Cytoarchitecture of the medial nucleus of trapezoid body of three neotropical species of bats (Noctilio leporinus, Phyllostomus hastatus, and Carollia perspicillata) with different foraging behavior / Citoarquitetura do núcleo medial do corpo trapezoidal de três espécies neotropicais de morcegos (Noctilio leporinus, Phyllostomus hastatus e Carollia perspicillata) com diferentes comportamentos de forrageamento

Abstract The present study was taken to test the hypothesis that the medial nucleus of the trapezoid body (MNTB) of echolocating neotropical bats with different foraging behavior will exhibit morphological variations in relative size, degree of complexity and spatial distribution. The brains were collected from six male adult bats of each species: Noctilio leporinus (fish-eating), Phyllostomus hastatus (carnivorous/ omnivorous) and Carollia perspicillata (fruit-eating) and were double-embedded and transverse serial sections were cut and stained with cresyl fast violet. The results showed that the MNTB is well developed in all the bats in general and the mean length of the MNTB was 1160 ± 124 µm in N. leporinus, 400 ± 59 µm in P. hastatus and 320 ± 25µm in C. perspicillata. The body and brain weight do not reflect proportionately on the size of the MNTB in the present study. The hearing frequency spectrum did not covary with the size of the MNTB among the bats studied. The MNTB is clearly demarcated from the ventral nucleus of the trapezoid body (VNTB) only in P. hastatus. The MNTB comprised mainly three types of cells in all three bats: dense-staining multipolar cells (12.5 µm and 25.0 µm diameter); light-staining multipolar cells measuring (12.5 µm and 25.0 µm diameter) and light-staining round cells (5.0 µm diameter). The large sized MNTB was observed in N. leporinus, which suggests that it relies heavily on echolocation whereas P. hastatus and C. perspicillata use echolocation as well but also rely on hearing, smell and vision.

Resumo O presente estudo foi realizado para testar a hipótese de que o núcleo medial do corpo trapezoide (MNTB) de morcegos neotropicais ecolocativos com comportamento forrageiro diferente apresenta variações morfológicas no tamanho relativo, grau de complexidade e distribuição espacial. Os cérebros foram coletados de seis morcegos machos adultos de cada espécie, Noctilio leporinus (comedor de peixe), Phyllostomus hastatus (carnívoro/onívoro) e Carollia perspicillata (comedor de frutas), e foram seccionados em série e seções seriais transversais duplas e coradas com cresil violeta. Os resultados mostraram que o MNTB é bem desenvolvido em todos os morcegos em geral e que o comprimento médio do MNTB foi de 1.160 ± 124 µm em N. leporinus, 400 ± 59 µm em P. hastatus e 320 ± 25 µm em C. perspicillata. O peso corporal e cerebral não reflete proporcionalmente o tamanho do MNTB no presente estudo. O espectro da frequência auditiva não covaria com o tamanho do MNTB entre os morcegos estudados. O MNTB é claramente demarcado do núcleo ventral do corpo trapezoidal (VNTB) apenas em P. hastatus. O MNTB compreendia principalmente três tipos de células nos três morcegos: células multipolares de coloração densa (12,5 µm e 25,0 µm de diâmetro), células multipolares de coloração clara (12,5 µm e 25,0 µm de diâmetro) e células redondas manchadas de luz (5,0 µm de diâmetro). O MNTB de grande porte foi observado em N. leporinus, o que sugere que ele depende muito da ecolocalização, enquanto P. hastatus e C. perspicillata também usam a ecolocalização, mas dependem da audição, olfato e visão.

Cytoarchitecture of the superior olivary complex of three neotropical species of bats (Noctilio leporinus, Phyllostomus hastatus and Carollia perspicillata) with different foraging behavior / Citoarquitetura do complexo olivar superior de três espécies neotropicais de morcegos (Noctilio leporinus, Phyllostomus hastatus e Carollia perspicillata) com diferentes comportamentos de forrageamento

