Representation of interaural time difference in the central nucleus of the barn owl's inferior colliculus

This paper investigates the role of the central nucleus of the barn owl's inferior colliculus in determination of the sound-source azimuth. The central nucleus contains many neurons that are sensitive to interaural time difference (ITD), the cue for azimuth in the barn owl. The response of these neurons varies in a cyclic manner with the ITD of a tone or noise burst. Response maxima recur at integer multiples of the period of the stimulating tone, or, if the stimulus is noise, at integer multiples of the period corresponding to the neuron's best frequency. Such neurons can signal, by means of their relative spike rate, the phase difference between the sounds reaching the left and right ears. Since an interaural phase difference corresponds to more than one ITD, these neurons represent ITD ambiguously. We call this phenomenon phase ambiguity. The central nucleus is tonotopically organized and its neurons are narrowly tuned to frequency. Neurons in an array perpendicular to isofrequency laminae form a physiological and anatomical unit; only one ITD, the array-specific ITD, activates all neurons in an array at the same relative level. We, therefore, may say that, in the central nucleus, an ITD is conserved in an array of neurons. Array-specific ITDs are mapped and encompass the entire auditory space of the barn owl. Individual space-specific neurons of the external nucleus, which receive inputs from a wide range of frequency channels (Knudsen and Konishi, 1978), are selective for a unique ITD. Space-specific neurons do not show phase ambiguity when stimulated with noise (Takahashi and Konishi, 1986). Space-specific neurons receive inputs from arrays that are selective for the same ITD. The collective response of the neurons in an array may be the basis for the absence of phase ambiguity in space-specific neurons.     

Response properties of neurons in the core of the central nucleus of the inferior colliculus of the barn owl

The central nucleus of the inferior colliculus (ICC) is particularly important for the processing of interaural time differences (ITDs). In the barn owl, neuronal best frequencies in a subnucleus of the ICC, the ICCcore, span the animal's entire hearing range (approximately equal to 200-10 000 Hz). This means that low-frequency ITD-sensitive ICCcore neurons in the owl can be directly compared to ITD-sensitive mammalian ICC neurons with similar best frequencies as well as to the high-frequency ITD-sensitive neurons usually studied in owls. This report represents a first attempt to systematically describe important physiological properties of ICCcore neurons in the barn owl, with particular attention to the low-frequency region (< 2 kHz). Responses were obtained from 133 neurons or small clusters of neurons; recording sites were confirmed by histological reconstruction of electrode tracks based on electrolytic lesions. Iso-intensity frequency response functions were typically approximately equal to 1 octave wide in the low-frequency range and approximately equal to 1/3 octave wide in the high-frequency range. Most neurons were ITD-tuned; both noise and pure tone stimuli yielded periodic ITD tuning curves with several equivalent response maxima. In most cases ITD tuning curves had a response peak within the barn owl's physiological ITD range. ITD tuning widths were inversely correlated with neuronal best frequency. None of the ICCcore neurons studied were sensitive to interaural level differences. Monaural inputs to ICCcore cells were typically binaurally balanced, i.e. they exhibited similar response thresholds, dynamic ranges, slopes and saturation levels, for both left and right ear monaural stimulation.     

Mapping responses to frequency sweeps and tones in the inferior colliculus of house mice

In auditory maps of the primary auditory cortex, neural response properties are arranged in a systematic way over the cortical surface. As in the visual system, such maps may play a critical role in the representation of sounds for perception and cognition. By recording from single neurons in the central nucleus of the inferior colliculus (ICC) of the mouse, we present the first evidence for spatial organizations of parameters of frequency sweeps (sweep speed, upward/downward sweep direction) and of whole-field tone response patterns together with a map of frequency tuning curve shape. The maps of sweep speed, tone response patterns and tuning curve shape are concentrically arranged on frequency band laminae of the ICC with the representation of slow speeds, build up response types and sharp tuning mainly in the centre of a lamina, and all (including high) speeds, phasic response types and broad tuning mainly in the periphery. Representation of sweep direction shows preferences for upward sweeps medially and laterally and downward sweeps mainly centrally in the ICC (either striped or concentric map). These maps are compatible with the idea of a gradient of decreasing inhibition from the centre to the periphery of the ICC and by gradients of intrinsic neuronal properties (onset or sustained responding). The maps in the inferior colliculus compare favourably with corresponding maps in the primary auditory cortex, and we show how the maps of sweep speed and direction selectivity of the primary auditory cortex could be derived from the here-found maps of the inferior colliculus.     

