Encoding properties of auditory neurons in the brain of a soniferous damselfish: response to simple tones and complex conspecific signals

The fish auditory system encodes important acoustic stimuli used in social communication, but few studies have examined response properties of central auditory neurons to natural signals. We determined the features and responses of single hindbrain and midbrain auditory neurons to tone bursts and playbacks of conspecific sounds in the soniferous damselfish, Abudefduf abdominalis. Most auditory neurons were either silent or had slow irregular resting discharge rates <20 spikes s⁻¹. Average best frequency for neurons to tone stimuli was ~130 Hz but ranged from 80 to 400 Hz with strong phase-locking. This low-frequency sensitivity matches the frequency band of natural sounds. Auditory neurons were also modulated by playbacks of conspecific sounds with thresholds similar to 100 Hz tones, but these thresholds were lower than that of tones at other test frequencies. Thresholds of neurons to natural sounds were lower in the midbrain than the hindbrain. This is the first study to compare response properties of auditory neurons to both simple tones and complex stimuli in the brain of a recently derived soniferous perciform that lacks accessory auditory structures. These data demonstrate that the auditory fish brain is most sensitive to the frequency and temporal components of natural pulsed sounds that provide important signals for conspecific communication.     

Studies of directional sensitivity of neurons in the cat primary auditory cortex

A set of impulsive transient signals has been synthesized for earphone delivery whose waveform and amplitude spectra, measured at the eardrum, mimic those of sounds arriving from a free-field source. The complete stimulus set forms a "virtual acoustic space" (VAS) for the cat. VAS stimuli are delivered via calibrated earphones sealed into the external meatus in cats under barbiturate anesthesia. Neurons recorded extracellularly in primary (AI) auditory cortex exhibit sensitivity to the direction of sound in VAS. The aggregation of effective sound directions forms a virtual space receptive field (VSRF). At about 20 dB above minimal threshold, VSRFs recorded in otherwise quiet and anechoic space fall into categories based on spatial dimension and location. The size, shape and location of VSRFs remain stable over many hours of recording and are found to be shaped by excitatory and inhibitory interactions of activity arriving from the two ears. Within the VSRF response latency and strength vary systematically with stimulus direction. In an ensemble of such neurons these functional gradients provide information about stimulus direction, which closely accounts for a human listener's spatial acuity. Raising stimulus intensity, introducing continuous background noise or presenting a conditioning stimulus all influence the extent of the VSRF but leave intact the gradient structure of the field. These and other findings suggest that such functional gradients in VSRFs of ensembles of AI neurons are instrumental in coding sound direction and robust enough to overcome interference from competing environmental sounds.     

Frequency and space representation in the primary auditory cortex of the frequency modulating batEptesicus fuscus

1. Frequency and space representation in the auditory cortex of the big brown bat, Eptesicus fuscus, were studied by recording responses of 223 neurons to acoustic stimuli presented in the bat's frontal auditory space. 2. The majority of the auditory cortical neurons were recorded at a depth of less than 500 microns with a response latency between 8 and 20 ms. They generally discharged phasically and had nonmonotonic intensity-rate functions. The minimum threshold, (MT) of these neurons was between 8 and 82 dB sound pressure level (SPL). Half of the cortical neurons showed spontaneous activity. All 55 threshold curves are V-shaped and can be described as broad, intermediate, or narrow. 3. Auditory cortical neurons are tonotopically organized along the anteroposterior axis of the auditory cortex. High-frequency-sensitive neurons are located anteriorly and low-frequency-sensitive neurons posteriorly. An overwhelming majority of neurons were sensitive to a frequency range between 30 and 75 kHz. 4. When a sound was delivered from the response center of a neuron on the bat's frontal auditory space, the neuron had its lowest MT. When the stimulus amplitude was increased above the MT, the neuron responded to sound delivered within a defined spatial area. The response center was not always at the geometric center of the spatial response area. The latter also expanded with stimulus amplitude. High-frequency-sensitive neurons tended to have smaller spatial response areas than low-frequency-sensitive neurons. 5. Response centers of all 223 neurons were located between 0 degrees and 50 degrees in azimuth, 2 degrees up and 25 degrees down in elevation of the contralateral frontal auditory space. Response centers of auditory cortical neurons tended to move toward the midline and slightly downward with increasing best frequency. 6. Auditory space representation appears to be systematically arranged according to the tonotopic axis of the auditory cortex. Thus, the lateral space is represented posteriorly and the middle space anteriorly. Space representation, however, is less systematic in the vertical direction. 7. Auditory cortical neurons are columnarly organized. Thus, the BFs, MTs, threshold curves, azimuthal location of response centers, and auditory spatial response areas of neurons sequentially isolated from an orthogonal electrode penetration are similar.     

