Sound Localization In Mammals Research Articles

A Test of the Stereausis Hypothesis for Sound Localization in Mammals.

The relative arrival times of sounds at both ears constitute an important cue for localization of low-frequency sounds in the horizontal plane. The binaural neurons of the medial superior olive (MSO) act as coincidence detectors that fire when inputs from both ears arrive near simultaneously. Each principal neuron in the MSO is tuned to its own best interaural time difference (ITD), indicating the presence of an internal delay, a difference in the travel times from either ear to the MSO. According to the stereausis hypothesis, differences in wave propagation along the cochlea could provide the delays necessary for coincidence detection if the ipsilateral and contralateral inputs originated from different cochlear positions, with different frequency tuning. We therefore investigated the relation between interaural mismatches in frequency tuning and ITD tuning during in vivo loose-patch (juxtacellular) recordings from principal neurons of the MSO of anesthetized female gerbils. Cochlear delays can be bypassed by directly stimulating the auditory nerve; in agreement with the stereausis hypothesis, tuning for timing differences during bilateral electrical stimulation of the round windows differed markedly from ITD tuning in the same cells. Moreover, some neurons showed a frequency tuning mismatch that was sufficiently large to have a potential impact on ITD tuning. However, we did not find a correlation between frequency tuning mismatches and best ITDs. Our data thus suggest that axonal delays dominate ITD tuning.SIGNIFICANCE STATEMENT Neurons in the medial superior olive (MSO) play a unique role in sound localization because of their ability to compare the relative arrival time of low-frequency sounds at both ears. They fire maximally when the difference in sound arrival time exactly compensates for the internal delay: the difference in travel time from either ear to the MSO neuron. We tested whether differences in cochlear delay systematically contribute to the total travel time by comparing for individual MSO neurons the best difference in arrival times, as predicted from the frequency tuning for either ear, and the actual best difference. No systematic relation was observed, emphasizing the dominant contribution of axonal delays to the internal delay.

The natural history of sound localization in mammals--a story of neuronal inhibition.

Our concepts of sound localization in the vertebrate brain are widely based on the general assumption that both the ability to detect air-borne sounds and the neuronal processing are homologous in archosaurs (present day crocodiles and birds) and mammals. Yet studies repeatedly report conflicting results on the neuronal circuits and mechanisms, in particular the role of inhibition, as well as the coding strategies between avian and mammalian model systems. Here we argue that mammalian and avian phylogeny of spatial hearing is characterized by a convergent evolution of hearing air-borne sounds rather than by homology. In particular, the different evolutionary origins of tympanic ears and the different availability of binaural cues in early mammals and archosaurs imposed distinct constraints on the respective binaural processing mechanisms. The role of synaptic inhibition in generating binaural spatial sensitivity in mammals is highlighted, as it reveals a unifying principle of mammalian circuit design for encoding sound position. Together, we combine evolutionary, anatomical and physiological arguments for making a clear distinction between mammalian processing mechanisms and coding strategies and those of archosaurs. We emphasize that a consideration of the convergent nature of neuronal mechanisms will significantly increase the explanatory power of studies of spatial processing in both mammals and birds.

Stochastic Model Explains the Role of Excitation and Inhibition in Binaural Sound Localization in Mammals

Interaural time differences (ITDs), the differences of arrival time of the sound at the two ears, provide a major cue for low-frequency sound localization in the horizontal plane. The first nucleus involved in the computation of ITDs is the medial superior olive (MSO). We have modeled the neural circuit of the MSO using a stochastic description of spike timing. The inputs to the circuit are stochastic spike trains with a spike timing distribution described by a given probability density function (beta density). The outputs of the circuit reproduce the empirical firing rates found in experiment in response to the varying ITD. The outputs of the computational model are calculated numerically and these numerical simulations are also supported by analytical calculations. We formulate a simple hypothesis concerning how sound localization works in mammals. According to this hypothesis, there is no array of delay lines as in the Jeffress' model, but the inhibitory input is shifted in time as a whole. This is consistent with experimental observations in mammals.

Mechanisms of Sound Localization in Mammals

The ability to determine the location of a sound source is fundamental to hearing. However, auditory space is not represented in any systematic manner on the basilar membrane of the cochlea, the sensory surface of the receptor organ for hearing. Understanding the means by which sensitivity to spatial cues is computed in central neurons can therefore contribute to our understanding of the basic nature of complex neural representations. We review recent evidence concerning the nature of the neural representation of auditory space in the mammalian brain and elaborate on recent advances in the understanding of mammalian subcortical processing of auditory spatial cues that challenge the "textbook" version of sound localization, in particular brain mechanisms contributing to binaural hearing.

Effects of omni-directional noise-exposure during hearing onset and age on auditory spatial resolution in the Mongolian gerbil ( Meriones unguiculatus) — a behavioral approach

Inhibitory inputs to the binaural brainstem nuclei medial and lateral superior olives (MSO and LSO, respectively) are thought to be important for sound localization in mammals. Here, we investigate whether aged gerbils that typically exhibit degenerative changes in auditory nuclei providing inhibition to MSO and LSO show diminished localization ability. We also tested the localization ability in gerbils reared in omni-directional white noise during hearing onset, a treatment that affects the adjustment of inhibitory inputs to MSO neurons possibly resulting in weakened sensitivity to interaural time difference. Localization ability of both groups was compared to that of young gerbils raised under control conditions. Stimuli had a duration of 125 ms and were pure tones of 0.5, 1, 2, 4 and 8 kHz, 300-Hz-bands of noise centered at 0.5, 2 and 8 kHz or broad-band noise. Gerbils trained in a two-alternative-forced-choice procedure indicated if sounds were presented from the left or from the right by choosing the respective response compartment of a Y-shaped experimental setup. The minimum resolvable angle (MRA) was calculated as the minimum angle between two loudspeaker locations that a gerbil was able to discriminate. MRAs for aged gerbils were higher compared to controls, whereas MRAs of noise-reared gerbils did not differ from those of the control group. Results are discussed with respect to the progressive degeneration affecting the gerbil's auditory system, changes in the anatomical arrangement of inhibitory inputs on binaural neurons in the MSO, and hearing thresholds.

