Interaural Pathway Research Articles

Redescription of the oldest crown clade penguin: cranial osteology, jaw myology, neuroanatomy, and phylogenetic affinities of Madrynornis mirandus

ABSTRACTMadrynornis mirandus, one of the few fossil penguins known from a nearly complete articulated skeleton, represents a key taxon for understanding the stem-crown transition in penguins. Despite the wealth of morphological character data preserved in the holotype specimen, the phylogenetic placement of this early late Miocene taxon has remained controversial. Reexamination of the Madrynornis mirandus holotype provides support for placement within the penguin crown clade. However, this placement is highly sensitive to the molecular signal and Madrynornis falls just outside the crown clade when molecular data are excluded. The neuroanatomy of Madrynornis shares many derived features with extant penguins, including an airencephalic brain shape, highly reduced bulbus olfactorius, and absence of an interaural pathway. However, the brain endocast differs from all surveyed extant species in that the eminentia sagittalis (wulst) is less caudally expanded, the tectum opticus is relatively less developed, and the flocculus is stouter and more laterally disposed. The cranial osteology and reconstructed jaw myology of Madrynornis suggest a primarily piscivorous diet, which likely characterizes the clade uniting Madrynornis, Inguza, Eudyptula, and Spheniscus.SUPPLEMENTAL DATA—Supplemental materials are available for this article for free at www.tandfonline.com/UJVPCitation for this article: Degrange, F. J., D. T. Ksepka, and C. P. Tambussi. 2018. Redescription of the oldest crown clade penguin: cranial osteology, jaw myology, neuroanatomy, and phylogenetic affinities of Madrynornis mirandus. Journal of Vertebrate Paleontology. DOI: 10.1080/02724634.2018.1445636.

Endocranial anatomy of Antarctic Eocene stem penguins: implications for sensory system evolution in Sphenisciformes (Aves)

ABSTRACTPenguins have a more than 60 million year long evolutionary history. Thus, stem lineage fossil taxa are key to understanding their evolution. Here, we present data on three virtual endocasts from stem penguin skulls collected from the Eocene La Meseta Formation of Seymour Island (Antarctica), along with comparative data from extant penguins and outgroups. These fossils appear to belong to three distinct species, and represent both the oldest (34.2 Ma) and the most basal penguin taxa that have yielded endocast data. Data collected from the fossils provide new support for several important shifts in neuroanatomy and cranial skeletal anatomy along the transition from stem to crown penguins, including (1) caudal expansion of the eminentia sagittalis, (2) an increase in the overlap of the telencephalon onto the cerebellum, (3) reduction of the bulbus olfactorius, and (4) loss of the interaural pathway. The large semicircular canal diameters of the Antarctic fossils as well as the more crownward stem penguin Paraptenodytes antarcticus together suggest that canal size increased in basal penguins relative to outgroup taxa but later decreased near the crown radiation. As in most other wing-propelled diving birds, the endocasts lack evidence of cerebellar folds and possess a relatively large floccular recess. Several aspects of the endocast morphology, including the exposure of the tectum opticum in dorsal view and the rostral displacement of the eminentia sagittalis away from the border of the cerebellum, are seen neither in crown penguins nor in Procellariiformes (the extant sister clade to Sphenisciformes) and so appear to represent unique characters of these stem taxa.

Evolution of the brain and sensory organs in Sphenisciformes: new data from the stem penguin Paraptenodytes antarcticus

