertical targets; and (3) that in some instances, the pinna response was the result of combined complex rotations and displacements.
Magnetic search coil recordings of pinna movements to visual targets
Video recording of pinna movements (Figs. 2, 3) was done for illustrative purposes only; for routine recordings of pinna movements we used the magnetic search coil. Our coil system can only measure yaw (horizontal) and pitch (vertical) changes in coil position; thus it has limitations for the study of pinna movements because the structure moves in a complex manner in three-dimensional space. The data in Figure 4, which were recorded during the videotaping session that produced the images shown in Figures 2 and 3, demonstrate that the two-dimensional search coil technique can provide a first approximation of the magnitude of pinna movements and precise information about their timing. The coil from which these recordings were obtained was implanted in Cat08's right pinna using the caudal approach (Fig. 1, left).
In all cases visual saccades started from a fixation LED at the primary position (0°,0°) to targets located at the four positions indicated above. The onset of the fixation LED usually occurred between 1200 and 900 msec, depending on how long it took the cat to enter the fixation window. There was more variability in pinna position during the spontaneous period before fixation onset than during the fixation period (between approximately 900 and 0 msec), indicating that the pinna adopted a more consistent position during the fixation of the LED at the primary position. This reduction in the spread is present in most traces. Notice that the pinnae did not assume random positions or seem to show periodic scanning movements.
The appearance of the visual targets evoked well defined consistent responses of the pinna in the direction of the sources. The amplitude of these movements did not match the eccentricity of the targets that evoked them: targets located 18° or 23° away from the primary position yielded pinna movements of ~10° (Fig. 4). Movements had both vertical and horizontal components, with the larger ones taking place along the axis on which the target was located. Finally, the movements were not symmetrical; movements of the right pinna were larger for the ipsilateral and upward targets than for the contralateral and downward targets, respectively. It is important to point out, however, that the movements measured by the coil depend on the placement of the coil on the pinna. For example, there are marked differences between these movements and those shown in Figure 5. Of course, these differences could also be attributable to differences in pinna movements between cats.
Pinna movements to auditory and visual targets
The pinna movement data shown in the previous figures were recorded during the course of standard saccade trials to visual stimuli presented within the cat's oculomotor range. In this section we compare pinna movements with both visual and auditory targets.
Plotted in Figure 5 are Cat09's right pinna movements recorded during standard saccade trials with a coil implanted in the caudal aspect of the structure (Fig. 1, left). The pinna movements that followed the onset of the visual stimulus were similar to those in Cat08 (Fig. 4); the largest component of movement was along the axis of the target and there was a similar asymmetry.
The broadband noise stimulus also evoked pinna movements in the direction of the sources (Fig. 5). Although these movements resemble those with equivalent visual targets, i.e., they are goal-directed and somewhat asymmetric, there are some marked differences between the pinna movements to visual and auditory targets. The major difference is that acoustically evoked movements have shorter latencies than those evoked by visual targets. The mean latency of the pinna movements to the visual target at (18°,0°) was 242.8 msec (SD, ±62.6 msec), whereas the mean to the auditory target at the same position was 34.6 msec (SD, ±15 msec). The mean latency of saccadic eye movements to the same visual target (234.7 msec; SD, ±33 msec) suggests that the eye and ear begin to move together and that pinna movements might be a part of a general orienting reflex.
We correlated the shortest pinna latency with eye movement latency in standard saccade trials to auditory and visual targets located on the ipsilateral side of the pinna at an eccentricity of 18°. Such data, from five different cats (Cat06, Cat09, Cat10, Cat11, and Cat14), are plotted in Figure 6. The mean latency of pinna movements to auditory targets is significantly shorter than the mean latency of pinna movements to visual targets (p The slope of the regression line for auditory data (0.03; r = 0.16) indicates that there is no relationship between the onset of pinna (26.5 msec; SD, 15.2 msec) and eye (265.6 msec; SD, 77.8 msec) movements for these targets. On the other hand the slope of the line for the visual data (0.75; r = 0.68) indicates that the onset of eye (mean, 233.8 msec; SD, 87.2 msec) and pinna movements (262.8 msec; SD, 96.2 msec) are related.