A topographic representation of auditory space in the external nucleus of the inferior colliculus of the guinea-pig

The possibility that the external nucleus of the inferior colliculus (ICX) of the pigmented guinea-pig contains a map of auditory space has been investigated. Auditory stimuli consisted of broad-band sound delivered under free-field anechoic conditions from a range of positions around the animal's azimuthal axis. The responses of clusters of neurons in the ICX to threshold and to near-threshold stimuli displayed sharp spatial tuning. The responses recorded from rostral ICX revealed a preference for auditory stimuli in the anterior field while more caudal neurons preferentially responded to sounds presented in the posterior field. Neurons at intermediate points, along the rostro-caudal axis of the nucleus, displayed preferences for sound stimuli in appropriately intermediate field positions along the contralateral azimuthal axis. At higher stimulus intensities the spatial tuning of the responses decreased, but the optimal direction of preference was usually retained. The contribution of binaural processing to auditory spatial tuning was evident, since unilateral cochlea ablation destroyed the spatial tuning at higher stimulus intensities. The results presented provide the first evidence that a topographically ordered representation of the contralateral auditory azimuth is present in the ICX of a mammal.     

Adaptation in the auditory midbrain of the barn owl (Tyto alba) induced by tonal double stimulation

During hunting, the barn owl typically listens to several successive sounds as generated, for example, by rustling mice. As auditory cells exhibit adaptive coding, the earlier stimuli may influence the detection of the later stimuli. This situation was mimicked with two double-stimulus paradigms, and adaptation was investigated in neurons of the barn owl's central nucleus of the inferior colliculus. Each double-stimulus paradigm consisted of a first or reference stimulus and a second stimulus (probe). In one paradigm (second level tuning), the probe level was varied, whereas in the other paradigm (inter-stimulus interval tuning), the stimulus interval between the first and second stimulus was changed systematically. Neurons were stimulated with monaural pure tones at the best frequency, while the response was recorded extracellularly. The responses to the probe were significantly reduced when the reference stimulus and probe had the same level and the inter-stimulus interval was short. This indicated response adaptation, which could be compensated for by an increase of the probe level of 5-7 dB over the reference level, if the latter was in the lower half of the dynamic range of a neuron's rate-level function. Recovery from adaptation could be best fitted with a double exponential showing a fast (1.25 ms) and a slow (800 ms) component. These results suggest that neurons in the auditory system show dynamic coding properties to tonal double stimulation that might be relevant for faithful upstream signal propagation. Furthermore, the overall stimulus level of the masker also seems to affect the recovery capabilities of auditory neurons.     

Visual deprivation modifies auditory directional tuning in the inferior colliculus

The aim of this study was to assess whether early visual deprivation could modulate the auditory directional tunings of single neurons in the central nucleus of the inferior colliculus of the rat. Extracellular recordings were carried out in normal and early bilaterally enucleated rats. Direction-specific auditory neurons were found in both groups, and no evidence was found for a topographical order of best azimuthal direction. Although the distribution of best azimuthal direction was unaltered in enucleated rats, our data suggest that early visual deprivation modifies the width of auditory directional receptive fields in the central nucleus of the inferior colliculus. This suggests that visual input plays a substantial role in refining auditory receptive fields in the inferior colliculus.     