Abstract The understanding of the echolocation by studying different auditory nuclei of echolocating bats can be an important link in elucidating questions arising in relation to their foraging behavior. The superior olivary complex (SOC) is the primary center for processing the binaural cues used in sound localization since echo locating bats rely on acoustic cues to navigate and capture prey while in flight. The present study was taken to test the hypothesis that the SOC of echolocating neotropical bats with different foraging behavior will exhibit morphological variations in relative size, degree of complexity and spatial distribution. The brains were collected from six male adult bats of each species: Noctilio leporinus (fish eating), Phyllostomus hastatus (carnivorous/omnivorous) and Carollia perspicillata (fruit eating). They were double-embedded and transverse serial sections were cut and stained with cresyl fast violet. The SOC measured as 640 ± 70 µm in the N. leporinus bat, 480 ± 50 µm in the P. hastatus and 240 ± 30 µm in the C. perspicillata bat. The principal nuclei of the SOC of in all three bats were the LSO, MSO and MNTB. The MSO and LSO were very well developed in N. leporinus bats. The MSO of N. leporinus bat subdivided into DMSO and VMSO. The main cell type of cells present in MSO and LSO are dark staining multipolar cells in all the bats studied. The well-developed MSO and LSO of N. leporinus bats indicate that these bats are highly sensitive to low frequency sounds and interaural intensity differences, which help these bats to forage over water by using various types of echolocation signals. The average size of SOC in P. hastatus and C. perspicillata bats can be attributed to the fact that these bats use vision and smell along with echolocation to forage the food.

Resumo O entendimento da ecolocalização pelo estudo de diferentes núcleos auditivos de morcegos pode ser um elo importante na elucidação das inúmeras questões que surgem em relação ao seu comportamento de forrageamento. O complexo olivar superior (SOC) é o principal centro de processamento das pistas binaurais usadas na localização do som, já que os morcegos ecolocalizadores contam com sinais acústicos para navegar e capturar as presas durante o vôo. O presente estudo foi realizado para testar a hipótese de que morcegos que usam a ecolocalização para diferentes comportamentos de forrageamento irão variar na estrutura, tamanhos relativos e grau de complexidade e distribuição espacial do grupo SOC. Os cérebros foram coletados de seis machos adultos de morcego de cada espécie: Noctilio leporinus (piscívoro), Phyllostomus hastatus (carnívoros/onívoros) e Carollia perspicillata (frugívoro). Eles foram seccionados em série e transversalmente, cortados e corados com coloração rápida cresil-violeta. tolet. O grupo SOC foi medido como 640 ± 70 µm no morcego N. leporinus, 480 ± 50 µm no P. hastatus e 240 ± 30 µm no morcego C. perspicillata. Os principais núcleos do grupo SOC dos três morcegos foram o LSO e o MSO e o MNTB. O MSO e o LSO foram muito bem desenvolvidos em morcegos N. leporinus. A MSO de N. leporinus foi subdividida em DMSO e VMSO. O principal tipo de células presentes na MSO e LSO são as células multipolares de coloração escura em todos os morcegos. Os MSO bem desenvolvidos e LSO de morcegos N. leporinus indicam que estes morcegos são altamente sensíveis a sons de baixa frequência e diferenças de intensidade interaural, que ajudaram estes morcegos a se alimentarem na superfície da água usando vários tipos de sinais de ecolocalização. O tamanho médio de SOC em morcegos de P. hastatus e C. perspicillata pode ser atribuído ao fato destes morcegos usarem visão e olfato junto com a ecolocalização para forragear.

Research progress in neurophysiological mechanism underlying distinguishing plants through classification of echoes in frequency modulation bats / 生理学报

By using echolocation system echolocating bats have the ability to complete the tasks of detection, localization and classification of the targets. Among the three fundamental tasks, the study of how bats use echolocation to classify targets was investigated later, and most of previous studies were focused on the analysis of simple targets. However, the echoes that bats received are mostly returning from complex objects or structures, which are so complex that they must be described by stochastic statistical approach. In recent years, the study on classification of complex echoes returning from different plants in frequency modulation (FM) bats has made significant progress. In this review article, we will briefly introduce and comment on some progress of studies based on the behavioral evidence, acoustic cues, relevant classification models, and neural bases underlying different classification cues to distinguish plants through classification of echoes in FM bats.