Penguins have undergone dramatic changes associated with the evolution of underwater flight and subsequent loss of aerial flight, which are manifest and well documented in the musculoskeletal system and integument. Significant modification of neurosensory systems and endocranial spaces may also be expected along this locomotor transition. However, no investigations of the brain and sensory organs of extinct stem lineage Sphenisciformes have been carried out, and few data exist even for extant species of Spheniscidae. In order to explore neuroanatomical evolution in penguins, we generated virtual endocasts for the early Miocene stem penguin Paraptenodytes antarcticus, three extant penguin species (Pygoscelis antarctica, Aptenodytes patagonicus, Spheniscus magellanicus), and two outgroup species (the common loon Gavia immer and the Laysan albatross Phoebastria immutabilis). These endocasts yield new anatomical data and phylogenetically informative characters from the brain, carotid arteries, pneumatic recesses, and semicircular canal system. Despite having undergone over 60 million years of evolution since the loss of flight, penguins retain many attributes traditionally linked to flight. Features associated with visual acuity and proprioception, such as the sagittal eminence and flocculus, show a similar degree of development to those of volant birds in the three extant penguins and Paraptenodytes antarcticus. These features, although clearly not flight-related in penguins, are consistent with the neurological demands associated with rapid manoeuvring in complex aquatic environments. Semicircular canal orientation in penguins is similar to volant birds. Interestingly, canal radius is grossly enlarged in the fossil taxon Pa. antarcticus compared to living penguins and outgroups. In contrast to all other living birds, the contralateral anterior tympanic recesses of extant penguins do not communicate. An interaural pathway connecting these recesses is retained in Pa. antarcticus, suggesting that stem penguins may still have employed this connection, potentially to enhance directional localization of sound. Paedomorphosis, already identified as a potential factor in crown clade penguin skeletal morphology, may also be implicated in the failure of an interaural pathway to form during ontogeny in extant penguins.

The role of pressure difference reception in the directional hearing of budgerigars (Melopsittacus undulatus)

In many birds, the middle ears are connected through an air-filled interaural pathway. Sound transmission through this pathway may improve directional hearing. However, attempts to demonstrate such a mechanism have produced conflicting results. One reason is that some species of birds develop a lower static air pressure in the middle ears when anaesthetized, which reduces eardrum vibrations. In anaesthetized budgerigars with vented interaural air spaces and presumed normal eardrum vibrations, we find that sound propagating through the interaural pathway considerably improves cues to the directional hearing. The directional cues in the received sound combined with amplitude gain and time delay of sound propagating through the interaural pathway quantitatively account for the observed dependence of eardrum vibration on direction of sound incidence. Interaural sound propagation is responsible for most of the frontal gradient of eardrum vibration (i.e. when a sound source is moved from a small contralateral angle to the same ipsilateral angle). Our study confirms that at low frequencies the interaural sound propagation may cause vibrations of the eardrum to differ much in time, thus providing a possible cue for directional hearing. The acoustically effective size of the head of our birds (diameter 28 mm) is much larger than expected from the dimensions of the skull, so apparently the feathers on the head have a considerable acoustical effect.

Physiological measurements and mathematical models for interaural pathways

The middle-ear cavities of birds, reptiles, and anurans are often connected through a tube, which can act as an interaural pathway between both eardrums. Such an arrangement of acoustically effective structures is described as a pressure-difference receiver. It is generally assumed that pressure-difference receivers enhance the skills for directional hearing in animals. Sound pressures and phases were measured with probe-microfones in the interaural pathway from Zebra Finches during azimuthal rotation. The results show pressure differences between right and left middle ear, which are dependent on the azimuth and the frequency of the applied sound. A mathematical model was constructed, which gives the resulting pressure and phase of two overlaying waves that travel different distances. Assuming one wave traveling through the pathway and a second around a sphere, the resulting wave from dependency on azimuth and frequency was calculated. The pattern shows the same characteristic pressure differences as the physiological measurements. The same procedures were performed with a sphere as a hardware model for a head with an interaural pathway. The results show again the expected characteristics. The combination of physiological measurements, mathematical modeling, and testing this model with hardware models gives a meaningful explanation for the acoustical properties of middle ears as a basis for psychological acoustics.

