Frontal Auditory Space Research Articles

Does visual experience influence the spatial distribution of auditory attention?

Sighted individuals are less accurate and slower to localize sounds coming from the peripheral space than sounds coming from the frontal space. This specific bias in favour of the frontal auditory space seems reduced in early blind individuals, who are particularly better than sighted individuals at localizing sounds coming from the peripheral space. Currently, it is not clear to what extent this bias in the auditory space is a general phenomenon or if it applies only to spatial processing (i.e. sound localization). In our approach we compared the performance of early blind participants with that of sighted subjects during a frequency discrimination task with sounds originating either from frontal or peripheral locations. Results showed that early blind participants discriminated faster than sighted subjects both peripheral and frontal sounds. In addition, sighted subjects were faster at discriminating frontal sounds than peripheral ones, whereas early blind participants showed equal discrimination speed for frontal and peripheral sounds. We conclude that the spatial bias observed in sighted subjects reflects an unbalance in the spatial distribution of auditory attention resources that is induced by visual experience.

Encoding of Sound Spatial Information by Neurons in The Rat Primary Auditory Cortex*

Many previous studies have shown that auditory cortical neurons are sensitive to sound spatial information, however, the mechanism of sound spatial coding is still not fully understood. Until now, detail studies on sound spatial coding have not been reported in the rat primary auditory cortex. Using electrophysiological technique, spatial response areas of 151 neurons in the rat primary auditory cortex were investigated. The relationships between spike counts and average first-spike latencies in the spatial response areas were analyzed. The results showed that, the majority (52.32%) of cortical neurons exhibited contralateral preference in the frontal auditory space whereas other neurons exhibited ipsilateral preference (18.54%) and midline preference (18.54%), and only a few neurons were included in the category of omnidirection (3.31%) and complex (7.28%). For the majority of cortical neurons, the arithmetic center of the preferred spatial area were distributed in the up and middle portion of the contralateral space relative to the recording side. Most neurons responded strongly to stimuli from their preferred space with shorter average first-spike latencies, and responded weakly to stimuli from non-preferred space with longer average latencies. In the spatial response area, the spike counts were negatively correlated with average first-spike latencies. The auditory cortex might use the information of both spike counts and average response time to code sound spatial information.

Azimuth-dependent recovery cycle affects directional selectivity of bat inferior collicular neurons determined with sound pulses within a pulse train

In our previous study, we have shown that the recovery cycle of most neurons in the inferior colliculus (IC) of the big brown bat, Eptesicus fuscus, is typically longer at ipsilateral azimuth than at contralateral azimuth under free-field stimulation conditions. The present study is to test the hypothesis that this azimuth-dependent recovery cycle may contribute to the variation of directional selectivity of IC neurons with sequential presented sound pulses within a pulse train. A 300-ms pulse train containing nine sound pulses of 4-ms with an inter-pulse interval of 33.3 ms was delivered at several selected azimuthal angles between ±80° lateral in the frontal auditory space of a bat. A family of nine directional selectivity curves was plotted with a neuron's number of impulses in response to each individual pulse against the azimuthal angles. The type and sharpness of these directional selectivity curves were then compared in relation to pulse position within the pulse train. All 675 directional selectivity curves obtained from 75 IC neurons could be described as directionally selective (423, 63%), hemifield (220, 32%), or non-directional (32, 5%). The directional selectivity curves of 45 (60%) neurons did not vary with pulse position. However, those of the remaining neurons (30, 40%) changed from one type to another such that the number of neurons with directionally selective curves progressively increased and the number of neurons with hemifield and non-directional selectivity curves decreased with increasing pulse position within the pulse train. Among 68 IC neurons whose directional selectivity curves were compared quantitatively, directional selectivity determined with sequentially presented sound pulses significantly increased in 38 (56%) neurons; decreased in 18 (26%) neurons but did not change in 12 (18%) neurons. This change of directional selectivity was due to the variation in recovery cycle of these IC neurons with azimuthal angle as we hypothesized.