Infection of the heart of Pimelodus ornatus (Teleostei, Pimelodidae), by Myxobolus sp. (Myxozoa, Myxobolidae) / Infecção do tecido cardíaco de Pimelodus ornatus (Teleostei, Pimelodidae), por Myxobolus sp. (Myxozoa, Myxobolidae)

The phylum Myxozoa Grassé, 1970, consists of a heterogenous group of around 50 genera that are worldwide disseminated in a wide variety of aquatic media. In the present study, 43 specimens of Pimelodus ornatus were collected from an adjacent area to the Cachoeira do Arari municipality on Marajó Island, in the Brazilian state of Pará, in 2013. Macroscopic analysis showed the presence of whitened plasmodia located in the cardiac muscle and also in the region between the bulbus arteriosus and atrium cordis. Microscopic analysis on the parasitized tissues revealed spores that were typically piriform, with the anterior portion slightly narrower than the posterior end. The spore valves were symmetrical. The present species is placed in the genus Myxobolus Butschli, 1882, because of the presence of a pair of equal polar capsules in each spore. The prevalence of parasitism observed was 13.9% (6/43). This research note reports the first occurrence of Myxobolus as a parasite of the heart in the teleostean fish P. ornatus in the Amazon region and confirms the occurrence of secondary myocarditis in this fish, caused by parasitism by Myxobolus sp. The rarity of this parasitic species of Myxobolus at this tissue site, associated with other spore morphology characteristics in the fish, suggests that it is an undescribed species.

O filo Myxozoa Grassé, 1970, consiste em um grupo heterogêneo de cerca de 50 gêneros que são disseminados em todo o mundo em uma grande variedade de meios aquáticos. No presente estudo, quarenta e três espécimes de Pimelodus ornatus foram coletados a partir de uma área adjacente à cidade de Cachoeira do Arari, na Ilha do Marajó, no Estado do Pará, em 2013. À análise macroscópica verificou-se a presença de plasmódios esbranquiçados, localizados no músculo cardíaco e também na região entre o bulbus arteriosus e o atrium cordis. A análise microscópica dos tecidos parasitados revelou esporos que eram tipicamente piriformes, com a porção anterior um pouco mais estreita do que a extremidade posterior, sendo suas válvulas simétricas. A prevalência do parasitismo observada foi de 13,9% (6/43). Esta nota de pesquisa relata a primeira ocorrência de Myxobolus como um parasita do coração no peixe teleósteo P. ornatus, na Região Amazônica e, confirma a ocorrência de miocardite secundária causada por esse parasitismo. A raridade da ocorrência de Myxobolus sp. neste tecido, associado a outras características morfológicas dos esporos no peixe, sugere que é uma espécie não descrita.

The role of the ventral nucleus of the lateral lemniscus in sound signal processing and auditory ascending transmission / 生理学报

The ventral nucleus of the lateral lemniscus (VNLL) is an important nucleus in the central auditory pathway which connects the lower brainstem and the midbrain inferior colliculus (IC). Previous studies have demonstrated that neurons in the VNLL could respond to sound signal parameters. Frequency tuning curves (FTCs) of VNLL neurons are generally wider than FTCs of IC neurons, suggesting that the VNLL does not enhance abilities of frequency discrimination and coding. Two types of rate-intensity functions (RIFs) are found in the VNLL: monotonic and non-monotonic RIFs. Intensity-tuning of VNLL neurons are affected by the temporal firing patterns during processing and encoding intensity. There are multiple temporal firing patterns in VNLL neurons. Onset pattern has a precise timing characteristic which is well suited to encode temporal features of stimuli, and also very important to animal behavior including bat's echolocation. The VNLL accepts inputs from lower nuclei, uploads glycine inhibitory outputs to IC, and modulates response characteristics generating and acoustic signal processing of IC neurons. Recent research suggests that fast inhibitory projection from the VNLL may delay the first spike latency of IC neurons, and the delayed inhibitory projection from the VNLL may mediate the temporal firing patterns of IC neurons. But how inhibitory inputs from the VNLL integrate in IC, and how inhibitory inputs from the VNLL enhance the ability of detecting sound signal of IC neurons are not very clear and need more direct evidence at the level of neurons. These questions will help further understand the role of upload during IC processes acoustic signal, which are our research target in the future. This article reviews the current literature regarding the roles of the VNLL in sound signal processing and the auditory ascending transmission, including advances in the relevant research in our laboratory.

Perception and selectivity of sound duration in the central auditory midbrain / 生理学报

Sound duration plays important role in acoustic communication. Information of acoustic signal is mainly encoded in the amplitude and frequency spectrum of different durations. Duration selective neurons exist in the central auditory system including inferior colliculus (IC) of frog, bat, mouse and chinchilla, etc., and they are important in signal recognition and feature detection. Two generally accepted models, which are "coincidence detector model" and "anti-coincidence detector model", have been raised to explain the mechanism of neural selective responses to sound durations based on the study of IC neurons in bats. Although they are different in details, they both emphasize the importance of synaptic integration of excitatory and inhibitory inputs, and are able to explain the responses of most duration-selective neurons. However, both of the hypotheses need to be improved since other sound parameters, such as spectral pattern, amplitude and repetition rate, could affect the duration selectivity of the neurons. The dynamic changes of sound parameters are believed to enable the animal to effectively perform recognition of behavior related acoustic signals. Under free field sound stimulation, we analyzed the neural responses in the IC and auditory cortex of mouse and bat to sounds with different duration, frequency and amplitude, using intracellular or extracellular recording techniques. Based on our work and previous studies, this article reviews the properties of duration selectivity in central auditory system and discusses the mechanisms of duration selectivity and the effect of other sound parameters on the duration coding of auditory neurons.