Directional sound processing and interaural sound transmission in a small and a large grasshopper

Physical mechanisms involved in directional hearing are investigated in two species of short-horned grasshoppers that differ in body length by a factor of 3­4. The directional cues (the effects of the direction of sound incidence on the amplitude and phase angle of the sounds at the ears) are more pronounced in the larger animal, but the scaling is not simple. At high frequencies (10­20 kHz), the sound pressures at the ears of the larger species (Schistocerca gregaria) differ sufficiently to provide a useful directionality. In contrast, at low frequencies (3­5 kHz), the ears must be acoustically coupled and work as pressure difference receivers. At 3­5 kHz, the interaural sound transmission is approximately 0.5 (that is, when a tympanum is driven by a sound pressure of unit amplitude at its outer surface, the tympanum of the opposite ear receives a sound pressure with an amplitude of 0.5 through the interaural pathway). The interaural transmission decreases with frequency, and above 10 kHz it is only 0.1­0.2. It still has a significant effect on the directionality, however, because the directional cues are large. In the smaller species (Chorthippus biguttulus), the interaural sound transmission is also around 0.5 at 5 kHz, but the directionality is poor. The reason for this is not the modest directional cues, but rather the fact that the transmitted sound is not sufficiently delayed for the ear to exploit the directional cues. Above 7 kHz, the transmission increases to approximately 0.8 and the transmission delay increases; this allows the ear to become more directional, despite the still modest directional cues.

Azimuthal sound localization in the European starling (Sturnus vulgaris): I. Physical binaural cues.

The physical measurements reported here test whether the European starling (Sturnus vulgaris) evaluates the azimuth direction of a sound source with a peripheral auditory system composed of two acoustically coupled pressure-difference receivers (1) or of two decoupled pressure receivers (2). A directional pattern of sound intensity in the free-field was measured at the entrance of the auditory meatus using a probe microphone, and at the tympanum using laser vibrometry. The maximum differences in the sound-pressure level measured with the microphone between various speaker positions and the frontal speaker position were 2.4 dB at 1 and 2 kHz, 7.3 dB at 4 kHz, 9.2 dB at 6 kHz, and 10.9 dB at 8 kHz. The directional amplitude pattern measured by laser vibrometry did not differ from that measured with the microphone. Neither did the directional pattern of travel times to the ear. Measurements of the amplitude and phase transfer function of the starling's interaural pathway using a closed sound system were in accord with the results of the free-field measurements. In conclusion, although some sound transmission via the interaural canal occurred, the present experiments support the hypothesis 2 above that the starling's peripheral auditory system is best described as consisting of two functionally decoupled pressure receivers.

Sound localization in the budgerigar and the interaural pathways

Sound localization presents a problem for animals with small heads (closely spaced ears) and poor high-frequency hearing. In recent tests of spatial resolving power, several small songbirds (i.e., great tit, canary, and zebra finch) show rather large minimum audible angles (MAA) on the order of 15–20 deg. These results are expected if conventional binaural time and intensity differences are used. Budgerigars (17-mm interaural distance), on the other hand, demonstrate an MAA of about 5 deg, which approaches the excellent ability of the barn owl with a much larger head (50-mm interaural distance). Recent work has suggested that interaural pathways connecting the two ears of birds could be involved in sound localization. Using latex injection medium, we have demonstrated interaural pathways in the budgerigar, canary, and zebra finch. Taken together, the results of these behavioral and anatomical studies indicate that the budgerigar may use the interaural pathway in sound localization.

The owl's interaural pathway is not involved in sound localization

Sound transmission through the barn owl's (Tyto alba) interaural pathway was measured by comparing the thresholds of single auditory neurons of the cochlear nucleus in response to independent stimulation of the ipsilateral and the contralateral ears. The interaural pathway acted as an acoustical low-pass filter. It attenuated sound by an average of 13 dB at 3.5 kHz, and by an average of 63 dB at 7.0 kHz under the experimental conditions used, as determined from single-unit thresholds. Sound pressure measurements in the middle ears confirmed the low-pass filter characteristics of the interaural pathway. Sound attenuation in the interaural pathway is too large to enable/the two ears to function as coupled pressure-difference receivers at the sound pressure levels and for the frequency range (6–8 kHz) important for sound localization by the owl.

