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J J Wenstrup

Publications and source records attributed to J J Wenstrup.

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Combination-sensitive neurons in the inferior colliculus.

We examined whether neurons in the inferior colliculus of the mustached bat (Pteronotus parnellii) are combination sensitive, responding to both low- and high-frequency components of the bat's sonar signal. These neurons, previously reported in the thalamus and cortex, analyze sonar target features including distance. Of 82 single units and 36 multiple units from the 58-112 kHz representations of the inferior colliculus, most (86%) displayed sensitivity to low-frequency sounds that was tuned in the range of the fundamental biosonar component (24-31 kHz). All histologically localized units were in the central nucleus of the inferior colliculus (ICC). There were two major types of combination-sensitive influences. Many neurons were facilitated by low-frequency sounds and selective for particular delays between the low- and high-frequency components. In other neurons, the low-frequency signal was inhibitory if presented simultaneously or a few milliseconds prior to the high-frequency signal. The results indicate that mechanisms creating specialized frequency comparisons and delay sensitivity in combination-sensitive neurons operate at the ICC or below. Since combination sensitivity or multipeaked tuning curves occur in the auditory systems of many species, ICC neurons in these animals may also respond to species-specific frequency combinations.

Acoustic Stimulation

Inputs to combination-sensitive neurons in the medial geniculate body of the mustached bat: the missing fundamental.

This study examined projections to combination-sensitive neurons in the medial geniculate body of the mustached bat. These specialized neurons respond to the combination of two temporally and spectrally distinct components of the bat's sonar pulse and echo, encoding target information. Combination-sensitive neurons respond to the bat's sonar fundamental, between 24-31 kHz, in conjunction with a higher harmonic signal. They are thought to be formed in the medial geniculate body (MGB) by convergent input from inferior colliculus representations of 24-31 kHz and higher frequencies. This study used anterograde and retrograde tract-tracing methods in conjunction with physiological recording to test this MGB convergence hypothesis. In anterograde tracing experiments, multiple deposits of two different tracers were placed in the central nucleus of the inferior colliculus (ICC), one tracer in the 24-31 kHz region and another in an ICC representation responding to a higher sonar harmonic. We found only limited overlap in the MGB labeling patterns of the two tracers, and little in many areas where combination-sensitive neurons are common. In retrograde tracing experiments, a single deposit of tracer was placed at a combination-sensitive recording site in the MGB. With the deposit mostly limited to combination-sensitive MGB areas, labeling in 24-31 kHz representations of the ICC was absent or minor. These results suggest that many combination-sensitive neurons in the MGB do not receive 24-31 kHz ICC input. The strongest inputs to combination-sensitive MGB regions originate in high-frequency representations of the ICC and combination-sensitive regions of auditory cortex. Additional projections arrive from the thalamic reticular nucleus, external nucleus of the inferior colliculus, and pericollicular tegmentum. Each projection may contribute to the 24-31 kHz sensitivity of combination-sensitive neurons in the medial geniculate body.

Acoustic Stimulation

Cytoarchitecture of the medial geniculate body in the mustached bat (Pteronotus parnellii).

The cytoarchitectonic organization of the medial geniculate body and adjoining thalamic nuclei was analyzed in the mustached bat (Pteronotus parnellii). These subdivisions provide a reference for structural, physiological, connectional, and neurochemical work. Most nuclei recognized in other mammals exist in the mustached bat, although the relative volume of the three divisions was species specific. The ventral division contains medium-sized neurons and a few smaller cells and is well developed. Neurons in the lateral part lie in regularly aligned rows corresponding to the laminae in Golgi material; in the medial part, these laminae are obscured by fibers. The dorsal division has at least four nuclei, each with a unique cytoarchitecture and myeloarchitectonic organization. The suprageniculate nucleus is prominent and has many large radiate neurons. Cells in the superficial dorsal nucleus have weekly laminated dendrites, while dorsal nucleus neurons have spherical dendritic fields. There is a wide range of neuropil patterns within the dorsal division. The suprageniculate nucleus has thick myelinated axons, while the fibers in the superficial and dorsal nuclei are much thinner. The rostral pole nucleus becomes prominent in the anterior one-half of the auditory thalamus; its architectonic affiliation is equivocal, and connectional and immunocytochemical studies suggest that it may belong to the dorsal division. The medial division is one nucleus with many types of neurons, and it has coarse axons without laminar orientation. It is the smallest of the divisions and is present throughout the medial geniculate complex, except at the caudal tip and at the rostral pole. Many features of medial geniculate body organization evident in other mammals are recognized in the mustached bat. These include a prominent ventral division, some of whose neurons have a laminar organization, and a comparatively small medial division that is devoid of fibrodendritic laminae. Other features, such as the presence of a large rostral pole nucleus, whose homologue in other species is uncertain, or the sparse number or small cells that may participate in local circuits, set it apart from carnivores and primates and suggest that there are species specific patterns of medial geniculate body organization.