Pinna movements to delayed saccade and sensory probe tasks
The results of Figure 6 suggest that pinna movements to auditory targets are coupled to the onset of the target, not to the eye movement. To confirm this observation, we also studied pinna movements using the delayed saccade task in which the eye movements are temporally dissociated from the target onset (Fig. 7). This allowed us to separate pinna movements that resulted from the presentation of a stimulus from those associated with the animal's orientation. The first part of the task, the fixation period before target presentation (time and auditory conditions. After the eyes acquired the fixation LED at (0°,0°), the pinna remained in a stationary position that was generally consistent from trial to trial. During the delay period the behavior of the eyes was similar in both visual and auditory conditions; they remained on the fixation LED, but the pinna behaved differently. In visual trials the pinna remained stationary during the entire 500 msec period in which the fixation light and the target overlapped and moved at about the same time the eyes started to move to the target after the fixation LED was turned off. In auditory trials the response of the pinna exhibited two components: one prominent and abrupt with very short latency (Fig. 7, filled arrows; mean, 21 msec; SE, ±2.2 msec) that was time-locked to target onset and another smaller and later at approximately the time of eye movement onset (open arrows).
The short-latency component was also revealed by the auditory sensory probe task, which required the cat to maintain fixation on an LED without an eye movement, thereby excluding the second component of the pinna response. To the cat the initial segments of delayed saccade (Fig. 7) and sensory probe (Fig. 8) trials are identical. Because eye movements to the target were not required, these sensory probe trials also enabled us to measure pinna movements to more eccentric targets, outside the cat's oculomotor range.
Figure 8 illustrates Cat14's pinna movements of both the left and right ears recorded with coils implanted with the caudal approach. The noise stimuli evoked prominent and consistent short-latency pinna movements that were largest for stimuli on the ipsilateral side. Note that the movements of the pinnae were graded as a function of speaker position, with the largest and smallest movements evoked by the most eccentric ipsilateral and contralateral probes, respectively. In these trials, the duration of the noise stimulus was 800 msec, and the reward was delivered 200 msec after the noise was turned off. Note that the large pinna movements to the most eccentric stimuli returned toward the central position after the offset of the noise.
We measured the latencies of pinna movements evoked by acoustic stimuli presented from different positions along the horizontal plane when the cat was fixating the LED at (0°,0°) and did not move its eyes (Fig. 8). Figure 9 includes results from Cat14's data shown in Figure 8 and from Cat11. Cat14's mean response latencies across all speaker positions were 24.5 msec (SD, ±9.7 msec; n = 176) for the left pinna and 23.4 msec (SD, ±11.1 msec; n = 166) for the right ear. The latencies were significantly longer for the most peripheral targets compared with the central one on both the ipsilateral and contralateral side, as evidenced by the lack of overlap of the confidence intervals in Figure 9.
Another characteristic of the short-latency component was its lack of habituation. In Cat06, the subject with the longest tenure in our studies, it was observed after >105 trials.
Pinna movements are goal-oriented
All cats that participated in our studies showed pinna movements in both visual and auditory trials that appeared to be goal-oriented. The data presented in Figures 2-6 show that the cats moved their pinnae purposely and consistently toward the stimulus. Furthermore, they seemed to be moving the ear to a particular position, regardless of the initial pinna position, as illustrated by the adjustments the cat made in some of the trials shown in Figure 5, in which the pinna was clearly in an anomalous position during the fixation period. In these trials the pinna was not in its usual position at the time the visual or auditory target came on, and the resulting pinna movement compensated for the unusual initial position, in some cases by moving in the opposite direction from the majority of the movements. Similar observations are found among the trials shown in Figure 8.
The consistent position of the pinna during the fixation period in the data shown in Figure 7 allowed us to compare the amplitude of the movements between the auditory and visual conditions. The mean amplitude of the pinna movements shown in Figure 7 to targets at (18°,0°) and (9°,0°) are plotted in Figure 10. The overlap of the confidence intervals suggests that the final pinna position in visual and auditory trials is similar, given a consistent starting position. Notice that in both cases the change in position is a weak function of target eccentricity.
Pinna movements to visual targets are not the result of training
Because our experimental design incorporates both auditory and visual trials (Populin and Yin, 1998), we were able to study the behavior of the pinna while the cat oriented to nonacoustic targets. Our findings confirm the observations of Joseph and Boussaud (1985), who reported that cat eye movements to visual targets were accompanied by electromyographic discharges in pinna muscles.
The consistency of the pinna movements to visual targets raised the possibility that they might be the result of some aspect of the training program used to teach cats to look at the location of sound sources (Populin and Yin, 1998). We examined the first trial of the first experimental session of three subjects (Cat09, Cat11, and Cat15), and in all cases the cats moved their pinnae in the direction of the visual target as they oriented.
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