Simo Hemilä

Kinetics of long-lived rhodopsin photoproducts in the frog retina as a function of the amount bleached

Abstract Results are reported on measurements on the isolated, perfused frog retina of the decay of the long-lived photoproducts of rhodopsin as a function of the amount bleached. We find that the rates of decay of metarhodopsin II and III are increased when the amount bleached is reduced below about 15 per cent of the total. This leads to a decay process where very little (or finally no) metarhodopsin III is formed (bleaches smaller than 2 per cent). After small bleaches a restricted capacity for regeneration of rhodopsin is found In total, the isolated retina appears able to regenerate about 10 per cent of the total rhodopsin.

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.

Modelling the effect of microsaccades on retinal responses to stationary contrast patterns

We have modelled the effect of microsaccades on retinal responses to achromatic borders and lines using physiologically realistic parameters. Typical microsaccade movement sequences were applied to the retinal image of stationary spatial contrast patterns as projected on the foveal cone mosaic after being passed through the optical transfer function of the eye. The resulting temporal contrast modulation over a cone receptive field was convolved with an analytical expression for the response waveform of primate cones (photocurrent: [Schnapf, J. L., Nunn, B. J., Meister, M. & Baylor, D. A. (1990). Visual transduction in cones of the monkey Macaca fascicularis. Journal of Physiology, 427, 681-713]; photovoltage: [Schneeweis, D. M. & Schnapf, J. L. (1999). The photovoltage of macaque cone photoreceptors: Adaptation, noise, and kinetics. Journal of Neuroscience, 19, 1203-1216]). The input to the ganglion cell was derived from the cone responses by the difference-of-Gaussians receptive field model of Donner and Hemilä [Donner, K. & Hemilä, S. (1996). Modelling the spatio-temporal modulation response of ganglion cells with difference-of-Gaussians receptive fields: Relation to photoreceptor response kinetics. Visual Neuroscience, 13, 173-186]. The modelled response waveforms suggest that microsaccades may significantly enhance sensitivity to edges, re-sharpen the image and, most interestingly, improve resolution of two closely spaced lines. The reason is that fine spatial structure of the retinal image when moving at suitable velocities is translated into a correlated temporal structure of responses of single cones and ganglion cells. The information content of the signal is not strongly dependent on positional accuracy and the effect is thus distinct from the presumed retinal basis of vernier acuity. Other eye movements (drift) with velocity distributions similar to that of the microsaccades slow return phase might be similarly useful, although the microsaccade has some distinguishing features that could be functionally significant, e.g., the neural motor control and the biphasic movement pattern.

Rod phototransduction modulated by bicarbonate in the frog retina : roles of carbonic anhydrase and bicarbonate exchange

1. Effects on rod phototransduction following manipulation of retinal CO2‐HCO3‐ and H+ fluxes were studied in dark‐adapted retinas of the frog and the tiger salamander. 2. Rod photoresponses to brief flashes of light were recorded from the isolated sensory retina as electroretinogram mass receptor potentials and from isolated rods by the suction‐pipette technique. The experimental treatments were: (1) varying [CO2] + [HCO3‐] in the perfusion fluid: (2) applying acetazolamide (AAA), which inhibits the enzyme carbonic anhydrase (CA); and (3) applying 4,4‐diisothiocyanatostilbene‐2,2‐disulphonic acid (DIDS) which blocks exchange mechanisms transporting HCO3‐ across cell membranes. 3. The concentration of the internal transmitter of the rods, cyclic GMP, was biochemically determined from the rod outer segment layer of retinas that had been incubated in the same solutions as were used for perfusion in the electrophysiological experiments. 4. The introduction of 6 mM‐sodium bicarbonate to replace half the buffer of a nominally CO2‐HCO3(‐)‐free (12 mM‐phosphate or HEPES, [Na+] constant) Ringer solution doubled the cyclic GMP concentration in the rod outer segment layer and increased the saturating response amplitude and the relative sensitivity of rods in the intact retina. 5. The introduction of 0.5 mM‐AAA into bicarbonate‐containing Ringer solution accelerated the growth of saturated responses and sensitivity. Incubation of the retina in AAA‐bicarbonate Ringer solution elevated the concentration of cyclic GMP ninefold compared with the phosphate control. 6. No effects of switching to bicarbonate‐AAA Ringer solution were observed in the photocurrent of isolated rods drawn into suction pipettes with only the outer segment protruding into the perfusion fluid. The target of AAA is probably the CA‐containing Müller cell. 7. The introduction of DIDS into the perfusate (at normal pH 7.5) set off a continuous decay of photoresponses which finally abolished light sensitivity completely. The decay proceeded regardless of whether bicarbonate and AAA were present or not. 8. Rods that had lost their photosensitivity in DIDS recovered almost fully when the pH of the DIDS perfusate was raised to 8.5. They also recovered when DIDS was washed out with bicarbonate Ringer solution at constant pH (7.5). 9. It is proposed that all our treatments ultimately modulate the intracellular pH of the rods which is determined by the relative rates of H+ leakage and HCO3‐ transport into the cells.(ABSTRACT TRUNCATED AT 400 WORDS)