Distribution of auditory motion-direction sensitive neurons in the barn owl's midbrain.

Barn owls have neurons sensitive to acoustic motion-direction in the midbrain. We report here that acoustic motion-direction sensitive neurons with receptive-field centres in frontal auditory space are not randomly distributed. In the inferior colliculus and optic tectum in the left (right) brain, the responses of about two-thirds of the motion-direction sensitive neurons were sensitive to clockwise (counter-clockwise) motion. The midbrain contains maps of auditory space that represent about 15 degrees of ipsilateral and all of contralateral space. Since a similar bias in motion-direction sensitivity was observed for neurons with receptive-field centres in ipsilateral as well as for neurons with receptive fields centres in contralateral auditory space, the brain side at which a motion-direction sensitive neuron was recorded was a more important predictor for the preferred direction of a cell than the spatial direction of the centre of the receptive field. Within one dorso-ventral electrode pass motion-direction sensitivity typically stayed constant suggesting a clustered or even a columnar-like organization. We hypothesize from these distributions that the right brain is important for orientating movements to the left hemisphere and vice versa.

Cytoarchitecture and Sound Activated Responses in the Auditory Cortex of the Big Brown Bat, Eptesicus fuscus

Under free field and closed-system stimulation conditions, we studied the frequency threshold curves, auditory spatial sensitivity and binaurality of neurons in the primary auditory cortex (AC) of the big brown bat, Eptesicus fuscus. All 298 recorded AC neurons discharged phasically. They were recorded at depths less than 1,000 μm with response latencies of 7–25 ms, best frequencies (BFs) of 28–97 kHz and minimum thresholds (MTs) of 8–90 dB SPL. They received excitatory inputs from the contralateral ear and either excitatory (EE) or inhibitory (EI) inputs from the ipsilateral ear. These cortical neurons were tonotopically organized along the anteroposterior axis of the AC. High best frequency neurons were located anteriorly and low best frequency neurons posteriorly. They were most sensitive to sounds delivered from a restricted region of the contralateral frontal auditory space (0°-50° in azimuth and 2° up, 15° down in elevation). Frontal auditory space representation appears to be systematically arranged according to the tonotopic axis such that the lateral space is represented posteriorly and the middle space anteriorly. Cortical neurons sequentially isolated from an orthogonally penetrated electrode had similar frequency threshold curves, BFs, MTs, points of maximal auditory spatial sensitivity and binaurality. The EE and EI columns are organized concentrically such that the small number of centrally located EE columns were surrounded by an overwhelming number of El columns. Using Nissl and Golgi stains as well as c-fos immunocytochemistry, we studied the Cytoarchitecture, cell types and sound elicited Fos-like immunoreactivity in the primary AC of this bat species. The primary AC of this bat species can be described into molecular (137 μm), external granular (55 μm), external pyramidal (95 μm), internal granular (102 μm), internal pyramidal (191 μm) and multiform (120 μm) layers. The main type of cells distributed among these six layers are the small, medium and large pyramidal cells. Others include the stellate, horizontal, granular, fusiform, basket, and Martinotii cells. When stimulated with 30 kHz and 79 dB SPL sounds under natural conditions, bilaterally and symmetrically distributed Fos-like immunoreactive neurons were observed in about 20% of neurons in each AC. When stimulated under monaurally plugged conditions, 39–48% more of Fos-like immunoreactive neurons were observed in the ipsilateral AC. This finding supports the fact that the primary AC receives auditory inputs mainly from the contralateral ear.

