Mechanisms of Sound Localization in Two Functionally Distinct Regions of the Auditory Cortex.

The auditory cortex is necessary for sound localization. The mechanisms that shape bicoordinate spatial representation in the auditory cortex remain unclear. Here, we addressed this issue by quantifying spatial receptive fields (SRFs) in two functionally distinct cortical regions in the pallid bat. The pallid bat uses echolocation for obstacle avoidance and listens to prey-generated noise to localize prey. Its cortex contains two segregated regions of response selectivity that serve echolocation and localization of prey-generated noise. The main aim of this study was to compare 2D SRFs between neurons in the noise-selective region (NSR) and the echolocation region [frequency-modulated sweep-selective region (FMSR)]. The data reveal the following major differences between these two regions: (1) compared with NSR neurons, SRF properties of FMSR neurons were more strongly dependent on sound level; (2) as a population, NSR neurons represent a broad region of contralateral space, while FMSR selectivity was focused near the midline at sound levels near threshold and expanded considerably with increasing sound levels; and (3) the SRF size and centroid elevation were correlated with the characteristic frequency in the NSR, but not the FMSR. These data suggest different mechanisms of sound localization for two different behaviors. Previously, we reported that azimuth is represented by predictable changes in the extent of activated cortex. The present data indicate how elevation constrains this activity pattern. These data suggest a novel model for bicoordinate spatial representation that is based on the extent of activated cortex resulting from the overlap of binaural and tonotopic maps. SIGNIFICANCE STATEMENT: Unlike the visual and somatosensory systems, spatial information is not directly represented at the sensory receptor epithelium in the auditory system. Spatial locations are computed by integrating neural binaural properties and frequency-dependent pinna filtering, providing a useful model to study how neural properties and peripheral structures are adapted for sensory encoding. Although auditory cortex is necessary for sound localization, our understanding of how the cortex represents space remains rudimentary. Here we show that two functionally distinct regions of the pallid bat auditory cortex represent 2D space using different mechanisms. In addition, we suggest a novel hypothesis on how the nature of overlap between systematic maps of binaural and frequency selectivity leads to representation of both azimuth and elevation.

Level-tolerant duration selectivity in the auditory cortex of the velvety free-tailed bat Molossus molossus.

It has been reported previously that in the inferior colliculus of the bat Molossus molossus, neuronal duration tuning is ambiguous because the tuning type of the neurons dramatically changes with the sound level. In the present study, duration tuning was examined in the auditory cortex of M. molossus to describe if it is as ambiguous as the collicular tuning. From a population of 174 cortical 104 (60 %) neurons did not show duration selectivity (all-pass). Around 5 % (9 units) responded preferentially to stimuli having longer durations showing long-pass duration response functions, 35 (20 %) responded to a narrow range of stimulus durations showing band-pass duration response functions, 24 (14 %) responded most strongly to short stimulus durations showing short-pass duration response functions and two neurons (1 %) responded best to two different stimulus durations showing a two-peaked duration-response function. The majority of neurons showing short- (16 out of 24) and band-pass (24 out 35) selectivity displayed "O-shaped" duration response areas. In contrast to the inferior colliculus, duration tuning in the auditory cortex of M. molossus appears level tolerant. That is, the type of duration selectivity and the stimulus duration eliciting the maximum response were unaffected by changing sound level.

Parvalbumin and calbindin expression in parallel thalamocortical pathways in a gleaning bat, Antrozous pallidus.

The pallid bat (Antrozous pallidus) listens to prey-generated noise to localize and hunt terrestrial prey while reserving echolocation to avoid obstacles. The thalamocortical connections in the pallid bat are organized as parallel pathways that may serve echolocation and prey localization behaviors. Thalamic inputs to the cortical echolocation call- and noise-selective regions originate primarily in the suprageniculate nucleus (SG) and ventral division of medial geniculate body (MGBv), respectively. Here we examined the distribution of parvalbumin (PV) and calbindin (CB) expression in cortical regions and thalamic nuclei of these pathways. Electrophysiology was used to identify cortical regions selective for echolocation calls and noise. Immunohistochemistry was used to stain for PV and CB in the auditory cortex and MGB. A higher percentage (relative to Nissl-stained cells) of PV(+) cells compared with CB(+) cells was found in both echolocation call- and noise-selective regions. This was due to differences in cortical layers V-VI, but not layers I-IV. In the MGB, CB(+) cells were present across all divisions of the MGB, with a higher percentage in the MGBv than the SG. Perhaps the most surprising result was the virtual absence of PV staining in the MGBv. PV staining was present only in the SG. Even in the SG, the staining was mostly diffuse in the neuropil. These data support the notion that calcium binding proteins are differentially distributed in different processing streams. Our comparative data, however, do not support a general mammalian pattern of PV/CB staining that distinguishes lemniscal and nonlemniscal pathways.