Binaural responses in the auditory midbrain of chicken (Gallus gallus)

The auditory midbrain is the location in which neurons represent binaural acoustic information necessary for sound localization. The external nucleus of the midbrain inferior colliculus (IC) of the barn owl is a classic example of an auditory space map, but it is unknown to what extent the principles underlying its formation generalize to other, less specialized animals. We characterized the spiking responses of 139 auditory neurons in the IC of the chicken (Gallus gallus) in vivo, focusing on their sensitivities to the binaural localization cues of interaural time (ITD) and level (ILD) differences. Most units were frequency‐selective, with best frequencies distributed unevenly into low‐frequency and high‐frequency (> 2 kHz) clusters. Many units showed sensitivity to either ITD (65%) or ILD (66%) and nearly half to both (47%). ITD selectivity was disproportionately more common among low‐frequency units, while ILD‐only selective units were predominantly tuned to high frequencies. ILD sensitivities were diverse, and we thus developed a decision tree defining five types. One rare type with a bell‐like ILD tuning was also selective for ITD but typically not frequency‐selective, and thus matched the characteristics of neurons in the auditory space map of the barn owl. Our results suggest that generalist birds such as the chicken show a prominent representation of ITD and ILD cues in the IC, providing complementary information for sound localization, according to the duplex theory. A broadband response type narrowly selective for both ITD and ILD may form the basis for a representation of auditory space.     

Spatial map of frequency tuning-curve shapes in the mouse inferior colliculus

Neurons in the central nucleus of the auditory midbrain inferior colliculus divide into four classes according to the shapes of their receptive fields. Neurons of two of these classes - sharply tuned, inhibition-dominated neurons of class II, and broadly tuned neurons of class III - show systematic gradients in their abundance on isofrequency contours. Sharp tuning is most prevalent in the center, broad tuning in the periphery of the ICC. This new map of tuning-curve shape adds to the six previously described maps of neural response properties on isofrequency contours of the ICC and stresses the fact that very different sensitivities and selectivities to sound properties are combined in local clusters of collicular neurons.     

The role of GABAergic inhibition in processing of interaural time difference in the owl's auditory system

The barn owl uses interaural time differences (ITDs) to localize the azimuthal position of sound. ITDs are processed by an anatomically distinct pathway in the brainstem. Neuronal selectivity for ITD is generated in the nucleus laminaris (NL) and conveyed to both the anterior portion of the ventral nucleus of the lateral lemniscus (VLVa) and the central (ICc) and external (ICx) nuclei of the inferior colliculus. With tonal stimuli, neurons in all regions are found to respond maximally not only to the real ITD, but also to ITDs that differ by integer multiples of the tonal period. This phenomenon, phase ambiguity, does not occur when ICx neurons are stimulated with noise. The main aim of this study was to determine the role of GABAergic inhibition in the processing of ITDs. Selectivity for ITD is similar in the NL and VLVa and improves in the ICc and ICx. Iontophoresis of bicuculline methiodide (BMI), a selective GABAA antagonist, decreased the ITD selectivity of ICc and ICx neurons, but did not affect that of VLVa neurons. Responses of VLVa and ICc neurons to unfavorable ITDs were below the monaural response levels. BMI raised both binaural responses to unfavorable ITDs and monaural responses, though the former remained smaller than the latter. During BMI application, ICx neurons showed phase ambiguity to noise stimuli and no longer responded to a unique ITD. BMI increased the response magnitude and changed the temporal discharge patterns in the VLVa, ICc, and ICx. Iontophoretically applied GABA exerted effects opposite to those of BMI, and the effects could be antagonized with simultaneous application of BMI. These results suggest that GABAergic inhibition (1) sharpens ITD selectivity in the ICc and ICx, (2) contributes to the elimination of phase ambiguity in the ICx, and (3) controls response magnitude and temporal characteristics in the VLVa, ICc, and ICx. Through these actions, GABAergic inhibition shapes the horizontal dimension of the auditory receptive fields.     

