Binaural mechanisms of spatial tuning in the cat's superior colliculus distinguished using monaural occlusion

1987 ◽  
Vol 57 (3) ◽  
pp. 688-701 ◽  
Author(s):  
J. C. Middlebrooks

This study explores the mechanisms of auditory spatial tuning in the superior colliculus of the anesthetized cat by correlating spatial tuning within specific regions of space with particular types of binaural interaction. The auditory spatial tuning of units was measured using a movable, broad-band stimulus presented in a free sound field. The contribution of each ear to the response of a unit was identified by acutely plugging one or the other ear. Every unit became largely or entirely unresponsive when a foam-rubber earplug was placed in the ear contralateral to the recording site. Thus, every unit exhibited an excitatory or facilitatory influence from the contralateral ear. A plug placed in the ipsilateral ear had different effects on different units. For half of the units (16/32), an ipsilateral earplug produced increases in the sizes of the units' receptive fields and increases in the magnitudes of their responses to stimuli presented from most locations. Thus, these units exhibited inhibition from the ipsilateral ear. Another class of units (9/32) exhibited ipsilateral facilitation, in that an ipsilateral earplug caused decreases in the sizes of the units' receptive fields and prominent decreases in their response magnitudes. For the remaining units (7/32), an ipsilateral earplug resulted in decreases in the sizes of the units' receptive fields, but produced both decreases in the responses of units to stimuli presented in their best areas and increases in the responses to stimuli presented away from the best areas. Thus these units exhibited mixed facilitatory and inhibitory ipsilateral influences. The influence of an ipsilateral earplug on a unit's response tended to correlate with its spatial tuning. The region of space within which a sound source was most effective in activating a unit was its “best area”. The best areas of units exhibiting ipsilateral inhibition were located furthest peripherally, those of units showing ipsilateral facilitation were located furthest frontally, and the best areas of units showing mixed ipsilateral influences were located in an intermediate area. The frequency tuning of units measured using a free-field tone source also tended to correlate with the locations of their best areas. Half of the units tested (27/54) responded to tones of the sound pressure levels (SPLs) that were used (up to 50 dB SPL).(ABSTRACT TRUNCATED AT 400 WORDS)

1987 ◽  
Vol 57 (3) ◽  
pp. 672-687 ◽  
Author(s):  
J. C. Middlebrooks ◽  
E. I. Knudsen

This study examines the influence of external ear position on the auditory spatial tuning of single units in the superior colliculus of the anesthetized cat. Unit responses to broad-band stimuli presented in a free sound field were measured with the external ears in a forward symmetrical position or with one or the other ear turned 40 degrees to the side; the ears are referred to as contra- or ipsilateral with respect to the side of the recording site. Changes in the position of either ear modified the spatial tuning of units. The region of space from which a stimulus was most effective in activating a unit is referred to as the unit's “best area”. Whenever the contralateral ear was turned to the side, best areas shifted peripherally and somewhat upward, roughly in proportion to the magnitude of the change in ear position. A turn of the ipsilateral ear to the side had more variable effects, but best areas generally shifted frontally. Best areas located between approximately 10 and 40 degrees contralateral when the ears were forward were least affected by changes in ipsilateral ear position. Changes in ear position also modified the maximum response rates of many units. Units with best areas located within approximately 20 degrees of the frontal midline when the ears were forward exhibited a pronounced decrease in responsiveness when either ear was turned. Units with more peripheral best areas tended to show no change or a slight increase in responsiveness. The influence of ear position on the directionality of the external ears was determined by mapping the cochlear microphonic response to tones or one-third-octave bands of noise before and after turning the ear. When the ears were forward, maximum interaural intensity differences (IIDs) were produced by high-frequency sound sources (greater than or equal to 20 kHz) located 20-40 degrees from the frontal midline and by lower frequency sources located further peripherally. The influence of ear position on the locations from which maximum IIDs were produced was similar to the influence of ear position on unit best areas. Changes in ipsilateral ear position had different effects on high- and low-frequency IIDs that were comparable with the effects of changes in ear position on frontally and peripherally located best areas, respectively.(ABSTRACT TRUNCATED AT 400 WORDS)