Animals

The neurons of the medial geniculate body in the mustached bat (Pteronotus parnellii).

The neurons in the medial geniculate body were studied in Golgi preparations from adult mustached bats (Pteronotus parnellii). Their somatic and dendritic configurations were compared with those of cells in other, nonecholocating mammals. A second goal was to use the thalamic nuclear subdivisions derived from Golgi material to integrate the findings in parallel studies of cytoarchitecture, immunocytochemistry, and tectothalamic connections. Three primary divisions are defined. The ventral division is large and has a stereotyped neuronal organization. Medium-sized perikarya (about 10 microns in diameter) represent tufted neurons; the fibrodendritic plexus forms laminae in the lateral part along which midbrain axons terminate. A smaller, possibly intrinsic, neuron with thin, sparse dendrites is rarely impregnated. Neurons in the larger, medial part, which represents frequencies of 60 kHz and higher, have more spherical dendritic fields; their branching pattern remains tufted, and the laminar organization was less evident. The dorsal division is about equal in size, and it has many nuclei and a corresponding neuronal diversity. These neurons are medium-sized except in the suprageniculate nucleus, where many cells are larger. Four dorsal division nuclei are recognized. Each has neurons with radiate or weakly tufted dendritic arbors. Superficial dorsal nucleus neurons are oriented from medial to lateral, imparting a slightly laminated appearance to the neuropil. A few smaller, stellate neurons with modest dendritic domains are present. Suprageniculate nucleus neurons have radiating dendritic fields that project spherically; they have fewer branches than dorsal nucleus neurons. The posterior limitans nucleus is dorsomedial to the suprageniculate nucleus; it has small neurons with long, sparsely branched dendrites. The rostral pole nucleus, included in the dorsal division on cytoarchitectonic grounds, had too few neurons impregnated to reveal its neuronal architecture. The medial division, the smallest of the main parts, is one nucleus with at least six types of cells, including the magnocellular, bushy tufted, disc-shaped, medium-sized multipolar, elongated, and small stellate neurons. There is no laminar arrangement. Many of the neurons resemble those in rodent, marsupial, carnivore, and primate auditory thalamic nuclei. Despite such morphological correspondences, functional differences, such as the evolution of combination sensitivity, suggest that structurally comparable auditory thalamic neurons may subserve diverse physiological representations.

Animals

Projections of physiologically defined subdivisions of the inferior colliculus in the mustached bat: targets in the medial geniculate body and extrathalamic nuclei.

This study examined the output of the central nucleus of the inferior colliculus to the medial geniculate body and other parts of the nervous system in the mustached bat (Pteronotus parnellii). Small deposits of anterograde tracers (horseradish peroxidase, [3H]leucine, Phaseolus vulgaris leucoagglutinin, wheat germ agglutinin conjugated to horseradish peroxidase, or biocytin) were made at physiologically defined sites in the central nucleus representing major components of the bat's echolocation signal. The topography, frequency specificity, and axonal morphology of these outputs were studied. The medial geniculate body was a major target of inferior collicular neurons, with three distinct input patterns. The projection to the ventral division was tonotopically organized, but had a relatively sparse contribution from neurons representing frequency modulated components of the biosonar pulse. The second input was to the rostral medial geniculate body, in which projections from inferior collicular neurons representing constant frequency sonar components were separated from those representing frequency modulated components. A third input was to the suprageniculate nucleus, which received strong, topographically arranged projections. Inputs to the dorsal nucleus and medial division were also observed. Extrathalamic regions receiving input included the pontine gray, external nucleus of the inferior colliculus, pericollicular tegmentum, nucleus of the brachium of the inferior colliculus, and pretectum. These central nucleus projections differed in organization and the structure of axon terminals, suggesting different physiological influences on their target nuclei. These results demonstrate that the central nucleus has divergent projections to various sensory and premotor nuclei, besides its well-established projection to the medial geniculate body.