Duration tuning in the inferior colliculus of the mustached bat.

We studied duration tuning in neurons of the inferior colliculus (IC) of the mustached bat. Duration-tuned neurons in the IC of the mustached bat fall into three main types: short (16 of 136), band (34 of 136), and long (29 of 136) pass. The remaining 51 neurons showed no selectivity for the duration of sounds. The distribution of best durations was double peaked with maxima around 3 and 17 ms, which correlate with the duration of the short frequency-modulated (FM) and the long constant-frequency (CF) signals emitted by Pteronotus parnellii. Since there are no individual neurons with a double-peaked duration response profile, both types of temporal processing seem to be well segregated in the IC. Most short- and band-pass units with best frequency in the CF2 range responded to best durations > 9 ms (66%, 18 of 27 units). However, there is no evidence for a bias toward longer durations as there is for neurons tuned to the frequency range of the FM component of the third harmonic, where 83% (10 of 12 neurons) showed best durations longer than 9 ms. In most duration-tuned neurons, response areas as a function of stimulus duration and intensity showed either V or U shape, with duration tuning retained across the range of sound levels tested. Duration tuning was affected by changes in sound pressure level in only six neurons. In all duration-tuned neurons, latencies measured at the best duration were longer than best durations, suggesting that behavioral decisions based on analysis of the duration of the pulses would not be expected to be complete until well after the stimulus has occurred.

Simulated head related transfer function of the phyllostomid bat Phyllostomus discolor.

UNLABELLED: This paper presents a calculation of the head related transfer function (HRTF) for the frontal hemisphere of the phyllostomid bat Phyllostomus discolor using an acoustic field simulation tool based on the boundary element method. From the calculated HRTF results, binaural interaural intensity differences (IIDs) are derived. THE RESULTS: Region of highest sensitivity, HRTF patterns, and IID patterns are shown to be in good agreement with earlier experimental measurements on other specimens of the same bat species, i.e., the differences are within the interspecies variability range. Next, it is argued that the proposed simulation method offers distinct advantages over acoustic measurements on real bat specimens. To illustrate this, it is shown how computer manipulation of the virtual morphology model allows a more detailed comprehension of bat spatial hearing by investigating the effects of different head parts on the HRTF. From this analysis it is concluded that for this species the pinna has a significantly larger effect on the HRTF and IID patterns than the head itself. This conclusion argues in favor of a series of recent simulation studies based on pinna morphology only [R. Muller, J. Acoust. Soc. Am. 116, 3701-3712 (2004); Muller et al., ibid 119, 4083-4092 (2006)].

The auditory cortex of the bat Phyllostomus discolor: Localization and organization of basic response properties.

BACKGROUND: The mammalian auditory cortex can be subdivided into various fields characterized by neurophysiological and neuroarchitectural properties and by connections with different nuclei of the thalamus. Besides the primary auditory cortex, echolocating bats have cortical fields for the processing of temporal and spectral features of the echolocation pulses. This paper reports on location, neuroarchitecture and basic functional organization of the auditory cortex of the microchiropteran bat Phyllostomus discolor (family: Phyllostomidae). RESULTS: The auditory cortical area of P. discolor is located at parieto-temporal portions of the neocortex. It covers a rostro-caudal range of about 4800 mum and a medio-lateral distance of about 7000 mum on the flattened cortical surface. The auditory cortices of ten adult P. discolor were electrophysiologically mapped in detail. Responses of 849 units (single neurons and neuronal clusters up to three neurons) to pure tone stimulation were recorded extracellularly. Cortical units were characterized and classified depending on their response properties such as best frequency, auditory threshold, first spike latency, response duration, width and shape of the frequency response area and binaural interactions. Based on neurophysiological and neuroanatomical criteria, the auditory cortex of P. discolor could be subdivided into anterior and posterior ventral fields and anterior and posterior dorsal fields. The representation of response properties within the different auditory cortical fields was analyzed in detail. The two ventral fields were distinguished by their tonotopic organization with opposing frequency gradients. The dorsal cortical fields were not tonotopically organized but contained neurons that were responsive to high frequencies only. CONCLUSION: The auditory cortex of P. discolor resembles the auditory cortex of other phyllostomid bats in size and basic functional organization. The tonotopically organized posterior ventral field might represent the primary auditory cortex and the tonotopically organized anterior ventral field seems to be similar to the anterior auditory field of other mammals. As most energy of the echolocation pulse of P. discolor is contained in the high-frequency range, the non-tonotopically organized high-frequency dorsal region seems to be particularly important for echolocation.

