Tonotopic organization of the auditory forebrain in a songbird,the European starling

Summary The auditory area in the caudomedial forebrain of birds is explored by microelectrode recordings in a songbird. Multi-unit recordings reveal a clear tonotopic representation of stimulus frequency (Figs. 1, 2a, 3) with a mainly dorsoventral gradient (low frequencies dorsal). Frequency tuning is lost only in peripheral parts of the nucleus where wideband responses prevail. The functional structure is related to neuroanatomical landmarks of the forebrain by means of a 3-dimensional reconstruction from cell- and fibre-stained brain sections (Figs. 3, 4). For instance, a core region of high spontaneous and evoked activity (Figs. 5, 6b) is related to the input region (field L2) of the area. Additional single unit recordings support the multi-unit data (Fig. 6). The tonotopic organization found in the starling is compared with the organization of the caudomedial forebrain reported for other bird families.Abbreviations cer cerebellum - fpl fasciculus prosencephali lateralis - lh lamina hyperstriatica - lmd lamina medullaris dorsalis - ven ventricle - 2DG 2-Deoxyglucose This work was supported by the Deutsche Forschungsgemeinschaft, SFB 114     

Tonotopic organization of auditory receptors of the bushcricket Pholidoptera griseoaptera (Tettigoniidae, Decticinae)

The peripheral and central tonotopy of auditory receptors of the bushcricket Pholidoptera griseoaptera is described. Out of 24 auditory receptor cells of the crista acustica 18 were identified by single-cell recordings in the prothoracic ganglion and complete staining with neurobiotin. Proximal receptor cells of the crista acustica were most sensitive to 6 kHz, with medial cells being sensitive to 20–30 kHz, whereas distal cells were most sensitive to frequencies higher than 50 kHz. Projection areas within the auditory neuropile in the prothoracic ganglion were to- notopically arranged. Proximal cells projected anteriorly, medial cells ventrally and posteriorly, and distal cells to more dorsal regions. Identified receptor cells revealed an interindividual variability of tuning and central projections. Receptor cells from the intermediate organ of a bushcricket were identified for the first time. Receptors of the distal intermediate organ were broadly tuned and less sensitive than those of the crista acustica. Receptor cells of the proximal intermediate organ were most sensitive to frequencies below 10 kHz. They projected in anterior portions of the auditory neuropile, whereas cells of the distal intermediate organ had terminations spread over almost the whole auditory neuropile.     

Tonotopic organization of the ventrorostral zone of the auditory cortex region AII in cats

The tonotopic organization of the ventrorostral (VR) zone of cortical auditory area AII was investigated in acute experiments on cats anesthetized with nembutal and unanesthetized immobilized animals. Response with the lowest threshold arose in 92% of test neurons to presentation of one or several sound frequencies. The majority (54%) were "tuned" to one characteristic frequency (CF), 38% to several frequencies, and 8% had no clear-cut CF. A connection was found between location of a unit within the VR zone and its CF. Neurons with the highest CF were located in the ventrocaudal AII. An increase was noted in numbers of neurons with the lowest CF with increasing distance (rost-rally) from the VR location zone of neurons tuned to a high frequency. Going by response to acoustic stimuli of frequencies ranging between 1 and 24 kHz, length of the VR projection zone of the AII was found to measure 1.8–2.0 mm. Location of the test zone in relation to auditory cortex sulci varied substantially from one animal to the next.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 22, No. 2, pp. 178–184, March–April, 1990.     

Temporal processing and adaptation in the songbird auditory forebrain

Songbird auditory neurons must encode the dynamics of natural sounds at many volumes. We investigated how neural coding depends on the distribution of stimulus intensities. Using reverse-correlation, we modeled responses to amplitude-modulated sounds as the output of a linear filter and a nonlinear gain function, then asked how filters and nonlinearities depend on the stimulus mean and variance. Filter shape depended strongly on mean amplitude (volume): at low mean, most neurons integrated sound over many milliseconds, while at high mean, neurons responded more to local changes in amplitude. Increasing the variance (contrast) of amplitude modulations had less effect on filter shape but decreased the gain of firing in most cells. Both filter and gain changes occurred rapidly after a change in statistics, suggesting that they represent nonlinearities in processing. These changes may permit neurons to signal effectively over a wider dynamic range and are reminiscent of findings in other sensory systems.     