Acoustic Stimulation

Patterns of GABAergic immunoreactivity define subdivisions of the mustached bat's medial geniculate body.

The anatomy and the spatial distribution of neurons and axonal endings (puncta) immunoreactive for glutamic acid decarboxylase (GAD) or gamma-aminobutyric acid (GABA) were studied in the medial geniculate body of the mustached bat (Pteronotus parnellii). The principal findings are that: 1) most GABAergic neurons are present in the dorsal and ventral divisions with few, if any, in the medial division; 2) only a small fraction, about 1% or less, of auditory thalamic neurons are immunopositive; 3) the density of immunoreactive puncta is independent on the number of GABAergic neurons in the thalamic divisions, with the ventral division having the largest number/unit area, the medial division about 75% of this value, and the dorsal division only about 50%; and 4) the form of the puncta was unique to each division, those in the ventral division being medium-sized and comparatively simple, those in the medial division predominantly large, coarse, and complex, while dorsal division ending were finer and more delicate. These patterns recapitulate, with some significant exceptions, those found in the rat and cat. The puncta could originate from several sources; while many may arise from intrinsic GABAergic Golgi type II local circuit neurons, these cells may not be the only or even the principal source. Thus, the dorsal division contains comparatively many immunopositive cells though fewer puncta than might be expected if the bulk of these were to arise from auditory thalamic interneurons. This suggests that other, extrinsic sources, such as the thalamic reticular nucleus, may be the source of such endings. A second point is that the form and density of the puncta is regionally specific within the medial geniculate complex. These local patterns might have a significant and regionally specific role in controlling the differential excitability of auditory thalamic neurons. The distribution of presumptive synaptic endings also has implications for the number and arrangement of glomeruli or synaptic nests. Thus, these circuit elements, which are common to the thalamic nuclei in other species, might play an important role in local synaptic circuits between different types of cells. If so, then the structural variations embodied in these patterns could subserve functional arrangements that differ among species. Such patterns might reflect concomitant physiological differences in the organization of local circuits within the microchiropteran medial geniculate body.

Animals

Spatial processing within the mustache bat echolocation system: possible mechanisms for optimization.

1. The directionality of an echolocation system is determined by the acoustic properties of both the emitter and receiver, i.e., by the radiation pattern of the emitted pulse and the directionally of the external ears. We measured the directionality of the echolocation system of the greater mustache bat (Pteronotus parnellii) at the 30 kHz, 60 kHz and 90 kHz harmonics of its echolocation pulse by summing, at points throughout the frontal sound field, the echo attenuation due to the spread of pulse energy and the attenuation due to the spread of pulse energy and the attenuation due to the directionality of its external ears. The pulse radiation pattern at the 3 harmonics was measured by comparing the output of a microphone moved throughout the frontal sound field against a second reference microphone at the center of the field. External ear directionality at the 3. harmonics was measured by presenting free-field sounds throughout the frontal sound field, and recording the intensity thresholds of cochlear microphonic potentials, and the intensity thresholds of monaural neurons in the inferior colliculus tuned to one of the 3 harmonics. 2. When compared with ear directionality, the echolocation system was found to be more directional for the center of the sound field in several respects. At all harmonics, attenuation of sounds originating in the peripheral part of the field was increased by 10 to 13 dB. Areas of maximum sound intensity contracted toward the center of the field. Also, the isointensity contours of the echolocation system were more radially symmetrical about the center of the field. 3. At 60 kHz, sound intensity along the azimuth within the echolocation system was nearly constant 26 degrees to either side of the center of the field. This suggests that the radiation pattern of the echolocation pulse and the directionality of the external ears complement one another to produce an acoustic environment at the center of the sound field in which stimulus intensity is stabilized to allow more effective analysis of various aspects of the echolocation target. In particular, we suggest that this intensity stabilization may allow the bat to more effectively resolve the interaural intensity differences it uses to localize prey. 4. Predictions of the azimuthal spatial tuning of binaurally sensitive neurons in the inferior colliculus within the echolocation system were compared with their spatial tuning when only ear directionality is considered.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation

