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Sound localization in cats and humans relies on head-centered acoustic cues. Studies have shown that humans are able to localize sounds during rapid head movements that are directed toward the target or other objects of interest. We studied whether cats are able to utilize similar dynamic acoustic cues to localize acoustic targets delivered during rapid eye-head gaze shifts. We trained cats with visual-auditory two-step tasks in which we presented a brief sound burst during saccadic eye-head gaze shifts toward a prior visual target. No consistent or significant differences in accuracy or precision were found between this dynamic task (2-step saccade) and the comparable static task (single saccade when the head is stable) in either horizontal or vertical direction. Cats appear to be able to process dynamic auditory cues and execute complex motor adjustments to accurately localize auditory targets during rapid eye-head gaze shifts., (Copyright © 2015 the American Physiological Society.)

The Franssen Effect (FE) is a striking auditory illusion previously demonstrated only in humans. To elicit the FE, subjects are presented with two spatially-separated sounds; one a transient tone with an abrupt onset and immediate ramped offset and the other a sustained tone of the same frequency with a ramped onset which remains on for several hundred ms. The FE illusion occurs when listeners localize the tones at the location of the transient signal, even though that sound has ended and the sustained one is still present. The FE illusion occurs most readily in reverberant environments and with pure tones of approximately 1-2.5 kHz in humans, conditions where sound localization is difficult in humans. Here, we demonstrate this illusion in domestic cats using, for the first time, localization procedures. Previous studies in humans employed discrimination procedures, making it difficult to link the FE to sound localization mechanisms. The frequencies for eliciting the FE in cats were higher than in humans, corresponding to frequencies where cats have difficulty localizing pure tones. These findings strengthen the hypothesis that difficulty in accurately localizing sounds is the basis for the FE.

Using the magnetic search coil technique to measure eye and ear movements, we trained cats by operant conditioning to look in the direction of light and sound sources with their heads fixed. Cats were able to localize noise bursts, single clicks, or click trains presented from sources located on the horizontal and vertical meridians within their oculomotor range. Saccades to auditory targets were less accurate and more variable than saccades to visual targets at the same spatial positions. Localization accuracy of single clicks was diminished compared with the long-duration stimuli presented from the same sources. Control experiments with novel auditory targets, never associated with visual targets, demonstrated that the cats localized the sound sources using acoustic cues and not from memory. The role of spectral features imposed by the pinna for vertical sound localization was shown by the breakdown in localization of narrow-band (one-sixth of an octave) noise bursts presented from sources along the midsagittal plane. In addition, we show that cats experience summing localization, an illusion associated with the precedence effect. Pairs of clicks presented from speakers at (+/-18 degrees,0 degrees ) with interclick delays of +/-300 microsec were perceived by the cat as originating from phantom sources extending from the midline to approximately +/-10 degrees.

Bushy cells in the anteroventral cochlear nucleus (AVCN) receive their principal excitatory input from the auditory nerve and are the primary source of excitatory input to more centrally located brainstem auditory nuclei. Despite this pivotal position in the auditory pathway, details of the basic physiological information being carried by axons of these cells and their projections to more central auditory nuclei have not been fully explored. In an attempt to clarify these details, we have physiologically characterized and anatomically labeled individual axons of the spherical bushy cell (SBC) class of the cat AVCN. The characteristic frequencies (CFs) of our injected SBC population are low, all less than 12 kHz and primarily (83%) less than 3 kHz, while their spontaneous activity is comparatively high (mean of 59 spikes/sec). In response to short tone bursts at CF, low CF (< 1 kHz) SBC units can phase-lock better than auditory nerve fibers. SBCs with CFs above 1 kHz have primary-like responses at all stimulus levels and can show robust phase-locking to an off-CF, 500 Hz tone. When compared with our previously reported population of labeled globular bushy cells (GBC; Smith et al., 1991, J. Comp. Neurol. 304:387-407), some similarities and differences are apparent in both physiological response properties and axonal projection pattern. GBCs show no low frequency bias in CFs, have lower spontaneous rates, and the high CF units exhibit a primary-like-with-notch response at high stimulus levels as a consequence of a very well timed onset component. Low CF, GBC short tone responses are indistinguishable from those of SBCs. Anatomically, the axons of SBCs cross the midline in the dorsal component of the trapezoid body and typically innervate the medial superior olive (MSO) on both sides, the ipsilateral lateral superior olive (LSO), and the contralateral ventral nucleus of the lateral lemniscus (VNLL). The projections to the contralateral, but not the ipsilateral MSO, show a rostral to caudal delay line configuration, similar to the scheme first proposed by Jeffress (1948, J. Comp. Psychol. 41:35-39). The form of this delay line is consistent with the topographic map of interaural time delays reported by Yin and Chan (1990, J. Neurophysiol. 64:465-488). Projections to the ipsilateral LSO often take an indirect route. In contrast, GBC axons travel in the ventral component of the trapezoid body, never innervate the MSO, rarely innervate the ipsilateral LSO, and always innervate the contralateral medial nucleus of the trapezoid body. The terminal specializations of both SBC and GBC axons contain round vesicles.