Tonotopic organization of the cochlear nucleus of the mustache bat,Pteronotus parnellii

Summary The tonotopic organization of the cochlear nucleus (CN) of the mustache bat, Pteronotus parnellii was studied by injecting horseradish peroxidase (HRP) in physiologically characterized CN-sites known to respond to a certain frequency. The tracer was transported by the branched fibers of the auditory nerve and bands of labeled terminals were found in each of the CN-subdivisions. Low to high frequencies are orderly represented in rostrocaudal direction in the anteroventral CN (AV) and in ventrodorsal direction in the posteroventral (PV) and dorsal CN (DCN). In all 3 subnuclei a vast overpresentation of the frequency band between 54–66 kHz, which includes the dominant second harmonic of the echolocation calls, is superimposed on this basic mammalian pattern of frequency representation. A deviation from the standard mammalian scheme of tonotopic arrangement is found in the cytoarchitecturally distinct marginal cell group (MA). This cell group extends in rostrocaudal direction along the medial margin of the AV, and the frequency representation in its most rostral 2 thirds is biased towards the low frequency range of the faint first harmonic of the echolocation call (24–32 kHz). Consequently the low frequencies lie adjacent to the regular slab organization of the range of higher frequencies represented in the AV. The temporal response patterns of MA neurons to tone stimuli are predominantly phasic or onset-types, in contrast to the primary like response type which prevails in the AV. The frequency representation and the physiological characteristics of the MA group can be relevant in the context of target range determination by echolocation.Abbreviations AV anteroventral cochlear nucleus - AV _a anterior part of AV - AV _p posterior part of AV - BF best frequency - CF constant frequency component of echolocation calls - CN cochlear nucleus - DAB diaminobenzidine - DCN dorsal cochlear nucleus - EP evoked potential - FM frequency modulated component of echolocation calls - HRP horseradish peroxidase - LSO lateral superior olive - IC inferior colliculus - MA marginal cell group - MAl lateral part of MA - MAm medial part of MA - OAE otoacoustic emission - PV posteroventral cochlear nucleus - PVl lateral part of PV - PV _m medial part of PV - PV _c caudal part of PV (octopus cell region) - RF resting frequency - SEOAE synchronous evoked OAE - TMB tetramethylbenzidine - VIII eight nerve     

Dominance, competition, and energetic reserves in the European starling, Sturnus vulgaris

We investigated the relationships between social dominance,competition for food, and strategies of body mass and fat regulationin the European starling (Sturnus vulgaris). In birds housedin groups of three, subdominant birds stored more fat than dominants.A removal experiment established a causal link between socialdominance and fat reserves; in groups that had the dominantindividual removed, the remaining birds reduced body mass andfat, relative to control groups that had the subordinate removed.In a second experiment, we investigated the influences of degreeof competition for food and dominance on body mass and fat reserves.Birds under high competition increased fat reserves and tendedto have higher body mass than birds under low competition. Theincrease in fat reserves was higher in the subdominants thanin the dominants. These results are consistent with hypothesesconcerning dominance-dependent access to food; subdominant birds,or birds under increased competition, may store more fat asan insurance against periods when food cannot be obtained. However,relations between dominance, body mass, and fat reserves mayalso arise through other proximate factors relating to dominance-dependentcosts and benefits of fat storage, such as predation risk andenergetic expenditure.     

