Rainer Voigt

Response properties of lobster chemoreceptors: tuning of primary taste neurons in walking legs

Summary1.We determined the tuning properties of 66 single chemoreceptor cells from the legs of the lobsterHomarus americanus. The specificity of these (taste) cells was tested electrophysiologically in the upper range of biologically relevant stimulus concentrations (3×10−4 mol/l) with 15 compounds listed in Table 1.2.Most of the chemoreceptors surveyed were narrowly tuned to specific test chemicals (Fig. 3). The best stimuli for these chemoreceptors were glutamate (Glu), ammonium chloride (NH4), betaine (Bet) and hydroxyproline (OH-Pro) (Fig. 4). Cell populations were defined by their best stimulus. Populations of cells responding best to Glu and NH4 were extremely narrowly tuned; populations responding best to Bet and OH-Pro were less narrowly tuned (Fig. 5, Table 2).3.Each cell population showed a range of response specificities, from cells responding to only one compound to cells responding more broadly to other compounds. Within each population cells were arranged by their tuning breadth (H). Cells that shared a best stimulus but responded also to other compounds showed no consistency for the next best stimulus (Fig. 6). This suggests that even cells responding to the same stimulus do not share the same receptor complement.4.The response patterns to Glu, NH4 and Bet elicited across all the chemoreceptor cells surveyed can be distinguished statistically as different from each other and from all others tested. Similarly, OH-Pro can be distinguished from all other stimuli except glycine and taurine (Figs. 8 and 9).5.Systematic prior exposure to all 15 test compounds (corresponding to 21 stimulus exposures) at our stimulus concentrations reduced the absolute sensitivity of Glu best cells but did not change the slope of their dose-response functions (Fig. 10) with respect to earlier results (Derby and Atema 1982a).6.We suggest that extremely narrowly tuned cells in lobster legs may function to detect key compounds as feeding stimuli over a large dynamic range of mixture concentrations such as found in nature. These cells may not be affected as much as broadly tuned cells by ambient backgrounds of cross-adapting compounds. In addition, both narrowly tuned and broadly tuned cells may participate in across fiber patterns to encode the quality of naturally occurring stimulus mixtures.

Tuning of chemoreceptor cells of the second antenna of the American lobster (Homarus americanus) with a comparison of four of its other chemoreceptor organs

Summary1.We determined the spectral tuning properties of 47 chemoreceptor cells of the antenna of Homarus americanus to amino acids and other compounds. Tests with 17 single compounds at 10-4M showed 40 of 47 cells responded best to hydroxyproline, 4 cells to taurine and 3 cells to betaine. Mean tuning breadth (H-metric) doubled with 10 fold increase in concentration.2.In hydroxyproline-best cells the mean threshold for hydroxyproline (Hyp) was found between 10-7M and 10-8M. An equimolar mixture of the 17 compounds generated a shallower stimulus-response function with thresholds similar to Hyp function (mixture suppression). Hyp-best cells were relatively narrowly tuned, often with arginine or leucine as second best stimuli.3.Thus, physiologically the second antenna of H. americanus is a major chemoreceptor organ. It is more than any of the 5 chemoreceptor organs studied so far dominated by a single best-cell type (Hyp). Receptor cell composition of antennae resembles that of antennules more than legs or maxillipeds. Hyp-best cells in antennae and lateral antennules have similar tuning spectra.4.Our cell tuning studies argue for independent receptors for all amino acids tested. We conclude that diversity of receptor cell tuning is created by cell-specific blends of receptors. At the organ level, differences in organ tuning result from different blends of receptor cells.