Modelling the spatio-temporal modulation response of ganglion cells with difference-of-Gaussians receptive fields : Relation to photoreceptor response kinetics

Difference-of-Gaussians (DOG) models for the receptive fields of retinal ganglion cells accurately predict linear responses to both periodic stimuli (typically moving sinusoidal gratings) and aperiodic stimuli (typically circular fields presented as square-wave pulses). While the relation of spatial organization to retinal anatomy has received considerable attention, temporal characteristics have been only loosely connected to retinal physiology. Here we integrate realistic photoreceptor response waveforms into the DOG model to clarify how far a single set of physiological parameters predict temporal aspects of linear responses to both periodic and aperiodic stimuli. Traditional filter-cascade models provide a useful first-order approximation of the single-photon response in photoreceptors. The absolute time scale of these, plus a time for retinal transmission, here construed as a fixed delay, are obtained from flash/step data. Using these values, we find that the DOG model predicts the main features of both the amplitude and phase response of linear cat ganglion cells to sinusoidal flicker. Where the simplest model formulation fails, it serves to reveal additional mechanisms. Unforeseen facts are the attenuation of low temporal frequencies even in pure center-type responses, and the phase advance of the response relative to the stimulus at low frequencies. Neither can be explained by any experimentally documented cone response waveform, but both would be explained by signal differentiation, e.g. in the retinal transmission pathway, as demonstrated at least in turtle retina.

Exploring the mammalian sensory space: co-operations and trade-offs among senses

The evolution of a particular sensory organ is often discussed with no consideration of the roles played by other senses. Here, we treat mammalian vision, olfaction and hearing as an interconnected whole, a three-dimensional sensory space, evolving in response to ecological challenges. Until now, there has been no quantitative method for estimating how much a particular animal invests in its different senses. We propose an anatomical measure based on sensory organ sizes. Dimensions of functional importance are defined and measured, and normalized in relation to animal mass. For 119 taxonomically and ecologically diverse species, we can define the position of the species in a three-dimensional sensory space. Thus, we can ask questions related to possible trade-off vs. co-operation among senses. More generally, our method allows morphologists to identify sensory organ combinations that are characteristic of particular ecological niches. After normalization for animal size, we note that arboreal mammals tend to have larger eyes and smaller noses than terrestrial mammals. On the other hand, we observe a strong correlation between eyes and ears, indicating that co-operation between vision and hearing is a general mammalian feature. For some groups of mammals we note a correlation, and possible co-operation between olfaction and whiskers.

High-frequency hearing in phocid and otariid pinnipeds: an interpretation based on inertial and cochlear constraints (L).

Audiograms in air and underwater, determined by previous workers for four pinniped species, two eared seals (Otariidae) and two phocids (Phocidae), are supplemented here by measurements on their middle ear ossicular mass, enabling mechanistic interpretations of high-frequency hearing and audiogram differences. Otariid hearing is not largely affected by the medium (air/water). This indicates that cochlear constraints limit high-frequency hearing in otariids. Phocids, however, have massive middle ear ossicles, and underwater hearing has radically shifted towards higher frequencies. This suggests that the high-frequency hearing of phocids in air is constrained by ossicle inertia.