Classical conditioning modifies cytochrome oxidase activity in the auditory system

The effects of excitatory classical conditioning on cytochrome oxidase activity in the central auditory system were investigated using quantitative histochemistry. Rats in the conditioned group were trained with consistent pairings of a compound conditional stimulus (a tone and a light) with a mild footshock, to elicit conditioned suppression of drinking. Rats in the pseudorandom group were exposed to pseudorandom presentations of the same tone, light and shock stimuli without consistent pairings. Untrained rats in a naive group did not receive presentations of the experimental stimuli.
 The findings demonstrated that auditory fear conditioning modifies the metabolic neuronal responses of the auditory system, supporting the hypothesis that sensory neurons are responsive to behavioural stimulus properties acquired by learning. There was a clear distinction between thalamocortical and lower divisions of the auditory system based on the differences in metabolic activity evoked by classical conditioning, which lead to an overt learned behavioural response versus pseudorandom stimulus presentations, which lead to behavioural habituation. Increases in cytochrome oxidase activity indicated that tone processing is enhanced during associative conditioning at upper auditory structures (medial geniculate nucleus and secondary auditory cortices). In contrast, metabolic activation of lower auditory structures (cochlear nuclei and inferior colliculus) in response to the pseudorandom presentation of the experimental stimuli suggest that these areas may be activated during habituation to tone stimuli. Together these findings show that mapping the metabolic activity of cytochrome oxidase with quantitative histochemistry can be successfully used to map regional long‐lasting effects of learning on brain systems.     

Some acoustic properties of neurones in the ferret inferior colliculus

Single neurones in the central nucleus of the ferret inferior colliculus (ICC) were studied using extracellular recording. Responses to pure tone stimuli were analyzed to assess the frequency organization of the nucleus, the sensitivity and tuning properties of neurones and the effects of binaural sound presentation. Excitatory tuning curves had the characteristic shape found for neurones in the auditory systems of other species. Many ferret neurones were inhibited by stimulus frequencies on either side of the range producing excitatory responses. Sharpness of excitatory tuning was found to be comparable with that reported for the cat. Neurones having best frequencies in the range 4–15 kHz showed the greatest sensitivity. All electrode penetrations revealed a dorsal-to-ventral progression of neurones of increasing best frequency. Some neurones were classified according to the predominant type of input from each ear. Over 80% of these units were binaurally influenced. Nearly all cells received an excitatory input from the contralateral ear and about one-third of those units were excited by ipsilateral stimulation. The remainder showed lateral response. These experiments demonstrate that the ferret may be a satisfactory alternative to other carnivores for studies of the auditory system.     

Fos-like immunoreactivity in central auditory neurons of the mouse

Fos-like immunoreactivity was used to study sound-induced activation of neurons in the auditory brainstem. Immunoreactivity was assayed with a polyclonal antibody to Fos. In response to 6-kHz tone bursts, the pattern of staining was a band of immunoreactive neurons positioned at the tonotopically appropriate position within the cochlear nucleus and the inferior colliculus. The band was narrow at low sound pressure levels but wider along the tonotopic axis at higher sound levels. In response to noise bursts, the pattern was broader and often extended throughout the auditory nuclei. Often within this broad pattern were “sub-bands” of immunostained neurons, interspersed with bands of unstained neurons. With increasing sound pressure levels above 35--55 dB, the number of Fos-like immunoreactive neurons increased for the cochlear nucleus, superior olivary complex, and inferior colliculus. In the cochlear nucleus and inferior colliculus, the stained cells were small, and hence their activity would be difficult to sample in electrophysiological studies. In the medial nucleus of the trapezoid body, the stained neurons had larger somata and other characteristics of principal cells. Anesthesia with Nembutal or Avertin, but not with ketamine or urethane, decreased the number of Fos-like immunoreactive neurons in the cochlear nucleus. The different anesthetics produced more variable results in the inferior colliculus. In anesthetized, monaurally stimulated animals, the presence of staining in the contralateral cochlear nucleus indicates that some Fos-like immunoreactivity may be mediated by descending or commissural systems. These observations indicate that Fos assays are useful for studying the pattern of neuronal activation in the auditory system and may also be useful in studying the descending auditory pathways. © 1995 Wiley-Liss, Inc.     

A comparison of the interaural time sensitivity of neurons in the inferior colliculus and thalamus of the unanesthetized rabbit.