Adaptive trade-off in floral morphology mediates specialization for flowers pollinated by bats and hummingbirds.

Evolution toward increased specificity in pollination systems is thought to have played a central role in the diversification of angiosperms. Theory predicts that the presence of trade-offs in adapting to different pollinator types will favor specialization, yet few studies have attempted to characterize such interactions in nature. I conducted flight cage experiments with bats, hummingbirds, and artificial flowers to examine effects of corolla width on pollination. I videotaped visits to analyze pollinator behavior and counted pollen grains transferred to stigmas. Results demonstrated that flower-pollinator fit is critical to effective pollination; wide corollas guided bat snouts better, and narrow corollas guided hummingbird bills better. Poor fit resulted in variable entry angles and decreased pollen transfer. A model using these results predicts that wide corollas will be selected for when bats make more than 44% of the visits and narrow corollas when they make fewer. Intermediate corollas are never favored (i.e., generalization is always suboptimal). This is the first study to clearly document a pollinator-mediated fitness trade-off in floral morphology.

Connections of functional areas in the mustached bat's auditory cortex with the auditory thalamus.

The auditory thalamus is the major target of the inferior colliculus and connects in turn with the auditory cortex. In the mustached bat, biosonar information is represented according to frequency in the central nucleus of the inferior colliculus (ICc) but according to response type in the cortex. In addition, the cortex has multiple areas with neurons of similar response type compared to the single tonotopic representation in the ICc. To investigate whether these transformations occur at the level of the thalamus, we injected anatomical tracers into physiologically defined locations in the mustached bat's auditory cortex. Injections in areas used for target ranging labeled contiguous regions of the auditory thalamus rather than separate patches corresponding to regions that respond to the different harmonic frequencies used for ranging. Injections in the two largest ranging areas produced labeling in separate locations. These results indicate that the thalamus is organized according to response type rather than frequency and that multiple mappings of response types exist. Injections in areas used for target detection labeled thalamic regions that were largely separate from those that interconnect with ranging areas. However, injections in an area used for determining target velocity overlapped with the areas connected to ranging areas and areas involved in target detection. Thus, separation by functional type and multiplication of areas with similar response type occurs by the thalamic level, but connections with the cortex segregate the functional types more completely than occurs in the thalamus.

Nectar bat stows huge tongue in its rib cage.

Bats of the subfamily Glossophaginae (family Phyllostomidae) are arguably the most specialized of mammalian nectarivores, and hundreds of neotropical plants rely on them for pollination. But flowers pollinated by bats are not known to specialize for bat subgroups (unlike flowers that have adapted to the length and curvature of hummingbird bills, for example), possibly because the mouthparts of bats do not vary much compared with the bills of birds or the probosces of insects. Here I report a spectacular exception: a recently-described nectar bat that can extend its tongue twice as far as those of related bats and is the sole pollinator of a plant with corolla tubes of matching length.

Relation between intrinsic connections and isofrequency contours in the inferior colliculus of the big brown bat, Eptesicus fuscus.