Frequency filter properties of lobster chemoreceptor cells determined with high-resolution stimulus measurement

Abstract1.We developed a high resolution, on-line stimulus measurement system for accurate control of chemical stimulus applications for Homarus americanus lateral antennule chemoreceptors. Focal stimulus presentations in an electrophysiological preparation with the receptor sensilla intact were measured at small spatial (30 μm) and time (5 ms) scales.2.We tested 15 receptor cells with ten 100 ms pulses of 104M hydroxyproline at 0.5, 1, 2 and 4 Hz and with a single 8 s square pulse. Individual cells showed differences in their capabilities to resolve pulses (“flicker fusion”). At 2 Hz stimulation, some cells could follow stimulus pulses while others could not. At 4 Hz, 3 cells could still encode individual stimulus pulses accurately. The population resolved pulses up to 2 Hz; at 4 Hz, the population response to a pulse series approximated the response to a square pulse.3.Repetitive stimulation caused a gradual decrease in the number of spikes and a gradual increase in first spike latency (“cumulative adaptation”). Increased stimulation frequency resulted in greater cumulative adaptation.4.Since individual differences in adaptation and disadaptation rates of the receptor cells could not be attributed to measured stimulus variability in situ, lobster chemoreceptor cell populations have intrinsic temporal diversity which, we hypothesize, could be used to analyze pulsatile stimuli that occur in natural turbulent odor plumes.

Temporal resolution in olfaction III: flicker fusion and concentration-dependent synchronization with stimulus pulse trains of antennular chemoreceptor cells in the American lobster

Abstract To understand how chemoreceptor organs may extract temporal information from odor plumes, we investigated the frequency filter properties of lobster chemoreceptor cells. We used rapid stimulation and high-resolution stimulus measurement for accurate stimulus control and recorded extracellular responses from chemoreceptors in the lobster lateral antennule in situ. We tested 16 hydroxyproline-sensitive cells with a series of ten 100-ms pulses at 10, 100 and 1000 μmol l−1 at stimulation frequencies from 0.5 Hz to 4 Hz. Receptor cell responses could accurately encode 10 μmol l−1, but not 100 or 1000 μmol l−1 pulses, delivered at rates of 4 Hz. Flicker-fusion frequency and synchronization with the stimulus pulse train were concentration dependent: performance rates above 1 Hz became poorer both with increasing pulse amplitude and frequency. Flicker fusion frequency was 3 Hz for 100 μmol l−1 pulses and 2 Hz for 1000 μmol l−1 pulses. Individual cells showed differences in their stimulus pulse following capabilities, as measured by the synchronization coefficient. These individual differences may form a basis for coding temporal features of an odor plume in an across-fiber pattern.

Response properties of chemoreceptors from the medial antennular filament of the lobster Homarus americanus

We determined the spectral tuning properties of 53 single cells from the medial antennular filament of the lobster Homarus americanus. Test stimuli were 15 single compounds and a mixture that included all 15 test compounds. Three main cell populations were found: hydroxyproline best (14 cells), taurine best (13 cells), and arginine best (11 cells). Most hydroxyproline and taurine best cells were narrowly tuned and had no consistent next best stimulus. In contrast, arginine best cells were generally broadly tuned and had consistent second (leucine) and third (lysine) best stimuli. Mixture suppression occurred in most cells. Responses of hydroxyproline, taurine, and arginine best cells to the mixture were 25%, 38%, and 50%, respectively, relative to the responses of these cells to their best compound alone (100%). In a second experiment, we tested 12 arginine sensitive cells with a series of arginine analogs. Most cells were broadly tuned and as a population showed a similar response ratio to arginine, leuc...

An Initial Study on the Effects of Signal Intermittency on the Odor Plume Tracking Behavior of the American Lobster, Homarus americanus