Sound duration and sound pattern affect the recovery cycles of inferior collicular neurons in leaf-nosed bat, Hipposideros armiger / 生理学报

The effects of sound duration and sound pattern on the recovery cycles of inferior collicular (IC) neurons in constant frequency-frequency modulation (CF-FM) bats were explored in this study. Five leaf-nosed bats, Hipposideros armiger (4 males, 1 female, 43-50 g body weight), were used as subjects. The extracellular responses of IC neurons to paired sound stimuli with different duration and patterns were recorded, and the recovery was counted as the ratio of the second response to the first response. Totally, 169 sound-sensitive IC neurons were recorded in the experiment. According to the interpulse interval (IPI) of paired sounds when neurons reached 50% recovery (50% IPI), the recovery cycles of these IC neurons were classified into 3 types: fast recovery (F, the 50% IPI was less than 15 ms), short recovery (S, the 50% IPI was between 15.1 and 30 ms) and long recovery (L, the 50% IPI was more than 30 ms). When paired CF stimuli with 2 ms duration was used, the ratio of F neurons was 32.3%, and it decreased to 18.1% and 18.2% respectively when 5 and 7 ms CF stimuli were used. The ratios of S and L neurons were 41.5%, 33.7%, 29.1% and 26.2%, 48.2%, 52.7% respectively when 2, 5 and 7 ms CF stimuli were used. The average 50% IPI determined after stimulation with paired 2 ms, 5 ms and 7 ms CF sounds were (30.2 ± 27.6), (39.9 ± 29.1) and (49.4 ± 34.7) ms, respectively, and the difference among them was significant (P< 0.01). When the stimuli of paired 2 ms CF sounds were shifted to paired 2 ms FM sounds, the proportion of F, S and L neurons changed from 32.3%, 41.5%, 26.2% to 47.7%, 24.6%, 27.7%, respectively, and the average 50% IPI decreased from (30.2 ± 27.6) to (23.9 ± 19.0) ms (P< 0.05, n = 65). When paired 5+2 ms CF-FM pulses were used instead of 7 ms CF sounds, the proportion of F, S and L neurons changed from 18.2%, 29.1%, 52.7% to 29.1%, 27.3%, 43.6%, respectively, and the average 50% IPI decreased from (49.4 ± 34.7) to (36.3 ± 29.4) ms (P< 0.05, n = 55). All these results suggest that the CF and FM components in echolocation signal of CF-FM bats play different roles during bats' hunting and preying on. The FM component of CF-FM signal presenting in the terminal phase can increase the number of F type neurons and decrease the recovery cycles of IC neurons for processing high repetition echo information, which ensures the bat to analyze the target range and surface texture more accurately.

GABAergic inhibition modulates intensity sensitivity of temporally patterned pulse trains in the inferior collicular neurons in big brown bats / 生理学报

The echolocating big brown bats (Eptesicus fuscus) emit trains of frequency-modulated (FM) biosonar signals with duration, amplitude, repetition rate, and sweep structure changing systematically during interception of their prey. In the present study, the sound stimuli of temporally patterned pulse trains at three different pulse repetition rates (PRRs) were used to mimic the sounds received during search, approach, and terminal stages of echolocation. Electrophysiological method was adopted in recordings from the inferior colliculus (IC) of midbrain. By means of iontophoretic application of bicuculline, the effect of GABAergic inhibition on the intensity sensitivity of IC neurons responding to three different PRRs of 10, 30 and 90 pulses per second (pps) was examined. The rate-intensity functions (RIFs) were acquired. The dynamic range (DR) of RIFs was considered as a criterion of intensity sensitivity. Comparing the average DR of RIFs at different PRRs, we found that the intensity sensitivity of some neurons improved, but that of other neurons decayed when repetition rate of stimulus trains increased from 10 to 30 and 90 pps. During application of bicuculline, the number of impulses responding to the different pulse trains increased under all stimulating conditions, while the DR differences of RIFs at different PRRs were abolished. The results indicate that GABAergic inhibition was involved in modulating the intensity sensitivity of IC neurons responding to pulse trains at different PRRs. Before and during bicuculline application, the percentage of changes in responses was maximal in lower stimulus intensity near to the minimum threshold (MT), and decreased gradually with the increment of stimulus intensity. This observation suggests that GABAergic inhibition contributes more effectively to the intensity sensitivity of the IC neurons responding to pulse trains at lower sound level.

