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First published online August 17, 2007
Journal of Experimental Biology 210, 2961-2968 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.003624

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Directional asymmetry in responses of local interneurons in the crayfish deutocerebrum to hydrodynamic stimulation of the lateral antennular flagellum

DeForest Mellon, Jr^1,* and Joseph A. C. Humphrey^1,2

¹ Department of Biology, University of Virginia, Charlottesville, VA 22903, USA
² Department of Mechanical and Aerospace Engineering, University of Virginia, Charlottesville, VA 22903, USA

View larger version (90K): [in this window] [in a new window]   Fig. 1. (A) Anterior aspects of Procambarus clarkii, showing the long paired second antennae (asterisks) and the biramous antennules, the lateral flagella of which are indicated by white arrows. There is an upward curve to each lateral flagellum, which in this large animal is 2.5 cm long. (B) Several annuli of a lateral antennular flagellum of P. clarkii. Aesthetasc sensilla (asterisks) are arrayed ventrally on each annulus of the distal half of the flagellum, usually in groups of 2–4. At least three other types of sensillum occur on the medial and lateral flagella, including the most numerous class, the beaked hairs, indicated here with white arrows, and a standing feathered hair (white caret).

View larger version (9K): [in this window] [in a new window]   Fig. 2. Diagram of the plumbing circuits associated with the reversible-flow olfactometer. A standard crayfish head preparation was secured in a recording chamber (not shown), and the lateral antennular flagellum on one side was inserted into the olfactometer and sealed at the base with VaselineTM. Fluid could be introduced to the olfactometer either through port A, at the base of the antennule, or alternatively through port B, beyond the tip of the flagellum. Solenoid switches were controlled so that when either water or odorant entered through one port, the exhaust to the opposite port was simultaneously opened. The diagram shows an instance when water is entering port A, flowing through the olfactometer past the flagellum in the PD direction, and out through exhaust B (arrows).

View larger version (17K): [in this window] [in a new window]   Fig. 3. Hydrodynamic and odorant response characteristics of Type I OL interneurons. (A) Intracellular records from a Type I cell in response to water and odorant pulses (indicated by upward excursions in horizontal lines below the record). The response to the onset of the water pulse was a phasic burst of impulses followed by a shallow hyperpolarization. The response to a brief (1 s) odor pulse consisted of a short hydrodynamic and a much longer spike train, the latter being dose-dependent. The dotted line (marked 0 in this and following figures) indicates the zero potential level. (B) The difference in response latencies between hydrodynamic (open bars) and odorant (filled bars) responses. Numerals next to each pair of bars show relative concentrations of the standard (0.1% w/v) tetramin odorant. Each bar is the mean ± 1 s.e.m. of five responses. (C) Response–intensity function of the neuron represented in A and B. Each data point is the mean ± s.e.m. of five odor presentations at that relative concentration to standard tetramin. The linear fit of the data points is described by the equation y=8(logx)+39.6, R=0.99.

View larger version (29K): [in this window] [in a new window]   Fig. 4. (A–C) Typical paired records from Type I neurons in three different preparations to water and odorant flow past the antennular flagellum in the (PD) proximal-to-distal and the (DP) distal-to-proximal directions. The cells were most sensitive to hydrodynamic movements in the PD direction, whereas the responses to odorants in the two respective flow directions were not very different from one another (see data in Fig. 5). The hydrodynamic aspects of odorant onset were damped by adaptation to the previous (water onset) stimulus and by the nearly seamless operation of the switching valve. At the start of a standard stimulus sequence, water was suddenly switched on from a no-flow condition; after 3 s odor was seamlessly exchanged for water within the olfactometer during a 4-s period, after which water replaced the odor flow for an additional 3 s. Rates of water flow through the olfactometer with the antennular flagellum in place for the neurons in A and B were, respectively, 15 ml min–1 (PD) and 14.4 ml min–1 (DP), 14.7 ml min–1 (PD) and 14.4 ml min–1 (DP). Odor flow rates for A and B, respectively, were 15.6 ml min–1 (PD) and 14.4 ml min–1 (DP), 18 ml min–1 (PD) and 16.8 ml min–1 (DP). Flow rates of water through the olfactometer in C were 14.4 ml min–1 (PD) and 13.8 ml min–1 (DP). Odor flow rates were 17.4 ml min–1 (PD) and 15 ml min–1 (DP), respectively.

View larger version (8K): [in this window] [in a new window]   Fig. 5. (A,B) Dose–response relationships for two Type I interneurons to different concentrations of tetramin delivered, respectively, in the PD flow direction (squares) and the DP flow direction (crosses). Each point is the mean ± 1 s.e.m. of spike responses to five odorant presentations. Linear fits of the responses of the neuron in A to odorant flows in the two directions are described by the equations (PD), y=13.4(logx)+53.4, R=0.97; (DP), y=14.8(logx)+57.5, R=0.98. Linear fits of the responses of the neuron in B to odorant flows are described by (PD), y=5.6(logx)+16.9, R=0.84, (DP), y=4.3(logx)+16.7, R=0.86. Paired t-test statistics for each of the means in the two plots indicate that, with one marginal exception (A, 0.1 relative concentration), the plots for the respective flow directions in each cell are not significantly different from each other.

View larger version (3K): [in this window] [in a new window]   Fig. 6. Bar graph illustrating differences in the spike responses of 12 Type I neurons following the onset of water flowing past the antennular flagellum in the PD direction (filled bar) and in the DP direction (open bar). Data represent the mean number of spikes following stimulus presentations (± 1 s.e.m.); the number of stimulus presentation pairs from which the means were calculated for each preparation was between 4 and 27. Statistical significance of the differences between the means is P<0.0025. The flow rate in the DP direction in each experiment was normalized to the PD flow rate. The mean value for flow rate obtained across all experiments was 1.12±0.06 (± s.e.m.).