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1.  Organization of the Auditory Brainstem in a Lizard, Gekko gecko. I. Auditory Nerve, Cochlear Nuclei, and Superior Olivary Nuclei 
The Journal of comparative neurology  2012;520(8):1784-1799.
We used tract tracing to reveal the connections of the auditory brainstem in the Tokay gecko (Gekko gecko). The auditory nerve has two divisions, a rostroventrally directed projection of mid- to high best-frequency fibers to the nucleus angularis (NA) and a more dorsal and caudal projection of low to middle best-frequency fibers that bifurcate to project to both the NA and the nucleus magnocellularis (NM). The projection to NM formed large somatic terminals and bouton terminals. NM projected bilaterally to the second-order nucleus laminaris (NL), such that the ipsilateral projection innervated the dorsal NL neuropil, whereas the contralateral projection crossed the midline and innervated the ventral dendrites of NL neurons. Neurons in NL were generally bitufted, with dorsoventrally oriented dendrites. NL projected to the contralateral torus semicircularis and to the contralateral ventral superior olive (SOv). NA projected to ipsilateral dorsal superior olive (SOd), sent a major projection to the contralateral SOv, and projected to torus semicircularis. The SOd projected to the contralateral SOv, which projected back to the ipsilateral NM, NL, and NA. These results suggest homologous patterns of auditory connections in lizards and archosaurs but also different processing of low- and high-frequency information in the brainstem.
doi:10.1002/cne.23013
PMCID: PMC4300985  PMID: 22120438
auditory nerve; ITD; cochlear nuclei; superior olive; reptile; lizard; tract tracing; Tokay gecko
2.  Spatial hearing in Cope’s gray treefrog: II. Frequency-dependent directionality in the amplitude and phase of tympanum vibrations 
Anuran ears function as pressure difference receivers, and the amplitude and phase of tympanum vibrations are inherently directional, varying with sound incident angle. We quantified the nature of this directionality for Cope’s gray treefrog, Hyla chrysoscelis. We presented subjects with pure tones, advertisement calls, and frequency-modulated sweeps to examine the influence of frequency, signal level, lung inflation, and sex on ear directionality. Interaural differences in the amplitude of tympanum vibrations were 1–4 dB greater than sound pressure differences adjacent to the two tympana, while interaural differences in the phase of tympanum vibration were similar to or smaller than those in sound phase. Directionality in the amplitude and phase of tympanum vibration were highly dependent on sound frequency, and directionality in amplitude varied slightly with signal level. Directionality in the amplitude and phase of tone- and call-evoked responses did not differ between sexes. Lung inflation strongly affected tympanum directionality over a narrow frequency range that, in females, included call frequencies. This study provides a foundation for further work on the biomechanics and neural mechanisms of spatial hearing in H. chrysoscelis, and lends valuable perspective to behavioral studies on the use of spatial information by this species and other frogs.
doi:10.1007/s00359-014-0883-5
PMCID: PMC4016234  PMID: 24504183
Hyla chrysoscelis; Eardrum vibrations; Auditory periphery; Hearing; Lung inflation
3.  Middle Ear Cavity Morphology Is Consistent with an Aquatic Origin for Testudines 
PLoS ONE  2013;8(1):e54086.
The position of testudines in vertebrate phylogeny is being re-evaluated. At present, testudine morphological and molecular data conflict when reconstructing phylogenetic relationships. Complicating matters, the ecological niche of stem testudines is ambiguous. To understand how turtles have evolved to hear in different environments, we examined middle ear morphology and scaling in most extant families, as well as some extinct species, using 3-dimensional reconstructions from micro magnetic resonance (MR) and submillimeter computed tomography (CT) scans. All families of testudines exhibited a similar shape of the bony structure of the middle ear cavity, with the tympanic disk located on the rostrolateral edge of the cavity. Sea Turtles have additional soft tissue that fills the middle ear cavity to varying degrees. When the middle ear cavity is modeled as an air-filled sphere of the same volume resonating in an underwater sound field, the calculated resonances for the volumes of the middle ear cavities largely fell within testudine hearing ranges. Although there were some differences in morphology, there were no statistically significant differences in the scaling of the volume of the bony middle ear cavity with head size among groups when categorized by phylogeny and ecology. Because the cavity is predicted to resonate underwater within the testudine hearing range, the data support the hypothesis of an aquatic origin for testudines, and function of the middle ear cavity in underwater sound detection.