Tangential medulla neurons in the mothManduca sexta. Structure and responses to optomotor stimuli

InManduca sexta, large tangential cells connect the medulla via the lobula valley (LoV) tract to the midbrain and the contralateral medulla. Tract neurons have been stained and recorded to determine their responses to optomotor stimulation. Neurons in the LoV-tract comprise a physiologically and anatomically heterogeneous population:

1. Motion insensitive medulla tangential (Mt) neurons arise from cell bodies in the ventral rind. Heterolateral cells arborize massively in both medullae and one or both halves of the midbrain. Mt-neurons respond to changes in light intensity. Physiological and anatomical evidence argues for their monocularity and transmission from the medulla on the side of the soma to the central brain and the contralateral medulla.
2. Motion sensitive neurons with cell bodies behind the protocerebral bridge connect the midbrain to the ipsior contralateral medulla. Direction-selective responses are characterized by excitation to motion in the preferred and inhibition in the opposite direction with maxima either in a horizontal or vertical direction. Peak values appear at contrast frequencies of appr. 3/s. The results suggest that these neurons are binocular and relay information from the midbrain to the medulla. They have been labelled as centrifugal medulla tangential (cMt) neurons.

The possible roles for tract neurons in visually guided behaviour are discussed.     

Spectrotemporal Response Properties of Core Auditory Cortex Neurons in Awake Monkey

So far, most studies of core auditory cortex (AC) have characterized the spectral and temporal tuning properties of cells in non-awake, anesthetized preparations. As experiments in awake animals are scarce, we here used dynamic spectral-temporal broadband ripples to study the properties of the spectrotemporal receptive fields (STRFs) of AC cells in awake monkeys. We show that AC neurons were typically most sensitive to low ripple densities (spectral) and low velocities (temporal), and that most cells were not selective for a particular spectrotemporal sweep direction. A substantial proportion of neurons preferred amplitude-modulated sounds (at zero ripple density) to dynamic ripples (at non-zero densities). The vast majority (>93%) of modulation transfer functions were separable with respect to spectral and temporal modulations, indicating that time and spectrum are independently processed in AC neurons. We also analyzed the linear predictability of AC responses to natural vocalizations on the basis of the STRF. We discuss our findings in the light of results obtained from the monkey midbrain inferior colliculus by comparing the spectrotemporal tuning properties and linear predictability of these two important auditory stages.     

A biologically plausible acoustic motion detection neural network

In this paper we present an acoustic motion detection system to be used in a small mobile robot. While the first purpose of the system has been to be a reliable computational implementation, cheap enough to be built in hardware, effort has also been taken to construct a biologically plausible solution. The motion detector consists of a neural network composed of motion-direction sensitive neurons with a preferred direction and a preferred region of the azimuth. The system was designed to produce a higher response when stimulated by motion in the preferred direction than in the null direction and that is in fact what the system does, which means that, as desired, the system can detect motion and distinguish its direction.     

Corticofugal modulation of initial neural processing of sound information from the ipsilateral ear in the mouse

Background

Cortical neurons implement a high frequency-specific modulation of subcortical nuclei that includes the cochlear nucleus. Anatomical studies show that corticofugal fibers terminating in the auditory thalamus and midbrain are mostly ipsilateral. Differently, corticofugal fibers terminating in the cochlear nucleus are bilateral, which fits to the needs of binaural hearing that improves hearing quality. This leads to our hypothesis that corticofugal modulation of initial neural processing of sound information from the contralateral and ipsilateral ears could be equivalent or coordinated at the first sound processing level.