of the world after each molt. That is, ommatidia viewing the most anterior region of the animals visual space now sample a more lateral region of visual space. As a consequence, the retinotopic map in the brain must undergo comparable rearrangements to accommodate inputs from new ommatidia sampling visual space in front of the animal. The retinotopic map has been determined for adult animals at the first two synaptic layers in the brain (6), but that of the juvenile remains to be studied. The retinotopic map must be plastic to accommodate the changing retinal mosaic as the eye grows. Supported by grants from the National Science Foundation, National Eye Institute, and the National Institutes of Mental Health. C. McGuiness and S. Meadors received REU Fellowships from the National Science Foundation. We thank the f the world after each molt. That is, ommatidia viewing the most terior egion f the animals visual space now sample a more ateral region f visual space. As a consequence, the retinotopic ap in the brain must undergo comparable rear ng ments to ccommodate inputs from new ommatidia sampling visual space front of the animal. The retinotopic map has been determined for dult animals at the first two synaptic layers n the b ain (6), but at of the juvenil remains to be studied. The retinotopic map ust be plastic o accommodate the changing retinal mosaic as the Monomoy National Wildlife Refuge, Morris Island, Chatham, Massachusetts.

Across-fiber patterns may contain a sensory code for stimulus intensity.

Various models for sensory coding have used statistical approaches based on the assumption that the stimulus intensity parameter is represented in the afferent neurons as mean firing frequency. In this paper we question the assumption that this is the only code for intensity. We show that in lobster olfactory receptors narrowly tuned to hydroxyproline, an across-fiber pattern (AFP) code distinguished more concentration levels over a 5 log step range than a response magnitude code and, unlike the latter, was unaffected by response summation time. AFP discrimination of stimulus intensity appears to be based on high inter-cell response variability and low intra-cell response variability.

Chemoreception by the red‐jointed fiddler crab Uca minax (Le Conte): Spectral tuning properties of the walking legs

The red‐jointed fiddler crab Uca minax is one of the most abundant macroinvertebrates inhabiting the temperate western Atlantic salt marshes, along the eastern and southern coasts of the United States. Dactyl chemoreception is the primary sensory modality involved in food detection. Ninety‐six chemoreceptor cells from 69 male and female second and third legs were tested with 20 compounds known to be stimulatory in other decapods. Each compound was tested as 1 s pulses at 10‐3M. Overall, chemoreceptor cells on the dactyls responded strongest to glutamate and ammonium chloride followed by citric acid. Glutamate‐ and ammonium chloride‐best cells formed the most prominent cell populations and were relatively narrowly tuned. Individual cells exhibited a range of tuning breadths based on responses to single compounds. Amines were moderately stimulatory. Surprisingly, hexose sugars which cause strong behavioural responses in U. minax elicited only weak physiological responses. Glutamate sensitivity separates U. ...

Spectral tuning of chemoreceptor cells in the lateral antennules of the American lobster, Homarus Americanus

Chemoreceptor cells in the lateral flagellum of the first antennae (lateral antennule) of the American lobster, Homarus americanus, serve, among other functions, in long distance orientation and mediate chemical recognition of food and chemical information used in social interactions. Based upon extracellular recordings of action potentials, we report on 60 cells identified with a 15‐compound equimolar mixture of mostly amino acids and a few other compounds used in previous studies of lobster chemoreceptors. Subsequently, all cells were tested with each compound separately. Forty‐three percent of all cells responded strongest to hydroxyproline, 13% to taurine, and 10% to glutamate. These cells were generally narrowly tuned and had no consistent second best stimulus. Other cells were more broadly tuned and responded strongest to valine, arginine, leucine, glutamine, serine, glycine, alanine and ammonium. Most chemoreceptor cells responded less to a mixture containing their best compound than to the best co...

Tuning Properties of Chemoreceptor Cells of the American Lobster: Temporal Filters

Chemical stimuli in the environment are distributed in a turbulent fashion that results in a chaotic series of patches of varying concentrations. The distribution of these patches changes with increasing distance from the odor source [1]. A patch of odor moving over a stationary point is measured as a pulse of odor occurring in time [2,3]. Animals such as lobsters that orient to distant odor sources extract spatial information from the temporal pulse patterns. We hypothesize that their chemoreceptors should be designed to encode pulsatile information as it occurs at varying stimulus concentrations and frequencies in an odor plume. This study investigates the temporal filter properties of chemoreceptor cells of the lateral antennule (which mediates distance orientation) of the lobster Homarus americanus.