Effects of backward masking on the responses of the inferior collicular neurons in the big brown bat, Eptesicus fuscus / 生理学报

Temporal features of sound convey information vital for behaviors as diverse as speech recognition by human and echolocation by bats. However, auditory stimuli presented in temporal proximity might interfere with each other. Although much progress has been made in the description of this phenomenon from psychophysical studies, the neural mechanism responsible for its formation at central auditory structures especially at the inferior colliculus (IC), a midbrain auditory nucleus which practically receives massive bilateral projections from all the major auditory structures in the brainstem, remains unclear. This study was designed to investigate it in vivo by using electrophysiological recording from the inferior collicular neurons of the big brown bat, Eptesicus fuscus. In our results, the responses of 12 (38%, n= 31) neurons to the test sound (leading sound) were obviously inhibited by the masker (lagging sound). The inhibitory effects in these neurons were correlated with the inter-stimulus level difference (SLD) and the inter-stimulus onset asynchrony (SOA) interval. The strength of backward masking increased with the masker intensity increasing, the test sound intensity decreasing and the SOA interval shortening. There were no obvious effects of backward masking on the responses of many other neurons (52%, 16/31), and yet in a part of these neurons, the neural inhibition of responses to the test sound was observed at the special SLD and the special SOA intervals. Moreover, few of the 31 sampled IC neurons (10%, 3/31) displayed facilitating responses to the test sound at the special SLD and the special SOA intervals. These data demonstrate that a lot of IC neurons are involved in the generation of the backward masking of acoustical perception. It is conjectured that the temporal dynamic integration between the leading inhibitory inputs evoked by the masker sound and the excitatory inputs evoked by the test sound might play a key role in shaping the acoustical response characteristics of the IC neurons.

Combination sensitivity and processing of communication calls in the inferior colliculus of the Moustached Bat Pteronotus parnellii

Muitos animais usam gritos de comunicação complexos nos seus comportamentos sociais. Sabemos em algumas espécies quais parâmetros dos gritos estimulam determinados comportamentos, mas não entendemos como o sistema auditivo codifica os gritos. Tampouco entendemos os mecanismos subjacentes à seletividade neural aos gritos. Nossos estudos do mesencéfalo auditivo do morcego Pteronotus parnellii revelaram um mecanismo neural importante para produzir respostas seletivas aos gritos. Neurônios que integram informação proveniente de várias freqüências diversas mostram seletividade a gritos de comunicação. "Sensibilidade a combinaçäes" de freqüências pode ser um mecanismo comum para codificar sons complexos, já que é importante também para codificar sinais de ecolocação.

Causes and consequences of song amplitude adjustment in a territorial bird: a case study in nightingales

A amplitude vocal, um dos fatores cruciais para a troca de sinais acústicos, tem sido negligenciada nos estudos da comunicação animal, mas trabalhos recentes sobre a variação do canto do Rouxinol-comum Luscinia megarhynchos evidenciaram sua importância no comportamento de canto das aves territoriais. No rouxinol a amplitude do canto não é aumentada ao máximo per se, mas é regulada individualmente de acordo com o nível de ruído de fundo que mascara o sinal. As aves também ajustam sua intensidade vocal às variáveis sociais, tais como nas interaçäes entre machos. Além disso, durante essas interaçäes, os machos tiram proveito da direcionalidade de seus cantos para emiti-los em direção aos receptores desejados no intuito de garantir a mais eficiente transmissão do sinal. Estudos do desenvolvimento desta sinalização típica de longo alcance sugerem que o nível sonoro seja altamente relacionado com o desenvolvimento geral e a aprendizagem, e deveria portanto ser visto como parte integrante da ontogenia do canto. Concluímos que a amplitude do canto é um parâmetro dinâmico do sistema de sinalização em aves, que é regulado individualmente de acordo com as exigências ecológicas da transmissão do sinal e o contexto social da comunicação.