Methodology/Principal Findings

With the focal electrical stimulation of the auditory cortex and single unit recording, this study examined corticofugal modulation of the ipsilateral cochlear nucleus. The same methods and procedures as described in our previous study of corticofugal modulation of contralateral cochlear nucleus were employed simply for comparison. We found that focal electrical stimulation of cortical neurons induced substantial changes in the response magnitude, response latency and receptive field of ipsilateral cochlear nucleus neurons. Cortical stimulation facilitated auditory response and shortened the response latency of physiologically matched neurons whereas it inhibited auditory response and lengthened the response latency of unmatched neurons. Finally, cortical stimulation shifted the best frequencies of cochlear neurons towards those of stimulated cortical neurons.

Conclusion

Our data suggest that cortical neurons enable a high frequency-specific remodelling of sound information processing in the ipsilateral cochlear nucleus in the same manner as that in the contralateral cochlear nucleus.     

Neural processing of auditory looming in the human brain

Acoustic intensity change, along with interaural, spectral, and reverberation information, is an important cue for the perception of auditory motion. Approaching sound sources produce increases in intensity, and receding sound sources produce corresponding decreases. Human listeners typically overestimate increasing compared to equivalent decreasing sound intensity and underestimate the time to contact of approaching sound sources. These characteristics could provide a selective advantage by increasing the margin of safety for response to looming objects. Here, we used dynamic intensity and functional magnetic resonance imaging to examine the neural underpinnings of the perceptual priority for rising intensity. We found that, consistent with activation by horizontal and vertical auditory apparent motion paradigms, rising and falling intensity activated the right temporal plane more than constant intensity. Rising compared to falling intensity activated a distributed neural network subserving space recognition, auditory motion perception, and attention and comprising the superior temporal sulci and the middle temporal gyri, the right temporoparietal junction, the right motor and premotor cortices, the left cerebellar cortex, and a circumscribed region in the midbrain. This anisotropic processing of acoustic intensity change may reflect the salience of rising intensity produced by looming sources in natural environments.     

Different Stimuli,Different Spatial Codes: A Visual Map and an Auditory Rate Code for Oculomotor Space in the Primate Superior Colliculus

Maps are a mainstay of visual, somatosensory, and motor coding in many species. However, auditory maps of space have not been reported in the primate brain. Instead, recent studies have suggested that sound location may be encoded via broadly responsive neurons whose firing rates vary roughly proportionately with sound azimuth. Within frontal space, maps and such rate codes involve different response patterns at the level of individual neurons. Maps consist of neurons exhibiting circumscribed receptive fields, whereas rate codes involve open-ended response patterns that peak in the periphery. This coding format discrepancy therefore poses a potential problem for brain regions responsible for representing both visual and auditory information. Here, we investigated the coding of auditory space in the primate superior colliculus(SC), a structure known to contain visual and oculomotor maps for guiding saccades. We report that, for visual stimuli, neurons showed circumscribed receptive fields consistent with a map, but for auditory stimuli, they had open-ended response patterns consistent with a rate or level-of-activity code for location. The discrepant response patterns were not segregated into different neural populations but occurred in the same neurons. We show that a read-out algorithm in which the site and level of SC activity both contribute to the computation of stimulus location is successful at evaluating the discrepant visual and auditory codes, and can account for subtle but systematic differences in the accuracy of auditory compared to visual saccades. This suggests that a given population of neurons can use different codes to support appropriate multimodal behavior.     

Directional asymmetry of the zebrafish epithalamus guides dorsoventral innervation of the midbrain target

The zebrafish epithalamus, consisting of the pineal complex and flanking dorsal habenular nuclei, provides a valuable model for exploring how left-right differences could arise in the vertebrate brain. The parapineal lies to the left of the pineal and the left habenula is larger, has expanded dense neuropil, and distinct patterns of gene expression from the right habenula. Under the influence of Nodal signaling, positioning of the parapineal sets the direction of habenular asymmetry and thereby determines the left-right origin of habenular projections onto the midbrain target, the interpeduncular nucleus (IPN). In zebrafish with parapineal reversal, neurons from the left habenula project to a more limited ventral IPN region where right habenular axons would normally project. Conversely, efferents from the right habenula adopt a more extensive dorsoventral IPN projection pattern typical of left habenular neurons. Three members of the leftover-related KCTD (potassium channel tetramerization domain containing) gene family are expressed differently by the left and right habenula, in patterns that define asymmetric subnuclei. Molecular asymmetry extends to protein levels in habenular efferents, providing additional evidence that left and right axons terminate within different dorsoventral regions of the midbrain target. Laser-mediated ablation of the parapineal disrupts habenular asymmetry and consequently alters the dorsoventral distribution of innervating axons. The results demonstrate that laterality of the dorsal forebrain influences the formation of midbrain connections and their molecular properties.     