doi:10.1371/journal.pone.0054086
PMCID: PMC3544720  PMID: 23342082
4.  Tone and call responses of units in the auditory nerve and dorsal medullary nucleus of Xenopus laevis 
The clawed frog Xenopus laevis produces vocalizations consisting of distinct patterns of clicks. This study provides the first description of spontaneous, pure-tone and communication-signal evoked discharge properties of auditory nerve (n.VIII) fibers and dorsal medullary nucleus (DMN) cells in an obligatorily aquatic anuran. Responses of 297 n.VIII and 253 DMN units are analyzed for spontaneous rates (SR), frequency tuning, rate-intensity functions, and firing rate adaptation, with a view to how these basic characteristics shape responses to recorded call stimuli. Response properties generally resemble those in partially terrestrial anurans. Broad tuning exists across characteristic frequencies (CFs). Threshold minima are −101 dB re 1 mm/s at 675 Hz; −87 dB at 1,600 Hz; and −61 dB at 3,000 Hz (−90, −77, and −44 dB re 1 Pa, respectively), paralleling the peak frequency of vocalizations at 1.2–1.6 kHz with ~500 Hz in 3 dB bandwidth. SRs range from 0 to 80 (n.VIII) and 0 to 73 spikes/s (DMN). Nerve and DMN units of all CFs follow click rates in natural calls, ≤67 clicks/s and faster. Units encode clicks with a single spike, double spikes, or bursts. Spike times correlate closely with click envelopes. No temporal filtering for communicative click rates occurs in either n.VIII or the DMN.
doi:10.1007/s00359-007-0285-z
PMCID: PMC3493246  PMID: 17989982
Auditory nerve; Hearing; Amphibian; Dorsal medullary nucleus; Sound communication
5.  Specialization for underwater hearing by the tympanic middle ear of the turtle, Trachemys scripta elegans 
Turtles, like other amphibious animals, face a trade-off between terrestrial and aquatic hearing. We used laser vibrometry and auditory brainstem responses to measure their sensitivity to vibration stimuli and to airborne versus underwater sound. Turtles are most sensitive to sound underwater, and their sensitivity depends on the large middle ear, which has a compliant tympanic disc attached to the columella. Behind the disc, the middle ear is a large air-filled cavity with a volume of approximately 0.5 ml and a resonance frequency of approximately 500 Hz underwater. Laser vibrometry measurements underwater showed peak vibrations at 500–600 Hz with a maximum of 300 µm s−1 Pa−1, approximately 100 times more than the surrounding water. In air, the auditory brainstem response audiogram showed a best sensitivity to sound of 300–500 Hz. Audiograms before and after removing the skin covering reveal that the cartilaginous tympanic disc shows unchanged sensitivity, indicating that the tympanic disc, and not the overlying skin, is the key sound receiver. If air and water thresholds are compared in terms of sound intensity, thresholds in water are approximately 20–30 dB lower than in air. Therefore, this tympanic ear is specialized for underwater hearing, most probably because sound-induced pulsations of the air in the middle ear cavity drive the tympanic disc.
doi:10.1098/rspb.2012.0290
PMCID: PMC3367789  PMID: 22438494
underwater sound; evolution; cochlea; auditory brainstem response
6.  Hearing in the African lungfish (Protopterus annectens): pre-adaptation to pressure hearing in tetrapods? 
Biology Letters  2010;7(1):139-141.