1983 ◽  
Vol 49 (3) ◽  
pp. 674-685 ◽  
Author(s):  
L. Z. Wise ◽  
D. R. Irvine

1. The auditory responses of 207 single neurons in the intermediate and deep layers of the superior colliculus (SC) of barbiturate -or chloralose-anesthetized cats were recorded extracellularly. Sealed stimulating systems incorporating calibrated probe microphone assemblies were employed to present tone- and noise-burst stimuli. 2. All acoustically activated neurons responded with onset responses to noise bursts. Of those neurons also tested with tonal stimuli, approximately 30% were unresponsive over the frequency range tested (0.1-40 kHz), while the others had higher thresholds to tones than to noise. 3. Details of frequency responsiveness were obtained for 55 neurons; 21 were broadly tuned, while 34 were sharply tuned with clearly defined characteristic frequencies (CFs). All sharply tuned neurons had CFs greater than or equal to 10 kHz. 4. The majority of neurons (81%) responded with latencies in the range 8-20 ms; only 11% of neurons had latencies greater than 30 ms. 5. Binaural response properties were examined for 165 neurons. The great majority (79%) received monaural excitatory input only from the contralateral ear (EO). However, most EO cells were binaurally influenced, the contralateral response being either inhibited (EO/I; 96 of 131 units) or facilitated (EO/F; 33 of 131 units) by simultaneous ipsilateral stimulation. Small subgroups were monaurally excited by either ear (EE cells; 8%) or were unresponsive monaurally but responded strongly to binaural stimulation (OO/F cells; 7%). 6. EO/I, EO/F, and OO/F neurons showed characteristic forms of sensitivity to interaural intensity differences (IIDs). The IID functions of EO/I neurons would be expected to produce large contralateral spatial receptive fields with clearly defined medial borders, such as have been described in studies of deep SC neurons employing free-field stimuli. 7. Preliminary evidence suggests a possible topographic organization of IID sensitivity in deep SC, such that the steeply sloping portion of the function (corresponding to the medial edge of the receptive field) is shifted laterally for EO/I neurons located more caudally in the nucleus. 8. The auditory properties of deep SC neurons are compared with previous reports and implications for the organization of auditory input are considered. The binaural properties and auditory spatial fields of deep SC neurons suggest that any representation of auditory space in this structure is unlikely to be based on restricted spatial fields.


2003 ◽  
Vol 90 (4) ◽  
pp. 2648-2659 ◽  
Author(s):  
Susanne J. Sterbing ◽  
Klaus Hartung ◽  
Klaus-Peter Hoffmann

How do neurons in the inferior colliculus (IC) encode the spatial location of sound? We have addressed this question using a virtual auditory environment. For this purpose, the individual head-related transfer functions (HRTFs) of 18 guinea pigs were measured under free-field conditions for 122 locations covering the upper hemisphere. From 257 neurons, 94% responded to the short (50-ms) white noise stimulus at 70 dB sound pressure level (SPL). Out of these neurons, 80% were spatially tuned with a receptive field that is smaller than a hemifield (at 70 dB). The remainder responded omnidirectionally or showed fractured receptive fields. The majority of the neurons preferred directions in the contralateral hemisphere. However, preference for front or rear positions and high elevations occurred frequently. For stimulation at 70 dB SPL, the average diameter of the receptive fields, based on half-maximal response, was less than a quarter of the upper hemisphere. Neurons that preferred frontal directions responded weakly or showed no response to posterior directions and vice versa. Hence, front/back discrimination is present at the single-neuron level in the IC. When nonindividual HRTFs were used to create the stimuli, the spatial receptive fields of most neurons became larger, split into several parts, changed position, or the response became omnidirectional. Variation of absolute sound intensity had little effect on the preferred directions of the neurons over a range of 20 to 40 dB above threshold. With increasing intensity, most receptive fields remained constant or expanded. Furthermore, we tested the influence of binaural decorrelation and stimulus bandwidth on spatial tuning. The vast majority of neurons with a low characteristic frequency (<2.5 kHz) lost spatial tuning under stimulation with binaurally uncorrelated noise, whereas high-frequency units were mostly unaffected. Most neurons that showed spatial tuning under broadband stimulation (white noise and 1 octave wide noise) turned omnidirectional when stimulated with 1/3 octave wide noise.