Information processing in the inferior colliculus depends on interactions between ascending pathways and intrinsic circuitry, both of which exist within a functional tonotopic organization. To determine how local projections of neurons in the inferior colliculus are related to tonotopy, we placed a small iontophoretic injection of biodextran amine at a physiologically characterized location in the inferior colliculus. We then used electrophysiological recording to place a grid of small deposits of Chicago Sky Blue throughout the same frequency range to specify an isofrequency contour. Using three-dimensional computer reconstructions, we analyzed patterns of transport relative to the physiologically determined isofrequency contour to quantify the extent of the intrinsic connection lamina in all three dimensions. We also performed a quantitative analysis of the numbers of cells in different regions relative to the biodextran amine injection. Biodextran amine-labeled fibers were mainly located dorsomedial to the injection site, confined within the isofrequency contour, but biodextran amine-labeled cells were mainly located ventrolateral to the injection site. When we counted numbers of labeled cells classified by morphological type, we found that both elongate and multipolar cells were labeled within the isofrequency contour. Because the dendrites of multipolar cells typically extend outside the isofrequency lamina, it is likely that they receive input from other isofrequency contours and relay it to more dorsomedial portions of their specific isofrequency contour, along with the frequency-specific projections of the elongate cells. Within a given isofrequency contour, there is a consistent organization in which intrinsic connections ascend from the ventrolateral portion to more dorsomedial points along the contour, forming a cascaded system of intrinsic feedforward connections that seem ideally suited to provide the delay lines necessary to produce several forms of selectivity for temporal patterns in inferior colliculus neurons.

Visual thalamocortical projections in the flying fox: parallel pathways to striate and extrastriate areas.

We studied thalamic projections to the visual cortex in flying foxes, animals that share neural features believed to resemble those present in the brains of early primates. Neurones labeled by injections of fluorescent tracers in striate and extrastriate cortices were charted relative to the architectural boundaries of thalamic nuclei. Three main findings are reported: First, there are parallel lateral geniculate nucleus (LGN) projections to striate and extrastriate cortices. Second, the pulvinar complex is expansive, and contains multiple subdivisions. Third, across the visual thalamus, the location of cells labeled after visual cortex injections changes systematically, with caudal visual areas receiving their strongest projections from the most lateral thalamic nuclei, and rostral areas receiving strong projections from medial nuclei. We identified three architectural layers in the LGN, and three subdivisions of the pulvinar complex. The outer LGN layer contained the largest cells, and had strong projections to the areas V1, V2 and V3. Neurones in the intermediate LGN layer were intermediate in size, and projected to V1 and, less densely, to V2. The layer nearest to the origin of the optic radiation contained the smallest cells, and projected not only to V1, V2 and V3, but also, weakly, to the occipitotemporal area (OT, which is similar to primate middle temporal area) and the occipitoparietal area (OP, a "third tier" area located near the dorsal midline). V1, V2 and V3 received strong projections from the lateral and intermediate subdivisions of the pulvinar complex, while OP and OT received their main thalamic input from the intermediate and medial subdivisions of the pulvinar complex. These results suggest parallels with the carnivore visual system, and indicate that the restriction of the projections of the large- and intermediate-sized LGN layers to V1, observed in present-day primates, evolved from a more generalized mammalian condition.

Reorganization of the cochleotopic map in the bat's auditory system by inhibition.

The central auditory system of the mustached bat shows two types of reorganization of cochleotopic (frequency) maps: expanded reorganization resulting from shifts in the best frequencies (BFs) of neurons toward the BF of repetitively stimulated cortical neurons (hereafter centripetal BF shifts) and compressed reorganization resulting from the BF shifts of neurons away from the BF of the stimulated cortical neurons (hereafter centrifugal BF shifts). Facilitation and inhibition evoked by the corticofugal system have been hypothesized to be respectively related to centripetal and centrifugal BF shifts. If this hypothesis is correct, bicuculline (an antagonist of inhibitory GABA-A receptors) applied to cortical neurons would change centrifugal BF shifts into centripetal BF shifts. In the mustached bat, electric stimulation of cortical Doppler-shifted constant-frequency neurons, which are highly specialized for frequency analysis, evokes the centrifugal BF shifts of ipsilateral collicular and cortical Doppler-shifted constant-frequency neurons and contralateral cochlear hair cells. Bicuculline applied to the stimulation site changed the centrifugal BF shifts into centripetal BF shifts. On the other hand, electric stimulation of neurons in the posterior division of the auditory cortex, which are not particularly specialized for frequency analysis, evokes centripetal BF shifts of cortical neurons located near the stimulated cortical neurons. Bicuculline applied to the stimulation site augmented centripetal BF shifts but did not change the direction of the shifts. These observations support the hypothesis and indicate that centripetal and centrifugal BF shifts are both based on a single mechanism consisting of two components: facilitation and inhibition.