The localization of low-frequency sounds (less than 3 kHz) along the azimuth involves comparing the ongoing difference in the time of arrival of a sound at the two ears. Information about interaural time differences (ITDs) is derived from an initial comparison performed in the superior olivary complex. However, little is known about which aspects of this information are transformed as it ascends the brainstem. To address this issue, we compared the ITD sensitivity of neurons in the inferior colliculus (IC) and auditory thalamus, successive stations in the auditory pathway. We found ITD sensitivity in the IC and thalamus to be similar in several respects. At both levels, the large majority of neurons responded maximally to ITDs within the range that a rabbit would normally encounter (+/- 300 microseconds) and preferred ipsilateral delays, delays that would be created by sounds in the contralateral sound field. The range of frequencies over which ITD sensitivity was expressed was also similar in the midbrain and thalamus. Several differences were also apparent. In comparison to IC neurons, neurons in the thalamus responded over more restricted ranges of ITD, responded at lower rates, and, in response to monaural stimulation, showed an increased influence of inhibition. Finally, a greater proportion of thalamic units had characteristic delays corresponding to intermediate discharge rates. The preservation of a bias for ipsilateral delays from IC to thalamus suggests that a representation of contralateral azimuths is present at both levels. Similarities between the two levels suggest that information about ITDs is faithfully transmitted from midbrain to thalamus. Differences in ITD sensitivity, such as the sharper tuning for ITDs, suggest that the thalamus is not a simple relay. Enhanced sensitivity to ITDs should translate to better-defined azimuthal receptive fields, and therefore may be a step toward achieving an optimal representation of azimuth within the auditory pathway.     

Spatial selectivity and binaural responses in the inferior colliculus of the great horned owl

In this study we have investigated the processing of auditory cues for sound localization in the great horned owl (Bubo virginianus). Previous studies have shown that the barn owl, whose ears are asymmetrically oriented in the vertical plane, has a 2-dimensional, topographic representation of auditory space in the external division of the inferior colliculus (ICx). As in the barn owl, the great horned owl's ICx is anatomically distinct and projects to the optic tectum. Neurons in ICx respond over only a small range of azimuths (mean = 32 degrees), and azimuth is topographically mapped. In contrast to the barn owl, the great horned owl has bilaterally symmetrical ears and its receptive fields are not restricted in elevation. The binaural cues available for sound localization were measured both with cochlear microphonic recordings and with a microphone attached to a probe tube in the auditory canal. Interaural time disparity (ITD) varied monotonically with azimuth. Interaural intensity differences (IID) also changed with azimuth, but the largest IIDs were less than 15 dB, and the variation was not monotonic. Neither ITD nor IID varied systematically with changes in the vertical position of a sound source. We used dichotic stimulation to determine the sensitivity of ICx neurons to these binaural cues. Best ITD of ICx units was topographically mapped and strongly correlated with receptive-field azimuth. The width of ITD tuning curves, measured at 50% of the maximum response, averaged 72 microseconds. All ICx neurons responded only to binaural stimulation and had nonmonotonic IID tuning curves. Best IID was weakly, but significantly, correlated with best ITD (r = 0.39, p less than 0.05). The IID tuning curves, however, were broad (mean 50% width = 24 dB), and 67% of the units had best IIDs within 5 dB of 0 dB IID. ITD tuning was sensitive to variations in IID in the direction opposite to that expected for time-intensity trading, but the magnitude of this effect was only 1.5 microseconds/dB IID. We conclude that, in the great horned owl, the spatial selectivity of ICx neurons arises primarily from their ITD tuning. Except for the absence of elevation selectivity and the narrow range of best IIDs, ICx in the great horned owl appears to be organized much the same as in the barn owl.     