Determinants of horizontal sound location selectivity of binaurally excited neurons in an isofrequency region of the mustache bat inferior colliculus.

1. The monaural and binaural response properties and the horizontal sound location sensitivity of 78 binaurally excited neurons from 26 bats were examined with a combined closed-field and free-field stimulation paradigm. The aim was to determine how the response properties of these neurons shape their selectivity for auditory space. All neurons were recorded within a single, greatly enlarged isofrequency (60 kHz) region of the mustache bat's central nucleus of the inferior colliculus (ICC). In this and two companion papers (Wenstrup et al. 1988a,b) that focused on binaurally inhibited neurons in this isofrequency region, our goal was to examine the neural mechanisms for binaural processing within a single frequency channel of the primary auditory system. 2. Binaurally excited neurons were defined as either excited by monaural input from both ears or, if excited by monaural stimulation of only one ear, facilitated by binaural stimulation. Some neurons also exhibited binaural inhibition. These neurons were divided into functional classes based on their responses to monaural and binaural stimulation presented under dichotic, closed-field conditions. The following notation was used: response to contralateral stimulation (E, excitatory; O, no effect), response to ipsilateral stimulation (E, excitatory; O, no effect)/response to binaural stimulation (F, facilitatory; I, inhibitory; O, no effect). Seven functional classes were observed: EE/O, EE/F, EE/I, EE/FI, EO/F, EO/FI, and OO/F. 3. Among EE neurons, thresholds for contralateral monaural stimulation were typically lower than for ipsilateral stimulation, and response magnitudes for contralateral stimulation were typically greater. Among EO/F and EO/FI neurons, only one eye, an OE/FI neuron, was excited by ipsilateral monaural stimulation. These results suggest that contralateral input provides the dominant excitatory influence. EE/FI and EO/FI neurons, which exhibited both binaural facilitation and inhibition, were typically inhibited at interaural intensity differences (IIDs) favoring the ipsilateral ear, suggesting that ipsilateral input provides the dominant inhibitory influence. 4. Neurons were tested over the range of naturally occurring IIDs (+/- 30 dB) at intensities of -20 to 30 dB relative to threshold. The IID functions of these neurons assumed three configurations: flat, with facilitation occurring at all IIDs; stepped, with facilitation occurring over part of the IID range, and peaked, with facilitation occurring over a limited band of IIDs. The majority of cells (90%) exhibited peaked IID functions, and most of these (73%), regardless of functional class, were maximally facilitated at an IID of 0 dB. 5. Neurons differed considerably in the strength of their binaural interactions.(ABSTRACT TRUNCATED AT 400 WORDS)

Action Potentials

The acoustic role of tracheal chambers and nasal cavities in the production of sonar pulses by the horseshoe bat, Rhinolophus hildebrandti.