Lungfishes are the closest living relatives of the tetrapods, and the ear of recent lungfishes resembles the tetrapod ear more than the ear of ray-finned fishes and is therefore of interest for understanding the evolution of hearing in the early tetrapods. The water-to-land transition resulted in major changes in the tetrapod ear associated with the detection of air-borne sound pressure, as evidenced by the late and independent origins of tympanic ears in all of the major tetrapod groups. To investigate lungfish pressure and vibration detection, we measured the sensitivity and frequency responses of five West African lungfish (Protopterus annectens) using brainstem potentials evoked by calibrated sound and vibration stimuli in air and water. We find that the lungfish ear has good low-frequency vibration sensitivity, like recent amphibians, but poor sensitivity to air-borne sound. The skull shows measurable vibrations above 100 Hz when stimulated by air-borne sound, but the ear is apparently insensitive at these frequencies, suggesting that the lungfish ear is neither adapted nor pre-adapted for aerial hearing. Thus, if the lungfish ear is a model of the ear of early tetrapods, their auditory sensitivity was limited to very low frequencies on land, mostly mediated by substrate-borne vibrations.
doi:10.1098/rsbl.2010.0636
PMCID: PMC3030901  PMID: 20826468
lungfish; hearing; vibration; tetrapod; sound; evolution
7.  Evolution of a sensory novelty: Tympanic ears and the associated neural processing 
Brain Research Bulletin  2007;75(2-4):365-370.
Tympanic hearing is a true evolutionary novelty that appears to have developed independently in at least five major tetrapod groups—the anurans, turtles, lepidosaurs, archosaurs and mammals. The emergence of a tympanic ear would have increased the frequency range and sensitivity of hearing. Furthermore, tympana were acoustically coupled through the mouth cavity and therefore inherently directional in a certain frequency range, acting as pressure difference receivers. In some lizard species, this acoustical coupling generates a 50-fold directional difference, usually at relatively high frequencies (2–4 kHz).
In ancestral atympanate tetrapods, we hypothesize that low-frequency sound may have been processed by non-tympanic mechanisms like those in extant amphibians. The subsequent emergence of tympanic hearing would have led to changes in the central auditory processing of both high-frequency sound and directional hearing. These changes should reflect the independent origin of the tympanic ears in the major tetrapod groups. The processing of low-frequency sound, however, may have been more conserved, since the acoustical coupling of the ancestral tympanate ear probably produced little sensitivity and directionality at low frequencies. Therefore, tetrapod auditory processing may originally have been organized into low- and high-frequency streams, where only the high-frequency processing was mediated by tympanic input.
The closure of the middle ear cavity in mammals and some birds is a derived condition, and may have profoundly changed the operation of the ear by decoupling the tympana, improving the low-frequency response of the tympanum, and leading to a requirement for additional neural computation of directionality in the central nervous system. We propose that these specializations transformed the low- and high-frequency streams into time and intensity pathways, respectively.
doi:10.1016/j.brainresbull.2007.10.044
PMCID: PMC3269633  PMID: 18331899
Middle ear; Tympanum; Lizard; Frog; Hearing; Auditory; Brain stem
8.  Acoustical Coupling of Lizard Eardrums 
Lizard ears are clear examples of two-input pressure-difference receivers, with up to 40-dB differences in eardrum vibration amplitude in response to ipsi- and contralateral stimulus directions. The directionality is created by acoustical coupling of the eardrums and interaction of the direct and indirect sound components on the eardrum. The ensuing pressure-difference characteristics generate the highest directionality of any similar-sized terrestrial vertebrate ear. The aim of the present study was to measure the gain of the direct and indirect sound components in three lizard species: Anolis sagrei and Basiliscus vittatus (iguanids) and Hemidactylus frenatus (gekkonid) by laser vibrometry, using either free-field sound or a headphone and coupler for stimulation. The directivity of the ear of these lizards is pronounced in the frequency range from 2 to 5 kHz. The directivity is ovoidal, asymmetrical across the midline, but largely symmetrical across the interaural axis (i.e., front–back). Occlusion of the contralateral ear abolishes the directionality. We stimulated the two eardrums with a coupler close to the eardrum to measure the gain of the sound pathways. Within the frequency range of maximal directionality, the interaural transmission gain (compared to sound arriving directly) is close to or even exceeds unity, indicating a pronounced acoustical transparency of the lizard head and resonances in the interaural cavities. Our results show that the directionality of the lizard ear is caused by the acoustic interaction of the two eardrums. The results can be largely explained by a simple acoustical model based on an electrical analog circuit.
doi:10.1007/s10162-008-0130-2
PMCID: PMC2580811  PMID: 18648878
lizard; tympanum; vibrometry; directional; hearing; reptile

Results 1-8 (8)