Complex sound analysis (frequency resolution, filtering and spectral integration) by single units of the inferior colliculus of the cat

The central nucleus of the inferior colliculus (ICC) is a center of convergence of brainstem input and is critical for auditory information processing. Here, the analysis of complex sound spectra by single neurons in the ICC is investigated. Several measures of frequency resolution (excitatory/inhibitory tuning curves, effective bandwidths, critical ratio bands, critical bands derived using narrowband masking and two-tone separation paradigms) have been obtained from the responses of these neurons at sound pressure levels (SPL) up to 80 dB above the units' response thresholds (nearly 110 dB SPL). Among our results are the following: (1) Narrowband masking measures of critical bands from ICC neurons closely parallel behavioral measures using the same stimulus paradigm. (2) Frequency resolution power as measured by critical bandwidths varies little as a function of stimulus intensity. (3) Tuning curves of ICC neurons provide no simple basis for predicting the frequency filtering of the same neurons excited by complex sound spectra. (4) There is a frequency dependence of all measures of frequency resolution similar to that found in psychophysical determinations of critical bandwidths. That is, spatial frequency resolution in the cochlea is the origin for the resolution found in the ICC and in behavioral tests. (5) Lateral inhibition at the level of the ICC clearly plays a role in frequency resolution. (6) Frequency resolution is encoded by response rate changes of ICC neurons and is independent of tone response threshold, response latency, spontaneous activity, tone response type, binaural response type. It is concluded that spectral analysis of sound is established by processes, ncluding lateral inhibition, independent of other basic response properties of neurons at the level of the ICC.     

Complex sound analysis (frequency resolution, filtering and spectral integration) by single units of the inferior colliculus of the cat

The central nucleus of the inferior colliculus (ICC) is a center of convergence of brainstem input and is critical for auditory information processing. Here, the analysis of complex sound spectra by single neurons in the ICC is investigated. Several measures of frequency resolution (excitatory/inhibitory tuning curves, effective bandwidths, critical ratio bands, critical bands derived using narrowband masking and two-tone separation paradigms) have been obtained from the responses of these neurons at sound pressure levels (SPL) up to 80 dB above the units' response thresholds (nearly 110 dB SPL). Among our results are the following: (1) Narrowband masking measures of critical bands from ICC neurons closely parallel behavioral measures using the same stimulus paradigm. (2) Frequency resolution power as measured by critical bandwidths varies little as a function of stimulus intensity. (3) Tuning curves of ICC neurons provide no simple basis for predicting the frequency filtering of the same neurons excited by complex sound spectra. (4) There is a frequency dependence of all measures of frequency resolution similar to that found in psychophysical determinations of critical bandwidths. That is, spatial frequency resolution in the cochlea is the origin for the resolution found in the ICC and in behavioral tests. (5) Lateral inhibition at the level of the ICC clearly plays a role in frequency resolution. (6) Frequency resolution is encoded by response rate changes of ICC neurons and is independent of tone response threshold, response latency, spontaneous activity, tone response type, binaural response type. It is concluded that spectral analysis of sound is established by processes, including lateral inhibition, independent of other basic response properties of neurons at the level of the ICC.     

The organization of frequency and binaural cues in the gerbil inferior colliculus

The inferior colliculus (IC) is the common target of separate pathways that transmit different types of auditory information. Beyond tonotopy, little is known about the organization of response properties within the 3‐dimensional layout of the auditory midbrain in most species. Through study of interaural time difference (ITD) processing, the functional properties of neurons can be readily characterized and related to specific pathways. To characterize the representation of ITDs relative to the frequency and hodological organization of the IC, the properties of neurons were recorded and the sites recovered histologically. Subdivisions of the IC were identified based on cytochrome oxidase (CO) histochemistry. The results were plotted within a framework formed by an MRI atlas of the gerbil brain. The central nucleus was composed of two parts, and lateral and dorsal cortical areas were identified. The lateral part of the central nucleus had the highest CO activity in the IC and a high proportion of neurons sensitive to ITDs. The medial portion had lower CO activity and fewer ITD‐sensitive neurons. A common tonotopy with a dorsolateral to ventromedial gradient of low to high frequencies spanned the two regions. The distribution of physiological responses was in close agreement with known patterns of ascending inputs. An understanding of the 3‐dimensional organization of the IC is needed to specify how the single tonotopic representation in the IC central nucleus leads to the multiple tonotopic representations in core areas of the auditory cortex.     