The acoustic role of the enlarged, bony, nasal cavities and rigid tracheal chambers in the horseshoe bat, Rhinolophus hildebrandti (Fig. 2) was investigated by determining the effect of their selective filling on the nasally emitted sonar pulse and on the sound traveling backwards down the trachea. Normal sonar signals of this bat contain a long constant frequency component with most energy in the second harmonic at about 48 kHz. The fundamental is typically suppressed 20 to 30 dB below the level of the second harmonic (Fig. 1). None of the experimental manipulations described affected the frequency of the sonar signal fundamental. Filling the dorsal and both lateral tracheal chambers had little effect on the emitted vocalization, but caused the level of the fundamental component in the trachea to increase 15 to 19 dB in most bats (Table 2). When only the dorsal chamber or only the two lateral chambers were filled, the effect was less striking and more variable (Tables 3 and 4), suggesting that the tracheal fundamental is normally suppressed by acoustic interaction between these three cavities. Filling the enlarged dorsal nasal cavities had no effect on the tracheal sound. The effect of this treatment on the nasally emitted sonar pulse was inconsistent. Sometimes the fundamental increased 10 to 12 dB, other times the intensity of all harmonics decreased; in still other cases the second, third or fourth harmonic increased, but the fundamental remained unchanged (Tables 5, 6, and 7). When bats were forced to vocalize through the mouth, by sealing the nostrils, there was a prominent increase in the level of the emitted fundamental (10 to 21 dB) and in the fourth harmonic (6 to 17 dB). In one instance there was also a significant increase in the level of the third harmonic (Tables 8 and 9). The supraglottal tract thus filters the fundamental from the nasally emitted sonar signal, although the role of the inflated nasal cavities in this process is unclear. We conclude that a high glottal impedance acoustically isolates the subglottal from the supraglottal vocal tract. The tracheal chambers do not affect the emitted sonar signal, but may attenuate the fundamental in the trachea and prevent it from being reflected from the lungs back towards the cochlea. It may be important to prevent the reflected fundamental from stimulating the cochlea, via tissue conduction, along multiple indirect pathways which would temporally smear cochlear stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Binaural neurons in the mustache bat's inferior colliculus. I. Responses of 60-kHz EI units to dichotic sound stimulation.

1. Single-unit responses to closed-field, dichotic sound stimuli were obtained from EI neurons in the mustache bat's inferior colliculus; these neurons are excited by sound to the contralateral ear and inhibited by sound to the ipsilateral ear. All units were tuned to the 60-kHz component of the bat's sonar signal. The goal of the study was to describe basic features of the sensitivity to interaural intensity differences (IIDs) and sound intensity among an isofrequency population of EI neurons. The following paper describes how these features of IID sensitivity shape the response to free-field sounds. 2. Three features of IID sensitivity were considered. The inhibitory threshold (Figs. 1 and 2) described the IID at which inhibitory effects became pronounced; it was defined as the IID at which the excitatory response to contralateral sound was suppressed by 50%. Most units (68%) were inhibited at positive IID values, for which the ipsilateral (inhibitory) sound was more intense. The maximum inhibition (Figs. 1 and 3) described the strength of ipsilateral inhibition; it was defined as the percent that each unit was inhibited below its response to monaural stimulation of the contralateral ear. The majority of units (58%) were almost totally suppressed by a sufficiently intense ipsilateral sound. The IID range (Figs. 1 and 4) described the sharpness or slope of the IID cutoff; it was defined as the IID range over which the response changed from nearly unsuppressed (80% of maximum response) to near maximum suppression (20% of maximum response). Most units (71%) had IID ranges of less than or equal to 15 dB. 3. A significant correlation between the inhibitory threshold and the maximum inhibition (Fig. 5) among the sample of EI units suggests that some common neural mechanisms underlie these features of IID sensitivity. 4. The response of EI neurons to binaural stimuli was a function of sound intensity as well as IID (Fig. 7). In part, this resulted from intensity-dependent changes in properties of binaural inhibition. For most units, basic measures of IID sensitivity changed to a limited extent as the sound intensity changed.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation

Binaural neurons in the mustache bat's inferior colliculus. II. Determinants of spatial responses among 60-kHz EI units.