1996 ◽  
Vol 76 (2) ◽  
pp. 1246-1266 ◽  
Author(s):  
M. T. Wallace ◽  
L. K. Wilkinson ◽  
B. E. Stein

1. The properties of visual-, auditory-, and somatosensory-responsive neurons, as well as of neurons responsive to multiple sensory cues (i.e., multisensory), were examined in the superior colliculus of the rhesus monkey. Although superficial layer neurons responded exclusively to visual stimuli and visual inputs predominated in deeper layers, there was also a rich nonvisual and multisensory representation in the superior colliculus. More than a quarter (27.8%) of the deep layer population responded to stimuli from more than a single sensory modality. In contrast, 37% responded only to visual cues, 17.6% to auditory cues, and 17.6% to somatosensory cues. Unimodal- and multisensory-responsive neurons were clustered by modality. Each of these modalities was represented in map-like fashion, and the different representations were in alignment with one another. 2. Most deep layer visually responsive neurons were binocular and exhibited poor selectivity for such stimulus characteristics as orientation, velocity, and direction of movement. Similarly, most auditory-responsive neurons had contralateral receptive fields and were binaural, but had little frequency selectivity and preferred complex, broad-band sounds. Somatosensory-responsive neurons were overwhelmingly contralateral, high velocity, and rapidly adapting. Only rarely did somatosensory-responsive neurons require distortion of subcutaneous tissue for activation. 3. The spatial congruence among the different receptive fields of multisensory neurons was a critical feature underlying their ability to synthesize cross-modal information. 4. Combinations of stimuli could have very different consequences in the same neuron, depending on their temporal and spatial relationships. Generally, multisensory interactions were evident when pairs of stimuli were separated from one another by < 500 ms, and the products of these interactions far exceeded the sum of their unimodal components. Whether the combination of stimuli produced response enhancement, response depression, or no interaction depended on the location of the stimuli relative to one another and to their respective receptive fields. Maximal response enhancements were observed when stimuli originated from similar locations in space (as when derived from the same event) because they fell within the excitatory receptive fields of the same multisensory neurons. If, however, the stimuli were spatially disparate such that one fell beyond the excitatory borders of its receptive field, either no interaction was produced or this stimulus depressed the effectiveness of the other. Furthermore, maximal response interactions were seen with the pairing of weakly effective unimodal stimuli. As the individual unimodal stimuli became increasingly effective, the levels of response enhancement to stimulus combinations declined, a principle referred to as inverse effectiveness. Many of the integrative principles seen here in the primate superior colliculus are strikingly similar to those observed in the cat. These observations indicate that a set of common principles of multisensory integration is adaptable in widely divergent species living in very different ecological situations. 5. Surprisingly, a few multisensory neurons had individual receptive fields that were not in register with one another. This has not been noted in multisensory neurons of other species, and these "anomalous" receptive fields could present a daunting problem: stimuli originating from the same general location in space cannot simultaneously fall within their respective receptive fields, a stimulus pairing that may result in response depression. Conversely, stimuli that originate from separate events and disparate locations (and fall within their receptive fields) may result in response enhancement. However, the spatial principle of multisensory integration did not apply in these cases. (ABSTRACT TRUNCATED)


1999 ◽  
Vol 82 (5) ◽  
pp. 2197-2209 ◽  
Author(s):  
Joshua I. Gold ◽  
Eric I. Knudsen