We made intraaxonal recordings from 30 individual globular bushy cell axons in the trapezoid body of the cat using HRP-filled glass microelectrodes. With subsequent HRP injection, we determined their axonal projection patterns. For cells with characteristic frequencies (CFs) above 3 kHz, short-tone peristimulus time histograms (PSTHs) at CF were typically primarylike at low tone intensities and primarylike with notch (PLN) or onset with low sustained activity (OL) at higher stimulus levels. Cells with CFs between 1 and 3 kHz showed the same response features with the spikes in the sustained region of the response phase-locked to the stimulus tone. Cells with CFs below 1 kHz showed phase-locked PSTHs with exceptionally high levels of synchrony compared to eighth nerve fibers with comparable CFs. This exceptional phase-locking was also noted when cells with CFs of 1-3 kHz were presented with tones below 1 kHz. Although the globular bushy cell axons were not completely filled from the soma of origin to terminal fields in the contralateral brainstem, a number of consistent anatomical features were distinguished in the population. All but one of the myelinated axons crossed the midline in the middle, large fiber component of the trapezoid body. Ipsilaterally, the axon always gave off from one to four collateral branches whose major targets were the posterior periolivary nucleus (PPO) and the lateral nucleus of the trapezoid body (LNTB). Minor termination sites for ipsilateral collateral branches were the dorsolateral periolivary nucleus (DLPO) and the lateral superior olive (LSO). Contralaterally the axon gave rise to one or two calyces of Held in the medial nucleus of the trapezoid body (MNTB). Three other major collateral branches arose from the contralateral axon and innervated a consistent set of areas. One headed caudally to innervate an area just ventromedial to the facial nucleus. Another followed the sixth nerve dorsally to innervate the dorsomedial periolivary nucleus (DMPO). A third collateral headed rostrally toward the ventral nucleus of the lateral lemniscus (VNLL), giving off occasional small sidebranches. Although each injected axon gave rise to a collateral that innervated the MNTB, it did not necessarily give rise to all three of the other collateral branches.

The dendritic and axonal morphology of neurons in the inferior colliculus of the cat was investigated after intracellular injection of HRP, in vivo. All injected axons gave off local collaterals, and most showed a widespread distribution and lacked a specific orientation. In contrast, the dendrites of injected neurons were distinguished by their degree of orientation and the direction of the longest axis of orientation. Dendrites showed a high, moderate, or low degree of orientation. Most highly oriented cells had their longest axis in the rostrocaudal direction with fewer in the mediolateral direction. In the central nucleus, only the rostrocaudally oriented cells correspond to the disc-shaped cells identified in Golgi preparations. Unlike most cells in our sample, the two cells that were disc-shaped had axons that were parallel to the orientation of the dendritic tree. In the dorsal cortex, rostrocaudally oriented cells also were found, but they had unoriented axons. In both the central nucleus and dorsal cortex, cells with a mediolateral axis of orientation or no specific orientation correspond to stellate cells and had axons with widespread local collaterals. These results suggest that an extensive network of local axon collaterals may contribute to neural processing within the inferior colliculus. In the central nucleus, local axons may establish connections within or across the fibrodendritic laminae. In the dorsal cortex, the local and afferent axons may form a complex reticular network. Finally, some injected cells had axons terminating locally and also entering the brachium of the inferior colliculus. This suggests that cells in the inferior colliculus may function as both interneurons and projection neurons.

Detailed, quantitative studies were made of the interaural phase sensitivity of 197 neurons with low best frequency in the inferior colliculus (IC) of the barbiturate-anesthetized cat. We analyzed the responses of single cells to interaural delays in which tone bursts were delivered to the two ears via sealed earphones and the onset of the tone to one ear with respect to the other was varied. For most (80%) cells the discharge rate is a cyclic function of interaural delay at a period corresponding to that of the stimulating frequency. The cyclic nature of the interaural delay curve indicates that these cells are sensitive to the interaural phase difference. These cells are distributed throughout the low-frequency zone of the IC, but they are less numerous in the medial and caudal zones. Cells with a wide variety of response patterns will exhibit interaural phase sensitivities at stimulating frequencies up to 3,100 Hz, although above 2,500 Hz the number of such cells decrease markedly. Using dichotic stimuli we could study the cell's sensitivity to the onset delay and interaural phase independently. The large majority of IC cells respond only to changes in interaural phase, with no sensitivity to the onset delay. However, a small number (7%) of cells exhibit a sensitivity to the onset delay as well as to the interaural phase disparity, and most of these cells show an onset response. The effects of changing the stimulus intensity equally to both ears or of changing the interaural intensity difference on the mean interaural phase were studied. While some neurons are not affected by level changes, others exhibit systematic phase shifts for both average and interaural intensity variations, and there is a continuous distribution of sensitivities between these extremes. A few cells also showed systematic changes in the shape of the interaural delay curves as a function of interaural intensity difference, especially at very long delays. These shifts can be interpreted as a form of time-intensity trading. A few cells demonstrated orderly changes in the interaural delay curve as the repetition rate of the stimulus was varied. Some of these changes are consonant with an inhibitory effect that occurs at stimulus offset. The responses of the neurons show a strong bias for stimuli that would originate from he contralateral sound field; 77% of the responses display mean interaural phase angles that are less than 0.5 of a cycle, which are delays to the ipsilateral tone.(ABSTRACT TRUNCATED AT 400 WORDS)