Sound transmission through the avian interaural pathways

1. The magnitude and phase of sound transmitted through the avian interaural pathways were measured acoustically and with cochlear microphonic recordings. 2. The acoustic measures indicated that a sound stimulus on one side of the head could be conducted through the tympanic membrane and across the interaural pathway to the opposite middle ear with an attenuation of about 25–35 dB. 3. The acoustic loss was primarily due to sound transmission across the tympanic membrane, with no further attenuation attributed to sound conduction through the interaural pathways. 4. A comparison of cochlear microphonic recordings during ipsilateral or contralateral stimulation indicated a loss of 15–20 dB due to sound conduction across the contralateral tympanic membrane and interaural pathways. 5. Sound conducted through the interaural pathway exhibited a frequency dependent phase delay. 6. The consequences of binaural stimulation on the cochlear microphonic response could be predicted by a vector addition of the response to monaural ipsilateral or contralateral stimulation. 7. The maintenance of a constant SPL at the contralateral ear varied the cochlear response to ipsilateral stimuli, in a frequency dependent manner, by as much as ±2 dB. 8. It is hypothesized that the chick interaural pathways act like the air filled trachae of insects, which connect the bilateral ears and are thought to be important in auditory localization.

The interaural pathway and auditory localization: Cochlear microphonic measures in free field sound

Cochlear microphonic 1.0 μV thresholds and phase were measured in pigeons exposed to free-field sound stimulation of varying horizontal azimuths. The pigeons were anesthetized and mounted on a rotating platform at a distance of one meter from a loudspeaker. The relative azimuth of the speaker to the binaural axis of the pigeon could be controlled remotely. The amplitude and phase responses of the CM to tone sources of varying direction were determined. One ear canal was then filled with plasticine and the measures were repeated. Comparison of the control and ear blocked measures showed differences in angular sensitivity of the CM which were related to sound conduction through the interaural pathway. The effects of interaural sound conduction on the azimuthal sensitivity of the CM were small but in the proper direction to increase the amplitude difference between the two ears. These results suggest that the combination of interaural sound conduction and the diffraction of sound about the head enable the pigeon to localize sounds in their best frequency range. [Work supported in part by NSF.]

Phase interactions resulting from the avain interaural pathway

Acoustic measures of sound transmission across the effective interaural pathway (the interaural pathway and a tympanic membrane) have described a 20–30 dB attenuation of frequencies within the audible range of the chicken [J. J. Rosowski, J. Acoust. Soc. Am. 61, S3(A) (1977)]. The present report is concerned with the phase delay imposed by the effective interaural pathway. Cochlear microphonic responses were recorded in young chickens under conditions of homolateral or contralateral sound stimulation. The stimuli consisted of continuous pure tones with frequencies between 125 and 6300 Hz. The phase response of the CM relative to the phase of the stimulus at the directly stimulated tympanic membrane was determined. Comparison of the CM phase response between conditions of homolateral or contralateral stimulation yielded a measure of the effective phase delay resulting from the interaural pathway. The interaural change in phase (Δφ) for frequencies between 125 and 500 Hz was 180°. This finding suggests that the interaural pathway allows a stimulation of the opposite tympanic membrane in the reverse direction of normal stimulation. At higher frequencies the interaural Δφ increased such that a Δφ of 800° was measured at 6300 Hz. These phase delays are much greater than would be expected from the interaural distances involved. Binaural stimulation resulted in complex interactions of the two stimuli which brought about changes in recorded CM amplitude and phase. A possible relationship between these interactions and localization phenomena will be discussed. [Work supported by NSF.]

Acoustic properties of the interaural pathway in the chicken

The acoustic transmission properties of the avian interaural pathway were measured in the chicken with a sound probe placed within the middle ear. Ten chickens, 3–9 days old, were anesthetized, both external meati were surgically excised, the animal was placed in a head holder, and sound tubes with associated probe microphones were sealed over the right and left tympanic rings. The left middle ear was opened, and a 1-mm-diam sound probe was placed in the middle ear. The ear was then resealed. Continuous pure tone stimuli of approximately 110 dB SPL and of various frequencies was presented first to one ear and then to the other. With each stimulus presentation SPL was measured at three places: the stimulated external ear, the opposite external ear, and in the middle ear. A reduction in SPL of 25–30 dB was noted in the left middle ear regardless of whether the left or right external ear was stimulated. These observations suggest that the interaural pathway imposes no attenuation on transmitted sound at frequencies within the audible range of the chicken. The importance of the interaural pathway in avian hearing has yet to be determined. [Work supported by NSF.]