Bimodal, auditory-visual neurons in the optic tectum of the barn owl are sharply tuned for sound source location. The auditory receptive fields (RFs) of these neurons are restricted in space primarily as a consequence of their tuning for interaural time differences and interaural level differences across broad ranges of frequencies. In this study, we examined the extent to which frequency-specific features of early auditory experience shape the auditory spatial tuning of these neurons. We manipulated auditory experience by implanting in one ear canal an acoustic filtering device that altered the timing and level of sound reaching the eardrum in a frequency-dependent fashion. We assessed the auditory spatial tuning at individual tectal sites in normal owls and in owls raised with the filtering device. At each site, we measured a family of auditory RFs using broadband sound and narrowband sounds with different center frequencies both with and without the device in place. In normal owls, the narrowband RFs for a given site all included a common region of space that corresponded with the broadband RF and aligned with the site's visual RF. Acute insertion of the filtering device in normal owls shifted the locations of the narrowband RFs away from the visual RF, the magnitude and direction of the shifts depending on the frequency of the stimulus. In contrast, in owls that were raised wearing the device, narrowband and broadband RFs were aligned with visual RFs so long as the device was in the ear but not after it was removed, indicating that auditory spatial tuning had been adaptively altered by experience with the device. The frequency tuning of tectal neurons in device-reared owls was also altered from normal. The results demonstrate that experience during development adaptively modifies the representation of auditory space in the barn owl's optic tectum in a frequency-dependent manner.


1994 ◽  
Vol 71 (1) ◽  
pp. 182-194 ◽  
Author(s):  
A. J. King ◽  
D. R. Moore ◽  
M. E. Hutchings

1. We have investigated the role of monaural cues provided by the outer ear in the construction of a map of auditory space in the superior colliculus. Single-unit recordings were made from the superior colliculus of adult ferrets that were deprived of binaural inputs by surgically ablating the ipsilateral cochlea on postnatal day 21 or 24. 2. The spatial response properties of auditory units in the deeper layers of this nucleus were studied using white-noise bursts presented under free-field conditions in an anechoic chamber. The thresholds of the units recorded in the monaural ferrets were not significantly different from those recorded in the superior colliculus of normal adult ferrets. In both groups the unit thresholds varied by 30-50 dB in each region of the superior colliculus. 3. In normal and monaural ferrets the elevation tuning tended to be sharper than the azimuth tuning. At sound levels of approximately 10 dB above threshold the auditory units recorded in both groups of animals were tuned to a specific region of space that was restricted in azimuth and elevation. The spatial location at which the maximum response was obtained (auditory best position) varied topographically in azimuth along the rostrocaudal axis of the nucleus and in elevation along the mediolateral axis. 4. The azimuthal distribution of best positions associated with each recording location in the superior colliculus of the monaural ferrets and the alignment between this dimension of the auditory map and that of the visual map in the overlying superficial layers were no different from those found at corresponding near-threshold sound levels in normal ferrets. 5. Elevation spatial selectivity was examined in a smaller sample of units. Although elevation best positions shifted downward from the medial to the lateral side of the nucleus in both normal and monaural ferrets, we found that the topography of the auditory representation and its alignment with the visual representation were statistically different in the two groups of animals. 6. Increasing the sound level does not affect the representation of auditory space in normal ferrets. However, when the stimulus level presented to monoaural ferrets was increased, the receptive fields either expanded so that the responses were no longer tuned to any particular region of space, or the responses remained tuned but exhibited a marked shift in the value of the best position.(ABSTRACT TRUNCATED AT 400 WORDS)