Anatomy and physics of the exceptional sensitivity of dolphin hearing (Odontoceti: Cetacea)

During the past 50xa0years, the high acoustic sensitivity and the echolocation behavior of dolphins and other small odontocetes have been studied thoroughly. However, understanding has been scarce as to how the dolphin cochlea is stimulated by high frequency echoes, and likewise regarding the ear mechanics affecting dolphin audiograms. The characteristic impedance of mammalian soft tissues is similar to that of water, and thus no radical refractions of sound, nor reflections of sound, can be expected at the water/soft tissue interfaces. Consequently, a sound-collecting terrestrial pinna and an outer ear canal serve little purpose in underwater hearing. Additionally, compared to terrestrial mammals whose middle ear performs an impedance match from air to the cochlea, the impedance match performed by the odontocete middle ear needs to be reversed to perform an opposite match from water to the cochlea. In this paper, we discuss anatomical adaptations of dolphins: a lower jaw collecting sound, thus replacing the terrestrial outer ear pinna, and a thin and large tympanic bone plate replacing the tympanic membrane of terrestrial mammals. The paper describes the lower jaw anatomy and hypothetical middle ear mechanisms explaining both the high sensitivity and the converted acoustic impedance match.

Long-lived photoproducts of porphyropsin in the retina of the crucian carp (Carassius carassius)

Abstract In the carp retina bleached porphyropsin is rapidly converted into a 390–400 nm product, which decays exponentially to 3-dehydroretinol. Because the photochemistry and kinetics of this product suggest that it corresponds to the intermediate named retinal in the frogs retina, we call it “3-dehydroretinal”. The difference between the carp and the frog is that the decay of carp metaporphyropsin II to “3-dehydroretinal” is faster than the decay of frog M II, and that the indirect pathway through M III is absent in the carp. In solution the bleaching sequence includes a long-lived 480 nm product, which does not occur in the retina.

Noise-equivalent and signal-equivalent visual summation of quantal events in space and time

Noise recorded in visual neurons, or variability in psychophysical experiments, may be quantified in terms of quantal fluctuations from an equivalent steady illumination. The conversion requires assumptions concerning how photon signals are pooled in space and time, i.e. how to pass from light fluxes to numbers of photon events relevant to the Poisson statistics describing signal/noise. It is usual to approximate real weighting profiles for the integration of photon events in space and time (the sensitivity distribution of the receptive field [RF] and the waveform of the impulse response [IR]) by sharp-bordered apertures of complete, equal-weight summation of events. Apertures based on signal-equivalence cannot provide noise-equivalence, however, because greater numbers of events summed with smaller weights (as in reality) have lower variances than smaller numbers summed with full weight. Thus sharp-bordered apertures are necessarily smaller if defined for noise- than for signal-equivalence. We here consider the difference for some commonly encountered RF and IR profiles. Summation areas, expressed as numbers of photoreceptors (cones or rods) contributing with equal weight, are denoted NS for signal and NN for noise; sharply delimited summation times are correspondingly denoted tS and tN. We show that the relation in space is NN = 0.5 NS for the Gaussian distribution (e.g. for the RF center mechanism of retinal ganglion cells). For a photoreceptor in an electrically coupled network the difference is even larger, e.g., for rods in the toad retina NN = 0.2 NS (NS = 13.7 rods and NN = 2.8 rods). In time, the relation is tN approximately 0.7 tS for realistic quantal response waveforms of photoreceptors. The surround input in a difference-of-Gaussians RF may either decrease or increase total noise, depending on the degree of correlation of center and surround noise. We introduce a third useful definition of sharp-bordered summation apertures: one that provides the same signal-to-noise ratio (SNR) for large-long stimuli as the real integration profiles. The SNR-equivalent summation area is N* = N2S/NN and summation time t* = t2S/tN.