Neurons in the inferior colliculus, auditory cortex and pontine nuclei of the FM bat, Eptesicus fuscus respond to pulse repetition rate differently

Single-neuron responses to pulse repetition rate in the inferior colliculus, auditory cortex and pontine nuclei of the FM bat, Eptesicus fuscus were studied under free-field stimulation conditions. The best frequency (BF) and minimum threshold (MT) of each neuron were first determined with a 4 ms pulse broadcast from a specific point (response center) of the bat's frontal auditory space at which the neuron had maximal spatial sensitivity. The neuron's intensity-rate function was then studied with a 4 ms BF pulse delivered at 10 dB increments above its MT in order to determine the best intensity to which the neuron discharged maximally. The neuron's discharge pattern and number of impulses to 32 trials of 300 ms train stimuli, which consisted of different number of 4 ms BF and best intensity pulses (1, 2, 3, 8, 12, 19, 24, 29 pulses/train) and delivered at an interpulse interval of 1000, 250, 170, 100, 40, 25, 15, 12 and 10 ms (i.e. at a pulse repetition rate of 1, 4, 6, 10, 25, 40, 67, 83, 100 pulses/s), were sequentially recorded. All neurons recorded from the inferior colliculus, auditory cortex and pontine nuclei discharged phasically (1–3 impulses) but they responded to the pulse repetition rate in different manners. More than 63% of 38 inferior collicular and 65 pontine neurons studied discharged impulses to each pulse within a train stimulus when the pulse repetition rate was up to 40 pulses/s. Although the number of neurons showing such a one-to-one following response decreased with increasing pulse repetition rate, at least 20% of neurons still maintained such a response pattern even at a pulse repetition rate of 100 pulses/s. In contrast, responses of 60% of 36 cortical neurons followed the pulse repetition rate only up to 10 pps beyond which all but one discharged impulses to the first pulse of a train stimulus. We suggest that the different discharge pattern to pulse repetition rate among individual neurons from these three brain centers is primarily due to their different recovery cycles.

Auditory response properties and spatial response areas of single neurons in the pontine nuclei of the big brown bat, Eptesicus fuscus

Using free-field acoustic stimulation conditions, we studied the response properties and spatial sensitivity of 146 pontine neurons of the big brown bat, Eptesicus fuscus. The best frequency (BF) and minimum threshold (MT) of a pontine neuron were first determined with a sound broadcast from a loudspeaker placed ahead of the bat. A BF sound was delivered from the loudspeaker as it moved across the frontal auditory space in order to locate the response center at which the neuron had its lowest MT. Then the basic response properties of the neuron to a sound delivered from the response center were studied. As in inferior collicular and auditory cortical neurons, pontine neurons can be characterized as phasic responders, phasic bursters and tonic responders. They have both monotonic and non-monotonic intensity-rate functions. However, most of them are broadly tuned as are cerebellar neurons. Auditory spatial sensitivity was studied for 144 pontine neurons. In 9 neurons, variation of MT with a BF sound delivered from several azimuthal and elevational angles along the horizontal and vertical planes crossing the neuron's response center was measured. In addition, variation in the number of impulses with several stimulus intensities at 10 dB increments above a neuron's MT delivered from each angle was also studied. The auditory spatial sensitivity of other pontine neurons was studied by measuring the response area of each neuron with stimulus intensities at 3, 5, 10, 15 or 40 dB above its lowest MT. The response areas of pontine neurons expanded asymmetrically with stimulus intensity, but the size of the response area was not correlated with either MT or BF. In half of the pontine neurons studied, the response area expanded greatly and eventually covered almost the entire frontal auditory space. The response areas of the other half of the pontine neurons only expanded to a restricted area of frontal auditory space. Two possible neural mechanisms underlying these two types of response areas are hypothesized. The response centers of all 144 neurons were located within a small area of the frontal auditory space. The locations of response centers of these neurons are not correlated with their BFs. The distribution pattern of these response centers is comparable to that of superior collicular and cerebellar neurons but is different from that of inferior collicular and auditory cortical neurons. The results of our study suggest that auditory information is integrated in the pontine nuclei before being further sent into the cerebellum.