Similarities of FM and AM receptive space of single units at the auditory midbrain

Complex sounds, including human speech, contain time-varying signals like frequency modulation (FM) and amplitude modulation (AM) components. In spite of various attempts to characterize their neuronal coding in the mammalian auditory systems, a unified view of their responses has not been reached. We compared FM and AM coding in terms of receptive space with reference to the input-output relationship of the underlying neural circuits. Using extracellular recording, single unit responses to a novel stimulus (i.e. random AM or FM tone) were obtained at the auditory midbrain of the anesthetized rat. Responses could be classified into three general types, corresponding to selective sensitivity to one of the following aspects of the modulation: (a) steady state, (b) dynamic state, or (c) steady-and-dynamic states. Such response typing was basically similar between FM and AM stimuli. Furthermore, the receptive space of each unit could be characterized in a three-dimensional Cartesian co-ordinate system formed by three modulation parameters: velocity, range and intensity. This representation applies to both FM and AM responses. We concluded that the FM and AM codings are very similar at the auditory midbrain and may likely involve similar neural mechanisms.     

Responses of midbrain auditory neurons in rats to FM and AM tones presented simultaneously

Speech and other communication signals contain components of frequency and amplitude modulations (FM, AM) that often occur together. Auditory midbrain (or inferior colliculus, IC) is an important center for coding time-varying features of sounds. It remains unclear how IC neurons respond when FM and AM stimuli are both presented. Here we studied IC neurons in the urethane-anesthetized rats when animals were simultaneously stimulated with FM and AM tones. Of 122 units that were sensitive to the dual stimuli, the responses could be grossly divided into two types: one that resembled the respective responses to FM or AM stimuli presented separately ("simple" sensitivity, 45% of units), and another that appeared markedly different from their respective responses to FM or AM tones ("complex" sensitivity, 55%). These types of combinational sensitivities were further correlated with individual cell's frequency tuning pattern (response area) and with their common response pattern to FM and AM sounds. Results suggested that such combinational sensitivity could reflect local synaptic interactions on IC neurons and that the neural mechanisms could underlie more developed sensitivities to acoustic combinations found at the auditory cortex.     

Orientation tuning of motion-sensitive neurons shaped by vertical-horizontal network interactions

We measured the orientation tuning of two neurons of the fly lobula plate (H1 and H2 cells) sensitive to horizontal image motion. Our results show that H1 and H2 cells are sensitive to vertical motion, too. Their response depended on the position of the vertically moving stimuli within their receptive field. Stimulation within the frontal receptive field produced an asymmetric response: upward motion left the H1/H2 spike frequency nearly unaltered while downward motion increased the spike frequency to about 40% of their maximum responses to horizontal motion. In the lateral parts of their receptive fields, no such asymmetry in the responses to vertical image motion was found. Since downward motion is known to be the preferred direction of neurons of the vertical system in the lobula plate, we analyzed possible interactions between vertical system cells and H1 and H2 cells. Depolarizing current injection into the most frontal vertical system cell (VS1) led to an increased spike frequency, hyperpolarizing current injection to a decreased spike frequency in both H1 and H2 cells. Apart from VS1, no other vertical system cell (VS2-8) had any detectable influence on either H1 or H2 cells. The connectivity of VS1 and H1/H2 is also shown to influence the response properties of both centrifugal horizontal cells in the contralateral lobula plate, which are known to be postsynaptic to the H1 and H2 cells. The vCH cell receives additional input from the contralateral VS2-3 cells via the spiking interneuron V1.     