Tonotopic organization and parcellation of auditory cortex in the FM-bat Carollia perspicillata.

In the short-tailed fruit bat (Carollia perspicillata), the auditory cortex was localized autoradiographically and studied electrophysiologically in detail by using metal microelectrodes and 10-ms tone stimuli. Because, in the weakly-anaesthetized preparation, neuronal responses to pure-tones were even found throughout the non-primary auditory cortex, characteristic frequencies and minimum thresholds of neuron clusters (multiunits) could be mapped consistently and used to define auditory cortical fields conventionally (i.e. as in studies of auditory cortex of non-echolocating mammals). Thus, within the electrophysiologically demarcated auditory cortex, six auditory fields were defined by criteria, as for example a gradient of characteristic frequencies (primary auditory cortex, AI; anterior auditory field, AAF; secondary auditory cortex, AII), reversal of the gradient across the field border (AI, AAF), uniform representation of a restricted band of frequencies (i.e. > 60 kHz; high-frequency fields I and II, HFI and HFII), and transition from low to high minimum thresholds or vice versa [dorsoposterior field (DP), AII, HFI, HFII]. As supportive evidence for the distinction of these auditory cortical fields, differences in neuronal response properties were also used. In comparison with other mammals (e.g. cat and mouse), both the relative position of the auditory fields (mainly AI, AAF, DP and AII) and the representational principles for sound parameters within these forebrain areas seem to reflect a 'fundamental plan' (discussion below) of mammalian auditory cortical organization. Two coherent dorsally displaced high-frequency representations (HFI, HFII) covering approximately 40% of the total auditory cortical surface seem particularly suited for the processing of the dominant biosonar second and third harmonic of this species, and hence can be regarded as an adaptation for echolocation.

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 microns 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 degree-50 degrees in azimuth and 2 degrees up, 15 degrees 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 EI 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 microns), external granular (55 microns), external pyramidal (95 microns), internal granular (102 microns), internal pyramidal (191 microns) and multiform (120 microns) 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.

Anatomical and physiological investigation of auditory input to the superior colliculus of the echolocating megachiropteran bat Rousettus aegyptiacus.

The objective of this study was to investigate whether a representation of auditory space in the superior colliculus (SC) of the echolocating megachiropteran bat (Rousettus aegyptiacus) exists. Additionally the subcortical auditory connectivity of the SC was investigated. A total of 207 units were recorded in five awake animals while presenting acoustic stimuli (white noise, clicks, and pure tones) at different positions in space. Six units responded to acoustic stimulation. Three of these located within the superficial layers and one located in the intermediate layers were classified as omnidirectional units. Two units were located within the deep layers. One was classified as a hemifield unit, and the other as a frontal unit. All units responded phasically to acoustic stimulation with a latency of 4-150 ms. None of them could be activated by visual stimuli. We further examined the interaction of paired auditory and visual stimulation in 116 visually responsive units. Responses to visual stimulation were markedly altered by acoustic stimulation in 5 units. The influence of the acoustic stimuli was temporally and spatially restricted, and resulted either in a reduction or an elevation of unit responsiveness. Horseradish peroxidase was injected into the SC of eight animals to investigate the auditory subcortical connectivity of the SC. Retrograde labeling in auditory structures was rare compared with labeling found in nonauditory structures (e.g., retina, substantia nigra, parabigeminal nucleus). In auditory structures retrograde labeling was found mainly in the external nucleus of the inferior colliculus and in the nucleus of the brachium of the inferior colliculus. To a lesser extent it was found in the nucleus sagulum and in the area medial to the lemniscal nuclei. In one case the dorsal nucleus of the lateral lemniscus and the anterolateral periolivary nucleus were labeled. Our results reveal only a sparse auditory input into the SC of the flying fox, R. aegyptiacus. On the basis of single-unit recordings, we did not find an elaborate representation of auditory space as it is described for several other species. The existence of auditory and bimodal neurones, in combination with their response properties, nonetheless indicate that there might be a representation of auditory space in the SC of R. aegyptiacus.

Comparative morphology of the pituitary gland in Australian flying foxes (Megachiroptera: genus Pteropus).