Animal Sonar: Processes and Performance

<i>Animal Sonar: Processes and Performance</i>

Frequency and space representation in the inferior colliculus of the FM bat, Eptesicus fuscus

The tonotopic organization and spatial sensitivity of 217 inferior collicular (IC) neurons of Eptesicus fuscus were studied under free field stimulation conditions. Acoustic stimuli were delivered from a loudspeaker placed 21 cm ahead of the bat to determine the best frequency (BF) and minimum threshold (MT) of isolated IC neurons. A BF stimulus was then delivered as the loudspeaker was moved horizontally across the frontal auditory space of the bat to locate the best azimuthal angle (BAZ) at which the neuron had its lowest MT. The stimulus was then raised 3 dB above the lowest MT to determine the horizontal extent of the auditory space within which a sound could elicit responses from the neurons. This was done by moving the loudspeaker laterally at every 5 degrees or 10 degrees until the neuron failed to respond. These measurements also allowed us to redetermine the BAZ at which the neuron fired maximal number of impulses. Electrodes were placed evenly across the whole IC surface and IC neurons were sampled as many as possible within each electrode penetration. Tonotopic organization and spatial sensitivity were examined among all 217 IC neurons as a whole as well as among IC neurons sequentially sampled within individual electrode penetrations. The whole population of 217 IC neurons is organized tonotopically along the dorsoventral axis of the IC. Thus, low frequency neurons are mostly located dorsally and high frequency neurons ventrally with median frequency neurons intervening in between. The BAZ of these 217 IC neurons tend to shift from lateral to medial portions of the contralateral frontal auditory space with increasing BF.(ABSTRACT TRUNCATED AT 250 WORDS)

Frequency and space representation in the primary auditory cortex of the frequency modulating bat Eptesicus 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.

Auditory spatial sensitivity of inferior collicular neurons of echolocating bats

The sensitivity of 94 inferior collicular (IC) neurons of Eptesicus fuscu and Myotis lucifugus to spatial location of the acoustic stimulus were studied under free-field stimulus conditions. The best frequency (BF) and minimum threshold (MT) of each neuron were determined with sound delivered in front of the bat. Then the variation in discharge rate of the neuron was measured with a BF sound broadcast from a moving loudspeaker at different angular positions along the horizontal, vertical or diagonal plane of the frontal auditory space. A wide range of stimulus intensities above the MT of the neuron was used. Neurons were classified into 3 classes on the basis of their spatial sensitivity: (1) omnisensitive neurons (15%) were broadly tuned to sound delivered in the frontal auditory space and their responses did not show any correlation with sound location; (2) stimulus intensity-dependent neurons (28%) varied their discharge rates with sound location and intensity so that the peak of their spatial response profiles also varied with stimulus intensity; and (3) stimulus intensity-independent neurons (57%) varied their discharge rates only with sound location over a wide range of stimulus intensities so that their peak discharge always appeared at the same or a small range of angle. In most cases, the medial limbs of spatial sensitivity curve for these neurons were extremely sharp and congruent. By moving the loudspeaker along the horizontal, vertical and diagonal planes, it was possible to approximate the boundary of the spatial response area of a neuron. Most IC neurons responded to sound delivered within 20° ipsilateral, 60° contralateral, 45° up and 40° down of the frontal auditory space, confirming previous similar studies. In general, an increasing stimulus repetition rate appeared to sharpen the spatial sensitivity curve of a neuron. Conversely, an increasing moving velocity of the stimulus decreased its response. The possible role of these 3 classes of neurons in echolocation and neural mechanisms underlying the spatial sensitivity of these neurons is discussed.

Auditory space representation in the inferior colliculus of the FM bat, Eptesicus fuscus