We used the binaural beat stimulus to study the interaural phase sensitivity of inferior colliculus (IC) neurons in the cat. The binaural beat, produced by delivering tones of slightly different frequencies to the two ears, generates continuous and graded changes in interaural phase. Over 90% of the cells that exhibit a sensitivity to changes in the interaural delay also show a sensitivity to interaural phase disparities with the binaural beat. Cells respond with a burst of impulses with each complete cycle of the beat frequency. The period histogram obtained by binning the poststimulus time histogram on the beat frequency gives a measure of the interaural phase sensitivity of the cell. In general, there is good correspondence in the shapes of the period histograms generated from binaural beats and the interaural phase curves derived from interaural delays and in the mean interaural phase angle calculated from them. The magnitude of the beat frequency determines the rate of change of interaural phase and the sign determines the direction of phase change. While most cells respond in a phase-locked manner up to beat frequencies of 10 Hz, there are some cells tht will phase lock up to 80 Hz. Beat frequency and mean interaural phase angle are linearly related for most cells. Most cells respond equally in the two directions of phase change and with different rates of change, at least up to 10 Hz. However, some IC cells exhibit marked sensitivity to the speed of phase change, either responding more vigorously at low beat frequencies or at high beat frequencies. In addition, other cells demonstrate a clear directional sensitivity. The cells that show sensitivity to the direction and speed of phase changes would be expected to demonstrate a sensitivity to moving sound sources in the free field. Changes in the mean interaural phase of the binaural beat period histograms are used to determine the effects of changes in average and interaural intensity on the phase sensitivity of the cells. The effects of both forms of intensity variation are continuously distributed. The binaural beat offers a number of advantages for studying the interaural phase sensitivity of binaural cells. The dynamic characteristics of the interaural phase can be varied so that the speed and direction of phase change are under direct control. The data can be obtained in a much more efficient manner, as the binaural beat is about 10 times faster in terms of data collection than the interaural delay.

The effects of changing stimulus frequency on the interaural phase sensitivity of neurons in the inferior colliculus (IC) were studied in barbiturate-anesthetized cats in order to reexamine the issue of characteristic delay (CD). Since the results obtained with the interaural delay and binaural beat stimuli are similar, we used the averaged interaural delay curves and binaural beat period histograms as comparable expressions of a neuron's interaural phase sensitivity. When the averaged interaural delay curves at different frequencies are plotted on a common time axis, for some cells the resulting superimposed delay curves show peaks or troughs that coincide at some CD. For most cells, though, this method of detecting a CD by visual inspection yields ambiguous and uncertain results. Composite curves, computed from the average of all the normalized superimposed delay curves, are also not helpful for showing CD. In order to provide a more objective means of analyzing the data, we plotted the mean interaural phase versus the stimulating frequency and computed the linear regression line, using the mean square error as a measure of linearity. The slope of the regression line is the CD for the neuron, and the phase intercept is referred to as the characteristic phase (CP). Cells that display a CD at the peak discharge have a CP = 0.0 cycles, while those that show a CD at the minimum discharge have a CP = 0.5. Cells that exhibit a CP at any value other than 0.0, 0.5, or 1.0 will have a CD at some relative amplitude other than the peak or trough. For cells that exhibit a CD at the peak or trough, results of the analysis procedure using the phase-frequency plot correspond to those obtained from visual inspection. For cells that do not show a common peak or trough, the analysis procedure not only specifies the location of the CD but also provides a statistical criterion of the linearity. From this analysis about 60% of the runs were identified as satisfying the criteria for CD at the P less than 0.005 level and 71% of these CDs are between +/- 300 micros. Most CD cells do not have the CD at the peak or trough of the response. Our results differ from those found in previous studies but they are in essential agreement with the original concept put forth by Rose et al. (31). Some cels exhibit little change in the CD or CP with variations in intensity, while others display marked systematic shifts in both CD and CP. In general, the peaks and troughs of the composite curves show less variability with intensity than the CD.(ABSTRACT TRUNCATED AT 400 WORDS)