Proposed mechanisms for coincidence detection in the auditory brainstem

Sound localization in mammals uses two distinct neural circuits, one for low- and one for high-frequency bands. Recent experiments call for revision of the theory explaining how the direction of incoming sound is calculated. We propose such a revised theory. Our theory is based on probabilistic spiking and probabilistic delay of spikes from both sides. We have applied the mechanism originally proposed as an operation on spike trains resulting in multiplication of firing rates. We have adapted this mechanism for the case of synchronous spike trains. The mechanism has to detect spikes from both sides within a short time window. Therefore, in both circuits neurons act as coincidence detectors. In the excitatory low-frequency circuit we call the mechanism the excitatory coincidence detection, to distinguish it from the mechanism of the inhibitory coincidence detection in the high-frequency circuit. The times to first spike and gains of the two mechanisms are calculated. We show how the output gains of the mechanisms predict the dip within the human frequency sensitivity range. This dip has been described in human psychophysical experiments.

A neural code for low-frequency sound localization in mammals.

We report a systematic relationship between sound-frequency tuning and sensitivity to interaural time delays for neurons in the midbrain nucleus of the inferior colliculus; neurons with relatively low best frequencies (BFs) showed response peaks at long delays, whereas neurons with relatively high BFs showed response peaks at short delays. The consequence of this relationship is that the steepest region of the function relating discharge rate to interaural time delay (ITD) fell close to midline for all neurons irrespective of BF. These data provide support for a processing of the output of coincidence detectors subserving low-frequency sound localization in which the location of a sound source is determined by the activity in two broad, hemispheric spatial channels, rather than numerous channels tuned to discrete spatial positions.

Visual factors in sound localization in mammals.

The ability of mammals to localize sound varies widely among species. During the past decade, evidence has accumulated that this variation cannot be accounted for simply on the basis of the availability of the physical cues for locus. Evidence is presented that a major factor in sound localization is the need to direct the field of best vision to a sound source for further scrutiny. Thus, species with broad fields of best vision (such as visual streaks) require less accurate information regarding the location of a sound source than do species with very narrow fields of best vision (such as foveae). To support this suggestion, data are reported for the width of the field of best vision in the form of retinal ganglion cell isodensity contours for thirteen species of mammals. The possible contribution of other factors including binocular fields, visual acuity, and the degree to which a species is predatory in lifestyle, is also examined.

Physiological and anatomical studies relevant to considerations of sound localization in mammals

Recent studies of the basic organization and response properties of neurons of auditory nuclei and auditory cortical fields bear important implications for considerations of how sound localization behavior is a product of these systems. First, a series of largely parallel, functionally distinct projection subsystems have been identified. Some general conclusions as to their individual roles in auditory behavior can be drawn, given response properties of neurons and connections within. There are sheetlike subdivisions oriented orthogonally to isofrequency contours, in the central nucleus of the inferior colliculus, the ventral division of the MGB and in several auditory cortical fields. They are completely interconnected from level to level. In cortical fields and in the central nucleus, these subdivisions have been demonstrated to be response specific. Some would appear to be involved in specific aspects of sound localization, others not. Second, it now appears likely that low‐frequency pitch sensation is decoded within the medial superior olive, a nucleus long implicated in sound localization. The conjoint information processing accomplishments in these two psychoacoustic dimensions and some of its functional implications will be discussed. [Supported by NIH Grant NS‐10414.]

The Morphology of Auditory Neurons and Auditory Localization

The mammalian auditory system of the brain stem contains a number of classes of nerve cells the morphology of which may be relevant to the binaural localization of sounds. The axons of the acoustic nerve give rise to large synaptic endings (bulbs of Held) on the cell bodies of two types o[ nerve cells (types c and g) of the cochlear nucleus. The size of these endings suggests that they dominate the firing patterns of the postsynaptic cells, preserving in them the temporal characteristics of the activity in the acoustic nerve fibers. The medial superior olivary (mso) nucleus contains horizontally oriented bipolar nerve cells whose lateral dendrites probably receive synaptic endings from contralateral type c cells. Their bilateral innervation from cells that are synaptically dominated by the acoustic nerve fibers has suggested that the cells of the mso are of significance in the location of sounds. The medial nucleus of the trapezoid body contains nerve cells each of which is innervated by a single massive synaptic ending (chalice of Held) from large axons of the contralateral type g cells. This would appear to be a rapidly conducting system in which temporal characteristics of acoustic nerve activity may be preserved. The number of nerve cells in the major nuclei of the superior olivary complex varies across mammalian species. The mso varies from 0 (bats and dolphin) to 4200 (cat) nerve cells. The absence of this nucleus in the echolocating bats and dolphin shows that this is not an essential structure for sound localization in mammals. The lateral superior olivary nucleus is well developed in bats (4300) and dolphin and is also present in all species we have examined. This suggests that this nucleus is involved in auditory localization and complex auditory discriminations. The medial nucleus of the trapezoid body is well developed (2100–5800 nerve cells) in all species examined.