1984 ◽  
Vol 52 (4) ◽  
pp. 709-723 ◽  
Author(s):  
E. I. Knudsen

Auditory units in the optic tectum of the barn owl (Tyto alba) were studied under free-field conditions with a movable sound source. These units are selective for sound location and their spatial tuning varies systematically across the tectum, forming a map of space (8). I found that frequency tuning, response latencies, and thresholds of units changed in parallel with their spatial tuning, suggesting that as a consequence these properties also are topographically distributed in the optic tectum. Response rates were determined primarily by the location of the sound source. Regardless of sound intensity, only stimuli delivered from a restricted “best area” elicited vigorous responses. Minimum response latencies were shortest for units with frontal best areas and increased systematically for units with best areas located more peripherally. The response latencies of units with best areas centered within 25 degrees of the owl's visual axis were virtually independent of sound intensity and speaker position. The latencies of units with more peripheral best areas varied with speaker position and were shortest when the speaker was in the best area. Thresholds to noise stimuli were lowest for units with best areas directly in front of the owl and increased systematically for units with best areas located more peripherally. Thus, in the representation of frontal space, where units have the smallest receptive fields and the magnification of space is the greatest (8), units also respond to the weakest sound fields. Many units (20%) could not be driven with tonal stimuli; of those that could, most were broadly tuned for frequency. Characteristic frequencies and high-frequency cutoffs shifted lower as best areas moved peripherally. High-frequency tones, which excited units with frontal best areas, either inhibited or failed to drive units with peripheral best areas. These systematic changes in unit response properties influence how sounds from different locations are represented in the tectum and reflect integrative strategies used by the owl's auditory system in deriving a representation of auditory space.


1987 ◽  
Vol 57 (2) ◽  
pp. 596-624 ◽  
Author(s):  
A. J. King ◽  
M. E. Hutchings

Extracellular single-unit recordings were made from auditory neurons in the superior colliculus of ferrets anesthetized with either a neuroleptic or a combination of barbiturate with paralysis. The response properties of these neurons were studied using white-noise bursts presented under free-field conditions in an anechoic chamber. Auditory neurons were found throughout the intermediate and deep layers of the superior colliculus. All neurons were spontaneously active, the rates of discharge varying from 0.1 to 61.1 spikes X s-1. Although the spontaneous discharge interspike-interval histograms for many units approximated to exponential distributions, the histograms of 44% had clear secondary peaks, indicating more than one preferred interval, and could not be modeled by a simple process. Most neurons (50%) responded only at stimulus onset, whereas 12% exhibited sustained discharges and 38% gave onset responses followed by a period of silence or reduced activity and then a period of elevated discharge, which was not apparently related to stimulus offset. Neurons with multipeaked response patterns were concentrated in the stratum griseum profundum. The latencies from arrival of the stimulus at the ear to the onset of neural activity ranged from 6 to 49 ms and decreased with increasing stimulus intensity. Although responsive to sounds over a large region of space, most neurons had clearly defined best positions at which the strongest response was obtained. The response declined as the speaker was moved away from this position, and nearly all units had peaked response profiles. The spatial tuning varied between different neurons, but most were more sharply tuned in elevation than in azimuth. Increasing the stimulus intensity did not, in general, alter the best positions of these neurons, but usually resulted in a broadening of the receptive fields, although other units became more sharply tuned. The best positions of auditory neurons varied systematically in azimuth from 20 degrees into the ipsilateral hemifield to 130 degrees into the contralateral hemifield as the electrode was moved from the rostrolateral to the caudomedial end of the superior colliculus. The best positions shifted in elevation along a rostromedial to caudolateral axis from 60 degrees above to 50 degrees below the visuoaural plane.(ABSTRACT TRUNCATED AT 400 WORDS)


1998 ◽  
Vol 80 (6) ◽  
pp. 2941-2953 ◽  
Author(s):  
Neil J. Ingham ◽  
Sally K. Thornton ◽  
Damian McCrossan ◽  
Deborah J. Withington