Single cell responses from the optic tectum of the zebra finch (Taeniopygia guttata castanotis Gould)

Responses of neurons of the optic tectum, the prominent, highly laminated mesencephalic station of the tectofugal visual pathway in birds, to computer-generated and other visual stimuli were examined in zebra finches. Our study shows that the contralateral retina projects to the tectum in topographic order. The representation of the visual field is tilted against the horizon by 22°. The representation of the contralateral hemifield extends to the ipsilateral side by 15°. Most neurons have receptive fields with excitatory centres of different shapes and inhibitory surround. A new type of neuronal receptive field is described which has an excitatory centre and a surround which is movement sensitive and preferably excited by very small spots. The first type of neurons is mostly located in upper tectal layers, the latter only in deeper layers. Excitatory centre sizes increase with depth, and there is a tendency of smaller receptive fields in the foveal region. The representation of the frontal visual field does not show specializations which could be expected if it were used for fixation of grain during pecking. Our results are in accordance with previous behavioural experiments. Accepted: 30 April 1999     

Response of Cat Ventrolateral Spinal Axons to an Itch-Producing Stimulus (Cowhage)

A comparison was made between different categories of mechanically sensitive, ventrolateral spinal axons to assess their sensitivity to the itch-producing substance cowhage. Of 52 wide-dynamic-range (WDR) units, 17 had contralateral, 22 had ipsilateral, and 13 had bilateral receptive fields. Of the 5 low-threshold units, 1 had an ipsilateral receptive field and the remainder were bilateral. Among the high-threshold units, 10 were contralateral, 6 ipsilateral, and 5 bilateral. Although there was no evidence of cowhage sensitivity in either low- or high-threshold spinal axons, neurons with WDR properties were reactive to cowhage. WDR neurons were subclassified on the basis of their resting discharge pattern as having intermittent, continuous, or no resting discharge. WDR units with an intermittent pattern of resting discharge demonstrated a significant sensitivity to active cowhage and hence might be regarded as pruritogen-responsive spinal axons. Inactive cowhage was used as a control stimulus. In some WDR units with large receptive fields, there were observations suggesting convergence of chemoreceptive and mechanoreceptive inputs, which produced inhibitory as well as excitatory effects.     

Bilateral collicular interaction: modulation of auditory signal processing in amplitude domain

In the ascending auditory pathway, the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from many lower auditory nuclei, intrinsic projections within the IC, contralateral IC through the commissure of the IC and from the auditory cortex. All these connections make the IC a major center for subcortical temporal and spectral integration of auditory information. In this study, we examine bilateral collicular interaction in modulating amplitude-domain signal processing using electrophysiological recording, acoustic and focal electrical stimulation. Focal electrical stimulation of one (ipsilateral) IC produces widespread inhibition (61.6%) and focused facilitation (9.1%) of responses of neurons in the other (contralateral) IC, while 29.3% of the neurons were not affected. Bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited IC neurons but produces opposite effects on the response of facilitated IC neurons. These two groups of neurons are not separately located and are tonotopically organized within the IC. The modulation effect is most effective at low sound level and is dependent upon the interval between the acoustic and electric stimuli. The focal electrical stimulation of the ipsilateral IC compresses or expands the rate-level functions of contralateral IC neurons. The focal electrical stimulation also produces a shift in the minimum threshold and dynamic range of contralateral IC neurons for as long as 150 minutes. The degree of bilateral collicular interaction is dependent upon the difference in the best frequency between the electrically stimulated IC neurons and modulated IC neurons. These data suggest that bilateral collicular interaction mainly changes the ratio between excitation and inhibition during signal processing so as to sharpen the amplitude sensitivity of IC neurons. Bilateral interaction may be also involved in acoustic-experience-dependent plasticity in the IC. Three possible neural pathways underlying the bilateral collicular interaction are discussed.     

Response of cat ventrolateral spinal axons to an itch-producing stimulus (cowhage).