BACKGROUND: Investigations of reproductive endocrinology of flying foxes (genus Pteropus) have been hampered by inadequate information on the normal morphology of the megachiropteran pituitary. METHODS: The novel technique of graphical three-dimensional (3-D) reconstruction, supported by more traditional anatomical techniques, have now been used to examine the shapes of, the interrelations between, the lobes of the pituitary of the little red flying fox, Pteropus scapulatus. Statistical analysis of data from three species tested whether there were changes in pituitary size with annual cycles in function, particularly with key stages of reproduction. RESULTS: In the three species of Australian flying foxes examined, the hypophyseal cleft is closed; the pars intermedia extends over the rostral, ventral, and lateral surfaces of the neural lobe. The pars distalis is broad rostrally and extends over two-thirds of the lateral and ventral pars intermedia. The hypophyseal recess is broad at the median eminence, then narrows and extends through the infundibulum to, but not into, the neural lobe. In adult animals the pituitary weight was 10.0 +/- 0.3 mg (mean +/- s.e.) in P. scapulatus, 14.7 +/- 0.5 mg in Pteropus poliocephalus (greyheaded flying foxes), and 18.7 +/- 1.5 mg in Pteropus alecto (black flying foxes). Pituitary weight was not significantly affected by reproductive stage. CONCLUSIONS: Thus histologically, the adenohypophysis and neurohypophysis are similar to those of other mammals. Comparative differences in pituitary size reflected differences in species body size rather than cyclical reproduction.

A possible neuronal basis for representation of acoustic scenes in auditory cortex of the big brown bat.

Behavioural studies and field observations demonstrate that echolocating bats simultaneously perceive range, direction and shape of multiple objects in the environment as acoustic images derived from echoes. Cortical echo delay-tuned neurons contribute to the perception of object range, because focal inactivation of these neurons disrupts behavioural discrimination of range. We report here that response properties of delay-tuned neurons in the cortical tonotopic area of the bat, Eptesicus, transform the sequential arrival times of echoes with different delays into a concurrent, accumulating neural representation of multiple objects at different ranges. The sharpness of delay tuning systematically increases at each best delay in a subpopulation of these neurons while responses to echoes at different delays are accumulated. The resulting concurrent, multiresolution representation of echo delay corresponds to neural implementation of a common representation of images used in computational vision and may provide the basis for representing acoustic images of multiple objects as acoustic 'scenes'.

Visual system of a naturally microphthalmic mammal: the blind mole rat, Spalax ehrenbergi.

Retinal projections and visual thalamo-cortical connections were studied in the subterranean mole rat, belonging to the superspecies Spalax ehrenbergi, by anterograde and retrograde tracing techniques. Quantitative image analysis was used to estimate the relative density and distribution of retinal input to different primary visual nuclei. The visual system of Spalax presents a mosaic of both regressive and progressive morphological features. Following intraocular injections of horseradish peroxidase conjugates, the retina was found to project bilaterally to all visual structures described as receiving retinal afferents in non-fossorial rodents. Structures involved in form analysis and visually guided behaviors are reduced in size by more than 90%, receive a sparse retinal innervation, and are cytoarchitecturally poorly differentiated. The dorsal lateral geniculate nucleus, as defined by cyto- and myelo-architecture, cytochrome oxidase, and acetylcholinesterase distribution as well as by afferent and efferent connections, consists of a narrow sheet 3-5 neurons thick, in the dorsal thalamus. Connections with visual cortex are topographically organized but multiple cortical injections result in widespread and overlapping distributions of geniculate neurons, thus indicating that the cortical map of visual space is imprecise. The superficial layers of the superior colliculus are collapsed to a single layer, and the diffuse ipsilateral distribution of retinal afferents also suggests a lack of precise retinotopic relations. In the pretectum, both the olivary pretectal nucleus and the nucleus of the optic tract could be identified as receiving ipsilateral and contralateral retinal projections. The ventral lateral geniculate nucleus is also bilaterally innervated, but distinct subdivisions of this nucleus or the intergeniculate leaflet could not be distinguished. The retina sends a sparse projection to the dorsal and lateral terminal nuclei of the accessory optic system. The medial terminal nucleus is not present. In contrast to the above, structures of the "non-image forming" visual pathway involved in photoperiodic perception are well developed in Spalax. The suprachiasmatic nucleus receives a bilateral projection from the retina and the absolute size, cytoarchitecture, density, and distribution of retinal afferents in Spalax are comparable with those of other rodents. A relatively hypertrophied retinal projection is observed in the bed nucleus of the stria terminalis. Other regions which receive sparse visual input include the lateral and anterior hypothalamic areas, the retrochiasmatic region, the sub-paraventricular zone, the paraventricular hypothalamic nucleus, the anteroventral and anterodorsal nuclei, the lateral habenula, the mediodorsal nucleus, and the basal telencephalon.(ABSTRACT TRUNCATED AT 400 WORDS)

Immunocytochemical localization of luteinizing hormone-releasing hormone (LHRH) in the nervus terminalis and brain of the big brown bat, Eptesicus fuscus.