Reverse lateralization of visual discriminative abilities in the European starling

Previous experiments on visual feature discrimination abilities have consistently shown a right-eye system lateralization in pigeons, Columba livia, and young domestic chickens, Gallus gallus domesticus, both nonpasserine species. Recently, however, it has been shown that photoreceptor distribution in the left and right retinas are asymmetrical in the European starling, Sturnus vulgaris, a passerine species. Single cone receptors are significantly more abundant in the left retina, which suggests that starlings should perform visual discrimination tasks more proficiently with the left eye, in contrast to previous findings with nonpasserines. We tested this hypothesis using the technique of monocular occlusion. In the first experiment, starlings were tested on a simultaneous visual discrimination task in three conditions: binocular (both eyes), left monocular (left eye only) and right monocular (right eye only). Subjects in the binocular and left-monocular conditions achieved significantly higher performance scores on the discrimination task than birds in the right-monocular condition. A second experiment found similar results, with birds in the left-monocular condition learning the discrimination task more than twice as quickly as those in the right-monocular condition. Subsequent tests with the alternative eye for both groups indicated no interocular transfer. These findings suggest that visual discriminative abilities in starlings are asymmetrical, and that they are lateralized in the opposite eye system than has been reported for all other species tested to date.     

Tonotopic organisation of the auditory organ of the locustValanga irregularis (Walker)

Summary The responses to pure tone stimuli of individual auditory receptors in the locustValanga irregularis were quantified and the location of receptors within the auditory organ identified through the intracellular injection of Lucifer Yellow. Three groups of receptors were identified and classified according to their site of attachment to the tympanic membrane (Gray 1960). Group a cells were attached to the elevated process and were tuned to sound frequencies from 4 to 6 kHz (Fig. 2). Group c cells were attached to the folded body and were tuned to sound frequencies from 2 to 3.5 kHz (Fig. 3). Group d cells were attached to the pyriform vesicle and were tuned to sound frequencies from 14 to 25 kHz (Fig. 4). The receptor cell bodies belonging to these groups were separated into three distinct regions of the auditory organ (Fig. 5). There was no evidence of any tonotopic organisation within the three groups (Fig. 6). These data therefore support the conclusion that the receptors within the auditory organ of the locust are organized into specific physiological groups (Michelsen 1971a) and thus suggest that the mechanics of the auditory apparatus may indeed play a role in defining the tuning of the receptors.     

Ectoparasitism and the role of green nesting material in the European starling

Summary The use of green nesting material is widespred among birds. Recent evidence suggests that birds use secondary chemicals contained in green plants to control ectoparasites. We manipulated green nesting material and ectoparasites of European starlings (Sturnus vulgaris) to test two hypotheses: (1) ectoparasites adversely affect prefledging survival and morphometrics or postfledging survival, and (2) green nesting material ameliorates the effects of ectoparasites. We recorded fat score, numbers of scabs, tarsal length, body mass, and hematocrit level on each nestling 17 days after hatching. We also fitted each nestling with unique patagial tags and resighted the starlings for 6–8 weeks after fledging to estimate survival and sighting rates. Nests devoid of green nesting material and dusted with the insecticide, carbaryl, had fewer high ectoparasite infestations, and nestlings had significantly lower scab scores, and significantly higher body masses than nestlings in undusted boxes. However, there was no difference in postfledging survival between birds from carbaryl-treated and undusted nests. There also was no difference in prefledging survival and morphometrics or postfledging survival between nestlings from boxes with and without green nesting material. These results do not support the hypothesis that starlings use green nesting material to control nest ectoparasites. We suggest an alternative hypothesis; green nesting material is used for mate selection or pairbonding in the starling.     

Tonotopic organization of the dorsocaudal zone of cortical area aii in the cat

The tonotopic organization of the dorsocaudal (DC) auditory cortex area AII was investigated during acute experiments on cats anesthetized with Nembutal. A capacity for selective response to presentation of auditory stimuli at a certain frequency was found in 93% of the neurons investigated. It was further observed that 75% of these cells were characterized by their fine tuning to one characteristic frequency (CF), the remaining 26% had several CF, and 7% reacted with a spike response to acoustic stimulation at all test frequencies and had no clearcut CF. A relationship was found between the location of a unit within the DC zone and its CF level. Neurons with the lowest CF were located in the upper position of the sylvian gyrus near the posterior ectosylvian sulcus. The CF of neurons rose progressively in step with increasing distance between the site of microelectrode recording and the low frequency focus of the DC zone travelling along the sylvian gyrus in a ventrorostral direction. Distance between low and high frequency foci of the DC zone measured 2.5–3.5 mm. Location of this zone in relation to the auditory cortex sulci varied considerably from one animal to another. Neurons with similar CF levels and arranged on this basis in vertical cortical columns could vary substantially in the dimensions of their receptive fields, sharpness of tunining to their own CF, and firing response pattern.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 20, No. 2, pp. 220–227, March–April, 1988.     

