Tom Reuter

What middle ear parameters tell about impedance matching and high frequency hearing

Acoustic energy enters the mammalian cochlea aided by an anatomical impedance matching performed by the middle ear. The purpose of this paper is to analyse the functional consequences of changes in scale of the middle ear when going from the smallest mammals to the largest. Our anatomical measurements in mammals of different sizes ranging from bats to elephants indicate that middle ear proportions are largely isometric. Thus the calculated transformer ratio is basically independent of animal size, a typical value lying between 30 and 80. Similarly, the calculated specific acoustic input impedance of the inner ear is independent of animal size, the average value being about 140 kPa s/m. We show that if the high frequency hearing limit of isometric ears is limited by ossicle inertia, it should be inversely proportional to the cubic root of the ossicular mass. This prediction is in reasonable agreement with published audiogram data. We then present a three-parameter model of the middle ear where some obvious deviations from perfect isometry are taken into account. The high frequency hearing limits of different species generally agree well with the predictions of this simple model. However, the hearing limits of small rodents clearly deviate from the model calculation. We interpret this observation as indicating that the hearing limit towards very high frequencies may be set by cochlear transduction mechanisms. Further we discuss the exceptional high frequency hearing of the cat and the amphibious hearing of seals.

Dark-adaptation processes in the rhodopsin rods of the frog's retina.

Abstract In the excised and opened frogs eye two phases of rod dark-adaptation can be distinguished. The slower phase, previously studied by us, depends on the rate of regeneration of rhodopsin. Supplementary evidence is here given based on measurements involving temperature changes of the eye during adaptation. The rate of regeneration, which has a Q10 of about 4.6, is thereby rapidly altered. This brings about quantitatively corresponding changes in the sensitivity of the single units studied. The initial, rapid phase of rod adaptation is found to depend on the decomposition of metarhodopsin in the rods, which shows the same time-course at different temperatures as the adaptation process. Here log threshold is found to be proportional to the amount of metarhodopsin. The evidence obtained in experiments at different temperatures further suggests that it is metarhodopsin II, which exists in a tautomeric equilibrium with metarhodopsin I, that causes this desensitization of the rods.

Visual performance of the toad (Bufo bufo) at low light levels: retinal ganglion cell responses and prey-catching accuracy.

The accuracy of toad snapping towards moving worm dummies under various levels of dim illumination (from absolute threshold to “moonlight”) was videorecorded and related to spike responses of retinal ganglion cells exposed to equivalent stimuli. Some toads (at ca. 16 °C) successfully snapped at dummies that produced only one photoisomerization per 50 rods per second in the retina, in good agreement with thresholds of sensitive retinal ganglion cells. One factor underlying such high sensitivity is extensive temporal summation by the ganglion cells. This, however, is inevitably accompanied by very long response latencies (around 3 s near threshold), whereby the information reaching the brain shows the dummy in a position where it was several seconds earlier. Indeed, as the light was dimmed, snaps were displaced successively further to the rear of the dummy, finally missing it. The results in weak but clearly supra-threshold illumination indicate that snaps were aimed at the advancing head as seen by the brain, but landed further backwards in proportion to the retinal latency. Near absolute threshold, however, accuracy was “too good”, suggesting that the animal had recourse to a neural representation of the regularly moving dummies to correct for the slowness of vision.

The synthesis of photosensitive pigments in the rods of the frog's retina

Abstract The amounts of photosensitive pigments in the frogs retina were measured at different stages of light- and dark-adaptation at 13–14°C. The following photosensitive pigments were observed: rhodopsin, isorhodopsin and the visual pigment of the green rods (VP 440). Both in intact frogs and in excised and opened eyes the regeneration of rhodopsin was found to be linear, apart from a small initial delay, until the point where 70 per cent is regenerated after 68 min of dark-adaptation. After that the regeneration curve follows, at least approximately a first-order reaction of 22 min half-return time. The regeneration of VP 440 is complete after 35 min in the dark. An isomerization of some coloured intermediate bleaching product (probably metarhodopsin I) into rhodopsin and isorhodopsin is demonstrated to occur during illumination. Using a simple densitometric method the density changes of the retina (probably caused by the fading of metarhodopsin I and II) were followed after a short exposure to strong light.

Scaling of the cetacean middle ear

Functionally interesting dimensions of the tympano-periotic complex were measured and compared in 18 odontocete and six mysticete species, ranging from small porpoises to the blue whale. We determined (i) the masses of the tympanic and periotic bones (T and P) and of the ossicles malleus, incus, and stapes (M, I and S), (ii) the volume occupied bythe tympanic bone (V), (iii) the areas of the tympanic plate and oval window (A1 and A2), (iv) the thickness of the tympanic plate (D), and (v) the densities of the ossicles (dM, dI, and dS). In most cases, roughly isometric scaling was found in both toothed and baleen whales. P is isometric to T, and the tympanic bone is structurally isometric in all species studied, although not within mysticetes as a group, shown by the isometric relations of V to T, of T(2/3) to A1, and of D to square root(A1). The essentially isometric scaling of the tympanic bone provides a basis for the functional models described by Hemilä et al. (1999). The relation of S to M+I is also isometric, but the relation of M+I+S to T is negatively allometric, as is the relation of A2 to A1, both with slopes close to 2/3. The possible functional implication of this allometry is unknown. The mean ossicular density is 2.64 g/cm3 for odontocetes, and 2.35 g/cm3 for mysticetes. The highly mineralized and convex tympanic plate provides cetaceans with a uniquely large and stiff sound collecting area.