1. The responses to closed-field and free-field sound stimuli were obtained from EI neurons in the 60-kHz isofrequency representation of the mustache bat's inferior colliculus. The goals of the study were 1) to examine how binaural interactions and the directional properties of the ear shape the spatial response of 60-kHz EI neurons and 2) to examine features of the spatial responses of these isofrequency neurons which may encode the location of a sound. 2. The free-field response of monaural neurons was used to describe directional effects of the head and external ears at 60 kHz. Monaural neurons were most sensitive to sounds originating 26 degrees into the contralateral field, with sharply reduced sensitivity in the ipsilateral field and the lateral extreme of the contralateral field. The interaural intensity difference (IID), computed by assuming that the ears had mirror-image directional sensitivities, was greatest for sounds between 26 and 52 degrees off the vertical midline, where IIDs typically ranged from 20 to 30 dB. These values agree well with previous measures of the directional sensitivity of the ear obtained from cochlear microphonic recordings. 3. The response of a monaural unit to closed-field stimulation was used to predict its response to free-field stimulation. This prediction agreed closely with the observed free-field response, indicating that the monaural unit's free-field response could be explained by the directional sensitivity of the contralateral ear and the unit's response as a function of contralateral sound intensity. 4. EI neurons differed in basic features of their binaural response properties, as described in a companion paper. To examine how these features of binaural inhibition shaped spatial responses, we obtained responses to free-field sounds among neurons whose binaural properties had been thoroughly characterized. We then compared the spatial response to a prediction based upon the directional properties of the ear and the sensitivity of the EI neurons to IIDs and intensity. The close agreement between the observed and predicted spatial responses in 11 of 12 EI units indicated that the spatial responses were determined largely by sensitivity to IIDs and intensity and by the directional properties of the ear. 5. EI neurons in our sample were most sensitive, and responded best, to sounds originating 26-39 degrees into the contralateral field. These spatial response features were independent of the binaural properties of EI neurons. Instead, they depended upon the directional properties of the ears at 60 kHz.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation

Binaural response organization within a frequency-band representation of the inferior colliculus: implications for sound localization.

The auditory system of the mustache bat (Pteronotus parnellii) contains a disproportionately large representation of a narrow frequency band, corresponding to the dominant, 60 kHz component of its echolocation signal. In the inferior colliculus (IC), the 60 kHz representation comprises an architectonically distinct region called the dorsoposterior division (DPD), which is accessible for detailed physiological study. We examined the topographic distribution of binaural responses within this one frequency-band representation of the inferior colliculus. We describe two primary results. First, neurons with different binaural response properties are spatially segregated into one of four binaural response-specific regions of the DPD: a large region of monaural (EO) responses; two regions containing neurons excited by sound from both ears (EE); and a region containing neurons excited by one ear and inhibited by the other (EI). Regions dominated by 60 kHz EI responses are also found in the lateral extremity of the IC, probably within the external nucleus. These results demonstrate functionally defined subdivisions in a single frequency-band representation of the IC. Moreover, they suggest that brain stem auditory projections to the DPD and/or intrinsic connections within the DPD are highly organized. Second, within the EI region of the DPD, there is a systematic shift in the sensitivity of EI multiunit responses to interaural intensity disparities (IIDs). Dorsally, EI neurons are suppressed only by relatively loud ipsilateral sounds, and there is a systematic decrease in the relative ipsilateral intensity required for suppression at more ventral recording sites. This result demonstrates that neurons sensitive to a sound localization cue are systematically organized within a frequency-band representation of the inferior colliculus. It has implications for the manner in which the location of a sound source is encoded within the primary auditory pathway.

Animals

A functional organization of binaural responses in the inferior colliculus.

Binaural responses are segregated within an enlarged isofrequency region of the mustache bat's inferior colliculus. In the part of this region containing E-I responses, there is an orderly shift in the sensitivity of unit clusters to interaural intensity disparities, having implications for the representation of auditory space within isofrequency regions of the inferior colliculus.

Animals

A representation of horizontal sound location in the inferior colliculus of the mustache bat (Pteronotus p. parnellii).

Binaurally sensitive E-I neurons in the inferior colliculus are topographically organized with respect to their sensitivity to interaural intensity disparities (IIDs). IID sensitivity dictates the azimuthal position of the medial border of a neuron's spatial receptive field. A sound moving along the azimuth will result in a change in the percentage of excited neurons as receptive field borders are crossed. Percent excitation within this population may provide a neural code for horizontal sound location.

Animals