Green nesting material has a function in mate attraction in the European starling

The function of fresh green nest material has long been debated. It has been suggested that it reduces the number of ectoparasites in nests and on nestlings (nest protection hypothesis), or is used by males to signal condition and paternal quality (male quality hypothesis) or is used as a sexually selected ornament to attract females (courtship hypothesis). We simultaneously tested these three hypotheses in the European starling, Sturnus vulgaris, in the field. Green material was carried by male starlings only, and mainly during nest building. It was not used to reduce ectoparasites. Males nesting in nestboxes that were experimentally contaminated with ectoparasites did not carry more green nest material than males nesting in control boxes, and experimental removal and addition of green material had no effect on the number of ectoparasites on the nestlings or on their body mass. Furthermore, the amount of green material carried into a nestbox was not associated with male body mass, paternal incubation attendance or nestling food provisioning. There is two-fold experimental evidence that males use green plant material to attract mates. First, removal of greenery resulted in a significantly lower percentage of nestboxes containing a clutch than the control or addition treatment. Second, unpaired male starlings sang more and carried more greenery into a nestbox when a caged female was positioned adjacent to the nestbox than when a caged male or an empty cage was present. Paired males, when subjected to the same experimental design, did not respond.     

Realized vs apparent reduction in enemies of the European starling

Release from parasites, pathogens or predators (i.e. enemies) is a widely cited ‘rule of thumb’ to explain the proliferation of nonindigenous species in their introduced regions (i.e. the ‘enemy release hypothesis’, or ERH). Indeed, profound effects of some parasites and predators on host populations are well documented. However, some support for the ERH comes from studies that find a reduction in the species richness of enemies in the introduced range, relative to the native range, of particular hosts. For example, data on helminth parasites of the European starling in both its native Eurasia and in North America support a reduction of parasites in the latter. However, North American ‘founder’ starlings were likely not chosen randomly from across Eurasia. This could result in an overestimation of enemy release since enemies affect their hosts on a population level. We control for the effects of subsampling colonists and find, contrary to previous reports, no evidence that introduced populations of starlings experienced a reduction in the species richness of helminth parasites after colonization of North America. These results highlight the importance of choosing appropriate contrast groups in biogeographical analyses of biological invasions to minimize the confounding effects of ‘propagule biases’.     

Carbonic anhydrase activity in kidney and lower intestine of the European starling

A histochemical investigation of kidney and lower intestine of the European starling (Sturnus vulgaris) shows no carbonic anhydrase activity in proximal convoluted tubules, although activity is seen in similarly prepared sections of rat proximal tubules. Early distal tubule cells in the starling are stained throughout the cytoplasm and at the apical and highly infolded basolateral membranes. Late distal tubules lose apical activity and have reduced basolateral infolding, resulting in less intense staining. Darkly stained intercalated cells appear in the connecting tubules and cortical collecting ducts. Both of these segments also show intense basolateral staining. Medullary cones of the starling are highly organized, with central zones containing unstained thin descending limbs of loops of Henle, surrounded by both medullary collecting ducts with only scattered cells staining for enzyme, and by thick ascending limb segments. The latter contain many uniformly stained cells intermingled with occasional unstained cells. Scattered cells of the starling colonic villi demonstrate intense apical brush border membrane staining as well as cytoplasmic staining. Cells lining the cloaca stain less intensely. A biochemical assay for carbonic anhydrase was used to quantify enzyme activity in these tissues. Starling kidney contained 1.96 ± 0.33 (mean ± SEM) enzyme units/mg protein, less than half the activity seen in rat kidney. Stripped colonic epithelium contained 0.66 ± 0.15 enzyme units/mg protein. These quantitative results correlate well with the interpretations derived from the histochemical observations. The lack of proximal tubule carbonic anhydrase activity suggests that the avian kidney relies more on distal nephron segments to achieve net acidification of the urine.     