Color discrimination mechanisms in the retina of the toad (Bufo bufo)

SummaryIn many class 2 ganglion cells in the toad (Bufo bufo) retina the blue-sensitive green rods contribute only to the “on” responses, while the yellow-sensitive cones contribute to both “on” and “off”. Thus the spectral sensitivities of the on and off responses deviate in the blue and violet parts of the spectrum (Fig. 1). This correlates with Dietzs (1972) finding that toads detect a moving blue prey-dummy irrespective of the intensity of the grey background.

The dark-adaptation of single units in the frog's retina and its relation to the regeneration of rhodopsin.

Abstract The dark-adaptation of single units in excised and opened frogs eyes has been recorded with such test parameters that a nervous reorganization or changes in summation within the receptive fields can be excluded as explanations of the sensitivity increase observed. Further, using light of wave-length 500 nm cone contributions can be excluded after more than 40 min of dark-adaptation. It has thus been possible to measure the sensitivity changes caused by the rhodopsin rods. Because the regeneration of rhodopsin has also been measured, the significance of the regeneration process for the sensitivity changes can be analysed. It is found, that the log threshold is linearly related to the log rate of regeneration at each instant, when the threshold is expressed in terms of the relative number of quanta absorbed. Moreover, this relationship is the same as that observed between the increment threshold and the intensity of the corresponding adapting field.

A model of the odontocete middle ear

The high acoustic sensitivity of the bottlenose dolphin is physically defined and related to the anatomy of the middle ear. The paper presents a conceptual and parametric analysis of the demands imposed by this high sensitivity upon the middle ear mechanisms: the head and the middle ear structures must collect sound energy from a large area and concentrate it onto the oval window. Assuming that the specific input impedance of the mammalian cochlea is relatively constant, and smaller than the characteristic acoustic impedance of water, we find that the impedance matching task of the cetacean middle ear is very different from that of terrestrial mammals: instead of a large pressure amplification, cetaceans need amplification of particle velocity. Our mechanical four-bone model of the odontocete middle ear is based on the anatomy of the tympano-periotic complex and consists of four rigid bone units (tympanic bone, the malleus-incus complex, stapes, periotic bone) connected through elastic junctions. The velocity amplification is brought about by lever mechanisms and elastic couplings. The model produced velocity amplifications ranging from 7- to 23-fold when provided with middle ear parameters from the six odontocete species for which audiograms are available. The model reproduces the complete audiograms of these six species fairly well for frequencies up to about 100-120 kHz.

Chromatic properties of the retinal afferents in the thalamus and the tectum of the frog (Rana temporaria)

In order to clarify physiological mechanisms underlying colour-specific visually guided behaviour, we measured spectral sensitivities of On-fibres projecting to the thalamus and class 2 and 3 fibres passing to tectum opticum. In addition we recorded responses of these fibres to moving coloured papers with known spectral reflectancies. The latter method, here called paper colourimetry, allowed us to change the relative stimulations of the blue-, green- and red-sensitive photoreceptors in any direction desired. Under the photopic conditions used the tectal fibres were driven exclusively by red-sensitive receptors, while the thalamic fibres received strong On-inputs from both red- and blue-sensitive receptors. Due to a partly antagonistic interaction between these inputs the On-fibres acted in a dichromatic way, responding with specific extended low-frequency discharges to all relative increases in blue receptor stimulation, e.g. to a great reduction in red stimulation combined with unchanged blue stimulation. Thus they have functional characteristics which could serve a visual system showing colour constancy.

Scaling of mammalian ethmoid bones can predict olfactory organ size and performance

The relation between size and performance is central for understanding the evolution of sensory systems, and much interest has been focused on mammalian eyes and ears. However, we know very little about olfactory organ size (OOS), as data for a representative set of mammals are lacking. Here, we present a cranial endocast method for estimating OOS by measuring an easily accessible part of the system, the perforated part of the ethmoid bone, through which the primary olfactory axons reach the olfactory bulb. In 16 species, for which relevant data are available, the area of the perforated ethmoid bone is directly proportional to the area of the olfactory epithelium. Thus, the ethmoid bone is a useful indicator enabling us to analyse 150 species, and describe the distribution of OOS within the class Mammalia. In the future, a method using skull material may be applied to fossil skulls. In relation to skull size, humans, apes and monkeys have small olfactory organs, while prosimians have OOSs typical for mammals of their size. Large ungulates have impressive olfactory organs. Relating anatomy to published thresholds, we find that sensitivity increases with increasing absolute organ size.