A comparison was made between different categories of mechanically sensitive, ventrolateral spinal axons to assess their sensitivity to the itch-producing substance cowhage. Of 52 wide-dynamic-range (WDR) units, 17 had contralateral, 22 had ipsilateral, and 13 had bilateral receptive fields. Of the 5 low-threshold units, 1 had an ipsilateral receptive field and the remainder were bilateral. Among the high-threshold units, 10 were contralateral, 6 ipsilateral, and 5 bilateral. Although there was no evidence of cowhage sensitivity in either low- or high-threshold spinal axons, neurons with WDR properties were reactive to cowhage. WDR neurons were subclassified on the basis of their resting discharge pattern as having intermittent, continuous, or no resting discharge. WDR units with an intermittent pattern of resting discharge demonstrated a significant sensitivity to active cowhage and hence might be regarded as pruritogen-responsive spinal axons. Inactive cowhage was used as a control stimulus. In some WDR units with large receptive fields, there were observations suggesting convergence of chemoreceptive and mechanoreceptive inputs, which produced inhibitory as well as excitatory effects.     

A system of insect neurons sensitive to horizontal and vertical image motion connects the medulla and midbrain

Summary The response properties and gross morphologies of neurons that connect the medulla and midbrain in the butterfly Papilio aegeus are described. The neurons presented give direction-selective responses, i.e. they are excited by motion in the preferred direction and the background activity of the cells is inhibited by motion in the opposite, null, direction. The neurons are either maximally sensitive to horizontal motion or to slightly off-axis vertical upward or vertical downward motion, when tested in the frontal visual field. The responses of the cells are dependent on the contrast frequency of the stimulus with peak values at 5–10 Hz. The receptive fields of the medulla neurons are large and are most sensitive in the frontal visual field. Examination of the local and global properties of the receptive fields of the medulla neurons indicates that (1) they are fed by local elementary motion-detectors consistent with the correlation model and (2) there is a non-linear spatial integration mechanism in operation.     

Coding of sound location and frequency in the auditory midbrain of diurnal birds of prey,families accipitridae and falconidae

Summary The coding of sound frequency and location in the avian auditory midbrain nucleus (nMLD) was examined in three diurnal raptors: the brown falcon (Falco berigora), the swamp harrier (Circus aeruginosus) and the brown goshawk (Accipiter fasciatus). Previously this nucleus has been studied with free field stimuli in only one other species, the barn owl (Tyto alba).We found some parallels between the organisation of nMLD in the diurnal raptors and that reported in the barn owl in that the central region of nMLD was tonotopically organised and contained cells that did not encode location, and the lateral region (nMLDl) contained cells which were sensitive to stimulus position. However, unlike the barn owl, which has units with circumscribed receptive fields, cells sensitive to stimulus location had large receptive fields which were restricted in azimuth but not in elevation (hemifield units). Such cells could not provide an acoustic space map in which both azimuthal and elevational dimensions were represented, but there was a tendency for units with contralateral borders to be found superficially, and those with ipsilateral borders to be found deep, in nMLDl. Hemifield units displayed receptive field properties consistent with the directional properties of the tympana in the presence of sound transmission through the interaural canal, if there is a central mechanism which is sensitive to interaural intensity differences.Abbreviations nMLD nucleus mesencephalicus lateralis pars dorsalis - SPL sound pressure level re 20 Pa - nMLDl lateral region of nMLD - ICC central nucleus of the inferior colliculus - ICX external nucleus of the inferior colliculus - IID interaural intensity difference - EI excitatory inhibitory     

Auditory spatial acuity approximates the resolving power of space-specific neurons

The relationship between neuronal acuity and behavioral performance was assessed in the barn owl (Tyto alba), a nocturnal raptor renowned for its ability to localize sounds and for the topographic representation of auditory space found in the midbrain. We measured discrimination of sound-source separation using a newly developed procedure involving the habituation and recovery of the pupillary dilation response. The smallest discriminable change of source location was found to be about two times finer in azimuth than in elevation. Recordings from neurons in its midbrain space map revealed that their spatial tuning, like the spatial discrimination behavior, was also better in azimuth than in elevation by a factor of about two. Because the PDR behavioral assay is mediated by the same circuitry whether discrimination is assessed in azimuth or in elevation, this difference in vertical and horizontal acuity is likely to reflect a true difference in sensory resolution, without additional confounding effects of differences in motor performance in the two dimensions. Our results, therefore, are consistent with the hypothesis that the acuity of the midbrain space map determines auditory spatial discrimination.