Sex-differentiated migration patterns, protandry and phenology in North European songbird populations

This study aims to investigate causes and mechanisms controlling protandrous migration patterns (the earlier breeding area arrival of males relative to females) and inter-sexual differences in timing of migration in relation to the recent climate-driven changes in phenology. Using standardised ringing data from a single site for eight North European migratory passerines collected throughout 22 years, we analysed sex-differentiated migration patterns, protandry and phenology of the entire populations. Our results show protandrous patterns for the first as well as later arriving individuals for all studied species. Males show more synchronous migration patterns compared to females and, hence, first arriving females followed males more closely than later arriving individuals. However, we found no inter-sexual differences in arrival trends as both sexes advance spring arrival over time with the largest change for the first arriving individuals. These findings seem in support of the “mate opportunity” hypothesis, as the arrival of males and females is strongly coupled and both sexes seem to compete for early arrival. Changes in timing of arrival in males and females as a response to climatic changes may influence subsequent mating decisions, with subsequent feedbacks on population dynamics such as reproductive success and individual fitness. However, during decades of consistent earlier spring arrival in all phases of migration we found no evidence of inter-sexual phenological differences.     

Computational models of temporal processing in the auditory thalamus

Previous work has shown that neurons in the medial geniculate body (MGB) of the echolocating bat, Myotis lucifugus, display response properties that are distinguishable from those of their afferents in the inferior colliculus (IC). Specifically, MGB neurons display phasic temporal discharge patterns, poor entrainment to trains of constant-amplitude sound pulses, and facilitated responses to amplitude-modulated trains of sound pulses (Llano and Feng 1999). In this study we used a modeling approach to examine the relative contributions of different known sources of inhibition on the temporal response properties of auditory thalamocortical neurons. We found that GABA_A-mediated post-excitatory inhibition resulting from coactivation of thalamocortical neurons and local inhibitory interneurons (in a triadic arrangement) is sufficient to reproduce many of the temporal response properties of MGB neurons. Addition of long-duration GABA_B-mediated inhibition gave the thalamocortical neuron temporal response characteristics that more closely resemble those seen in the experimental data. Neither recurrent inhibition from the thalamic reticular nucleus nor post-synaptic nonlinear mechanisms were necessary to reproduce the temporal transformations between the IC and MGB. This work suggests that feed-forward inhibitory circuitry, coupled with slow GABA_B-mediated inhibition, can emulate temporal information processing at the MGB. The transformation taking place in the MGB can be used to extract salient features from complex, time-varying stimuli, such as echoes returning from moving prey. Received: 11 August 1999 / Accepted in revised form: 5 April 2000     

Gap detection in the European starling (Sturnus vulgaris)

Summary Gap-detection thresholds were determined for single units in the cochlear ganglion and in auditory nerve fibres of the starling from responses to two broad-band noise bursts separated by a temporal gap of between 0.4 and 204.8 ms. All 35 units showed a threshold within the range of gap sizes tested. The median minimum-detectable gap was 12.8 ms with the minimum being 1.6 ms. A multiple regression analysis revealed that the size of the minimum-detectable gap was not significantly correlated with the neuron's CF, with its sharpness of tuning as given by its bandwidth 10 dB above threshold, or with its Q_10dB value. Only the level of stimulation above the neuron's threshold showed a significant negative correlation with the size of the minimum-detectable gap. These results are discussed with respect to theoretical considerations of limits posed on temporal resolution by the characteristics of peripheral filters. These findings are also discussed in the context of the coding of gaps at different levels of the starling's auditory system and in relation to psychoacoustic results in the starling on gap detection and time resolution described by temporal modulation transfer functions.