The Maturation of the Superior Collicular Map of Auditory Space in the Guinea Pig is Disrupted by Developmental Auditory Deprivation

Guinea pigs, reared from birth in an environment of omnidirectional white noise, fail to develop a map of auditory space in the deeper layers of the superior colliculus. Collicular responses from such noise-reared animals reveal large auditory spatial receptive fields. The representation of auditory space in the colliculus shows no topographic order. Exposing developing animals to the noise environment only for restricted time periods showed that animals reared normally up to 26 days after birth (DAB) and then placed in the noise chamber could not construct spatial maps, whereas animals reared normally to 30 DAB and then placed in the noise chamber until the terminal mapping experiment could construct topographically organized spatial maps with local receptive fields. Limiting the noise exposure to the period between 26 and 30 DAB was sufficient to prevent spatial map formation. The failure to form a map of auditory space did not reflect environmental damage to the cochlea or the functional organization of the primary auditory pathway. The response thresholds of cochlear microphonics and of auditory responses in both the inferior and superior colliculus were normal in noise-reared animals. Similarly normal were the tonotopic organization and frequency tuning characteristics of inferior collicular neurons. The rearing environment thus appears to exert a selective effect upon the maturation of the superior collicular map of auditory space. We attribute this effect to the masking, by the omnidirectional broad-band noise, of discrete localized auditory stimuli. Cues deriving from these latter stimuli would appear to be necessary for the elaboration of the map of auditory space. This auditory experience operates during a 4 day crucial developmental period from 26 to 30 DAB. This is the same developmental time window as that during which visual experience is required for the construction of the map.     

Spectral envelope coding in cat primary auditory cortex: linear and non‐linear effects of stimulus characteristics

Electrophysiological studies in mammal primary auditory cortex have demonstrated neuronal tuning and cortical spatial organization based upon spectral and temporal qualities of the stimulus including: its frequency, intensity, amplitude modulation and frequency modulation. Although communication and other behaviourally relevant sounds are usually complex, most response characterizations have used tonal stimuli. To better understand the mechanisms necessary to process complex sounds, we investigated neuronal responses to a specific class of broadband stimuli, auditory gratings or ripple stimuli, and compared the responses with single tone responses. Ripple stimuli consisted of 150–200 frequency components with the intensity of each component adjusted such that the envelope of the frequency spectrum is sinusoidal. It has been demonstrated that neurons are tuned to specific characteristics of those ripple stimulus including the intensity, the spacing of the peaks, and the location of the peaks and valleys (C. E. Schreiner and B. M. Calhoun, Auditory Neurosci. 1994; 1 : 39–61). Although previous results showed that neuronal response strength varied with the intensity and the fundamental frequency of the stimulus, it is shown here that the relative response to different ripple spacings remains essentially constant with changes in the intensity and the fundamental frequency. These findings support a close relationship between pure-tone receptive fields and ripple transfer functions. However, variations of other stimulus characteristics, such as spectral modulation depth, result in non-linear alterations in the ripple transformation. The processing between the basilar membrane and the primary auditory cortex of broadband stimuli appears generally to be non-linear, although specific stimulus qualities, including the phase of the spectral envelope, are processed in a nearly linear manner.     

Population-Wide Bias of Surround Suppression in Auditory Spatial Receptive Fields of the Owl's Midbrain

The physical arrangement of receptive fields (RFs) within neural structures is important for local computations. Nonuniform distribution of tuning within populations of neurons can influence emergent tuning properties, causing bias in local processing. This issue was studied in the auditory system of barn owls. The owl's external nucleus of the inferior colliculus (ICx) contains a map of auditory space in which the frontal region is overrepresented. We measured spatiotemporal RFs of ICx neurons using spatial white noise. We found a population-wide bias in surround suppression such that suppression from frontal space was stronger. This asymmetry increased with laterality in spatial tuning. The bias could be explained by a model of lateral inhibition based on the overrepresentation of frontal space observed in ICx. The model predicted trends in surround suppression across ICx that matched the data. Thus, the uneven distribution of spatial tuning within the map could explain the topography of time-dependent tuning properties. This mechanism may have significant implications for the analysis of natural scenes by sensory systems.