Ingham, Neil J., Sally K. Thornton, Damian McCrossan, and Deborah J. Withington. Neurotransmitter involvement in development and maintenance of the auditory space map in the guinea pig superior colliculus. J. Neurophysiol. 80: 2941–2953, 1998. The mammalian superior colliculus (SC) is a complex area of the midbrain in terms of anatomy, physiology, and neurochemistry. The SC bears representations of the major sensory modalites integrated with a motor output system. It is implicated with saccade generation, in behavioral responses to novel sensory stimuli and receives innervation from diverse regions of the brain using many neurotransmitter classes. Ethylene-vinyl acetate copolymer (Elvax-40W polymer) was used here to deliver chronically neurotransmitter receptor antagonists to the SC of the guinea pig to investigate the potential role played by the major neurotransmitter systems in the collicular representation of auditory space. Slices of polymer containing different drugs were implanted onto the SC of guinea pigs before the development of the SC azimuthal auditory space map, at ∼20 days after birth (DAB). A further group of animals was exposed to aminophosphonopentanoic acid (AP5) at ∼250 DAB. Azimuthal spatial tuning properties of deep layer multiunits of anesthetized guinea pigs were examined ∼20 days after implantation of the Elvax polymer. Broadband noise bursts were presented to the animals under anechoic, free-field conditions. Neuronal responses were used to construct polar plots representative of the auditory spatial multiunit receptive fields (MURFs). Animals exposed to control polymer could develop a map of auditory space in the SC comparable with that seen in unimplanted normal animals. Exposure of the SC of young animals to AP5, 6-cyano-7-nitroquinoxaline-2,3-dione, or atropine, resulted in a reduction in the proportion of spatially tuned responses with an increase in the proportion of broadly tuned responses and a degradation in topographic order. Thus N-methyl-d-aspartate (NMDA) and non-NMDA glutamate receptors and muscarinic acetylcholine receptors appear to play vital roles in the development of the SC auditory space map. A group of animals exposed to AP5 beginning at ∼250 DAB produced results very similar to those obtained in the young group exposed to AP5. Thus NMDA glutamate receptors also seem to be involved in the maintenance of the SC representation of auditory space in the adult guinea pig. Exposure of the SC of young guinea pigs to γ-aminobutyric acid (GABA) receptor blocking agents produced some but not total disruption of the spatial tuning of auditory MURFs. Receptive fields were large compared with controls, but a significant degree of topographical organization was maintained. GABA receptors may play a role in the development of fine tuning and sharpening of auditory spatial responses in the SC but not necessarily in the generation of topographical order of the these responses.


1985 ◽  
Vol 54 (4) ◽  
pp. 757-781 ◽  
Author(s):  
Z. M. Fuzessery ◽  
G. D. Pollak

This study of the neural representation of sound location in the bat Pteronotus parnellii describes how the peripheral and central components of its auditory system shape the horizontal and vertical spatial selectivity of single neurons in the inferior colliculus. Pteronotus extracts spatial information from the echoes of an emitted pulse composed of four constant-frequency harmonics (30, 60, 90, and 120 kHz), each terminated by a downward frequency sweep. To quantify the intensity cues available in the echo, cochlear microphonic response thresholds were used to measure the directional selectivity of the ear and the interaural intensity level disparities (IIDs) created between ears at standardized speaker positions in the bat's frontal sound field, at frequencies in the pulse spectrum. Speaker positions where thresholds were lowest were termed the sensitive area (SA) of the ear. Positions where IID values were greater than 10 dB were termed the difference area (DA). Ear directionality exhibited a pronounced frequency dependence, both in terms of the degree of directional selectivity and the position of the SA. At the 30-kHz harmonic of the pulse, the ear was broadly directional; the SA covered most of the lower half of the ipsilateral field. The ear was highly directional at the 60- and 90-kHz harmonics. Also, the vertical position of the SA changed dramatically between 60 and 90 kHz, from the horizontal midline at 60 kHz to 40 degrees below the midline at 90 kHz. The positions of the DAs also showed a pronounced frequency dependence. The 30-kHz DA was restricted to the extreme lateral part of the frontal sound field. The 60- and 90-kHz DAs were located in the same positions as the equivalent SAs and exhibited the same difference in vertical position. The DAs of the pulse harmonics differ in both their horizontal and vertical positions; the ears thus generate pronounced binaural spectral cues, which provide two-dimensional spatial information. In the inferior colliculus, a combined paradigm of closed-field dichotic stimulation, followed by free-field stimulation, was used to document the frequency tuning and binaural response properties of single neurons and to correlate these properties with the neuron's horizontal and vertical spatial selectivity in the frontal sound field. Where a neuron responded to free-field stimulation at the lowest intensity is termed its SA. A neuron's frequency tuning primarily influenced its degree of spatial selectivity and its sensitivity in the vertical plane, reflecting the directional properties of the external ears at the neuron's best frequency.(ABSTRACT TRUNCATED AT 400 WORDS)


Sign in / Sign up

Export Citation Format

Share Document