The auditory spatial response areas of 333 inferior collicular (IC) neurons of Eptesicus fuscus were studied under free-field acoustic stimulus conditions. A stimulus was delivered from a loudspeaker placed 14 cm in front of a bat and the best frequency of an encountered neuron was determined. Then a best frequency (BF) stimulus was delivered as the loudspeaker was moved across the frontal auditory space to determine the response of the neuron. At the response center, the neuron had the lowest minimum threshold. The stimulus was then raised 3–15 dB above the lowest minimum threshold of the neuron and the spatial response area for each stimulus intensity was measured. The response center and spatial response area of a neuron measured with a one-octave downward-sweep FM stimulus were similar to those measured with the pure tone pulse. The spatial response area of a neuron expanded asymmetrically with the stimulus intensity. High BF neurons generally had smaller spatial response areas than low BF neurons had. All 333 response centers were located in the contralateral auditory space. Response centers of low neurons tended to be located laterally while those of high BF neurons were located medially. Although each neuron had a point of lowest minimum threslhold in the contralateral auditory space, the point-to-point representation of the auditory space was not systematically organized. This representation was not correlated with the recording sites of the neurons in the mediolateral, posteroanterior and dorsoventral axes of the IC.

Auditory spatial response areas of single neurons and space representation in the cerebellum of echo locating bats

Using free-field acoustic stimulation conditions, we studied the auditory spatial response areas of 242 cerebellar neurons of Eptesicus fuscus. A best frequency stimulus was delivered from a loudspeaker which was moved across the frontal auditory space in order to determine the response center of each cerebellar neuron. At the response center, the neuron had its lowest minimum threshold. The stimulus was then raised 5–15 dB above the lowest minimum threshold of each neuron and the spatial response area for each stimulus intensity was measured. The spatial response area of each neuron expanded asymmetrically with the stimulus intensity. The size of the spatial response area was not correlated with the minimum threshold, best frequency or recording depth of the neuron. The distribution of the best frequencies of single neurons was not correlated with their recording depths or minimum thresholds. The response centers of all cerebellar neurons were located within a small area of the central portion of the frontal auditory space suggesting that the cerebellum could play an effective role in orienting the bat toward the echo source within the frontal gaze during insect capture.

Pinna position affects the auditory space representation in the inferior colliculus of the FM bat, Eptesicus fuscus

Using free-field acoustic stimulus conditions, we studied the auditory space representation in the inferior colliculus (IC) of the big brown bat, Eptesicus fuscus, under different pinna positions. Stimuli were delivered from a loudspeaker placed 14 cm in front of the bat to determine the best frequency (BF) of an isolated neuron. A BF stimulus was then delivered as the loudspeaker was moved across the frontal auditory space of the bat to locate the response center of the neuron. At the response center, the neuron has its lowest minimum threshold (MT). The stimulus was then raised 5-dB above the lowest MT to measure the spatial response area. Both response center and spatial response area of each neuron were measured under different pinna positions. Variation in the response center and MT of each neuron under different pinna positions was determined and a possible reason for this variation was discussed. The variation in auditory space representation in the IC due to variation in pinna position is presented. We suggest that during echolocation a bat could make changes in its pinna position to create additional binaural disparity for accurate target localization.

Ear position affects the auditory space representation in the inferior colliculus of bats

Using free field acoustic stimulation conditions, the spatial response areas of single neurons and auditory space representation in the inferior colliculus (IC) of the big brown bat Eptesicus fuscus, was studied under different ear positions. A best frequency stimulus was delivered from the loudspeaker which was moved manually across the frontal auditory space of the bat to determine the response center of the neuron. At the response center, the neuron had its maximal directional sensitivity. The spatial response area of each neuron was determined for acoustic stimuli set at several intensity levels above the minimum threshold of the neuron. The spatial response areas of each IC neuron expanded unsymmetrically with the stimulus intensity. The size of the spatial response area was not correlated with the minimum threshold, best frequency, or recording depth of each neuron. Although each neuron had a point of maximal directional sensitivity, the point‐to‐point representation of the auditory space was not systematically organized. This representation was not correlated with the recording site of each neuron in the mediolateral, posteroanterior and dorsoventral axes of the IC. Both the response centers and spatial response areas of individual neurons varied with ear position but individual variations were complementary. It is likely that a mobile auditory space representation may provide the bat with versatility in maximizing the directional sensitivity of its echolocation system for accurate prey capture. [Work of Philip Jen supported by NIH.]