Little is known about the immunohistochemistry of the nervous system in bats. This is particularly true of the nervus terminalis, which exerts strong influence on the reproductive system during ontogeny and in the adult. Luteinizing hormone-releasing hormone (LHRH) was visualized immunocytochemically in the nervus terminalis and brain of juvenile and adult big brown bats (Eptesicus fuscus). The peripheral LHRH-immunoreactive (ir) cells and fibers (nervus terminalis) are dispersed along the basal surface of the forebrain from the olfactory bulbs to the prepiriform cortex and the interpeduncular fossa. A concentration of peripheral LHRH-ir perikarya and fibers was found at the caudalmost part of the olfactory bulbs, near the medioventral forebrain sulcus; obviously these cells mediate between the bulbs and the remaining forebrain. Within the central nervous system (CNS), LHRH-ir perikarya and fibers were distributed throughout the olfactory tubercle, diagonal band, preoptic area, suprachiasmatic and supraoptic nuclei, the bed nuclei of stria terminalis and stria medullaris, the anterior lateral and posterior hypothalamus, and the tuber cinereum. The highest concentration of cells was found within the arcuate nucleus. Fibers were most concentrated within the median eminence, infundibular stalk, and the medial habenula. The data obtained suggest that this distribution of LHRH immunoreactivity may be characteristic for microchiropteran (insectivorous) bats. The strong projections of LHRH-containing nuclei in the basal forebrain (including the arcuate nucleus) to the habenula, may indicate close functional contact between these brain areas via feedback loops, which could be important for the processing of thermal and other environmental stimuli correlated with hibernation.

Connections and frequency representation in the auditory brainstem of the mustache bat, Pteronotus parnellii.

The goals of this study were to describe the cochlear frequency map of the mustache bat, Pteronotus parnellii, and to relate the organization of cochlear primary afferents to that of the second-order projections from the cochlear nucleus to the superior olivary complex. Small deposits of horseradish peroxidase (HRP) were placed in the cochlear nucleus at sites that were physiologically characterized with respect to unit-best frequency. From the deposits, labeled fibers were traced in the retrograde direction to the cochlea and in the anterograde direction to the superior olive. Cochleas from both experimental and control animals were examined with light and electron microscopy. The peripheral axons of spiral ganglion neurons were counted in order to quantify the unusual variation in the innervation density along the cochlear spiral of the mustache bat. Regions of increased innervation density were found at the beginning and end of the basal turn of the cochlea. The highest cochlear innervation density consistently occurred in the upper basal turn. In horseradish peroxidase tracing experiments, this region contained labeled fibers only when HRP deposits were made at sites within the cochlear nucleus with unit-best frequencies around 60 kHz. These findings support the suggestion (Kössl and Vater, '85) that the cochlear sites of increased innervation density are related to the neural and behavioral emphasis that this echolocating bat places upon the analysis of the 60 kHz frequency band. The general arrangement of tonotopic maps within the cochlea, cochlear nucleus, and superior olive was consistent with previous observations in this bat and other mammalian species. At all three levels, there was evidence of a disproportionately large representation of frequencies around 60 kHz, similar to the enlarged representation reported within the inferior colliculus and auditory cortex of the mustache bat. In all cases there was a consistent relation between the size of the HRP deposit and the number and distribution of retrogradely labeled neurons in the cochlea. For most cases there was a similar relation between the size of the deposit and the terminal arborization field of anterogradely labeled fibers in the superior olive. However, in cases with deposits associated with the 60 kHz frequency band, the size of the labeled arborization field was more than twice as large as expected from the size of the deposits and from the extent of labeling in the cochlea. These cases suggest that the representation of frequencies around 60 kHz, already overrepresented in both the cochlea and cochlear nucleus, may be further expanded at the level of the superior olivary complex.