First published online May 19, 2008
Journal of Experimental Biology 211, 1819-1828 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016402
Computational mechanisms of mechanosensory processing in the cricket
Gwen A. Jacobs*,
John P. Miller and
Zane Aldworth
Center for Computational Biology, 1 Lewis Hall, Montana State University,
Bozeman, MT 59717, USA
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Fig. 1. The cricket cercal system. (A) Acheta domestica. The cerci are the
two antenna-like structures, covered with fine hairs, extending from the rear
of the abdomen. This is a female: the ovipositor can be distinguished between
the two cerci. (B) Scanning electron microscope close-up of a segment of the
cercus. The cercus is approximately 1 cm in length. (C) Computer
reconstructions of a primary sensory interneuron (blue) and three primary
sensory afferents (red, light blue and brown) in their correct anatomical
relationships. These cells were stained in different animals and the
reconstructions were scaled and aligned to a common coordinate system. Scale:
40 µm between tick marks on the scale bars. The inset shows a cartoon of a
cut-away view of the cricket nervous system. The terminal abdominal ganglion,
where the sensory neurons and interneurons are located, is indicated with a
red arrow.
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Fig. 2. Anatomical prediction of synaptic connectivity between filiform sensory
afferents and interneurons. (A) A reconstruction of interneuron right (R)10-2
is shown in yellow. Afferent arbors from 12 different filiform hair receptors
are shown in other colors. The color of each afferent corresponds to its
direction of peak activation. These 12 classes span the range of all different
classes of receptor directional sensitivities. Inset cartoon shows the color
code indicating the preferred stimulus direction with respect to the cricket
body coordinates. (B) Composite view (saggital) of 11 different sensory
afferents from the left cercus illustrating the continuous representation of
direction selectivity within the nervous system. Cells with similar
directional tuning arborize near each other and those tuned to other
directions are spatially segregated showing their color. (C) Image of the
afferent map of air current direction, from both cerci, with an image of the
compartmental model of interneuron 10-2 imbedded in the map. Each directional
class of afferent arbors is transformed into a `statistical cloud'
corresponding to the density of synaptic terminals for that stimulus
direction. This provides a direct demonstration of the neural map of
direction. The overlap between the sensory interneuron with the afferent map
of air current direction predicts synaptic connectivity from the afferents
onto that interneuron. Here we just mask the interneuron dendrites with the
color corresponding to the statistical cloud of afferent synapses in that
region. (D) Image of the distribution of synaptic varicosities of the
population of sensory afferents from the left cercus tuned to different air
current directions from the left cercus. Same view as in B. The varicosities
form a continuous three-dimensional structure in the neuropil. Note that the
peak directional tuning of the varicosities changes continuously with location
around the structure. Starting at the top of the structure (pink) and moving
clockwise [red, yellow (out of view), green and blue].
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Fig. 3. Directional tuning curve for interneuron 10-2a. (A) Single puffs of air
from eight different directions relative to the cricket (top traces) elicit
various patterns of spiking activity (bottom traces) in an interneuron of
class R10-2a. Scale bar: x 10 ms, y 875 mm
s–1 (stimulus)/10 mV (intracellular membrane potential). (B)
To generate the tuning curve the same cell as in A was presented with 10
stimuli from each of 24 different directions in the horizontal plane (15°
separation between samples). The number of spikes elicited in the 60 ms window
following stimulus onset was counted for each trial, and mean and s.d. across
trials is shown as a function of stimulus direction. The spontaneous firing
rate of the cell was also determined, and the gray broken line shows the
expected number of spontaneous spikes in a 60 ms window. Note that stimuli
from angles –15° to 105° inhibit the firing activity of this
cell below the spontaneous rate, which can also be seen as a slight
hyperpolarization in the membrane potentials of A. (C) The mean values from B,
plotted in polar instead of Cartesian coordinates.
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Fig. 4. Directional tuning curves for ventral giant interneurons (vGIs) and dorsal
giant interneurons (dGIs). (A) Mean Cartesian tuning curves for interneurons
with axons in the ventral group, with amplitude normalized to maximal firing
rate. The shaded background represents ±1 s.d. across the populations
of specified neurons. Ai: 8-1a (medial giant interneuron, MGI); Aii: 9-1a
(lateral giant interneuron, LGI); Aiii: 9-1b; Aiv: 10-1a. (B) Mean Cartesian
tuning curves for dGIs, grouped into potential functional units (data format
as in A). Bi: 7-2a and 8-2a; Bi: 9-2a and 9-3a; Bi: 10-2a and 10-3a. (C)
Representation of peak directional selectivity of all GIs with unimodal
directional tuning in relation to the cricket. R, right; L, left.
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Fig. 5. Stimulus reconstruction and coherence measurements. (A) A 500 ms recording
of 10–200 Hz band-passed Gaussian White Noise (GWN; r.m.s.=73 mm
s–1) stimulation (lower panel) and elicited response (upper
panel) in a right 10-2a interneuron (same cell as in
Fig. 3). (B) Linear kernel
obtained from a full 100 s of simultaneously recorded stimulus and response
data. (C) Stimulus from A (black) and best linear estimate obtained from
stimulus reconstruction using kernel in B (broken blue line). The upper panel
shows the full stimulus and stimulus estimate; the lower panel shows both
after low-pass filtering below 50 Hz. (D) Upper panel: stimulus–response
coherence mean (black line) ±1 s.d. (gray background), calculated over
10 repeats of stimulus. Lower panel: power spectra of stimulus (upper and
lower panels calculated from data in A). (E) Stimulus reconstruction using
kernel from B on a test data set where the stimulus was drawn from the same
statistical distribution as the stimulus in A (upper and lower panels same
convention as in C). (F) Simultaneous recording for 500 ms of R10-2a (blue,
not the same cell as A) and L10-3a (green) in response to a 10–300 Hz
band-passed GWN stimulus (lower trace, r.m.s.=43 mm s–1). (G)
Estimated reconstruction of stimulus in F using combined kernel from R10-2a
and L10-3a (upper and lower panels same convention as in C and E). (H) Upper
panel: coherence curves from data in F obtained using only cell R10-2a (blue),
only cell L10-3a (green), and both cells together as a functional unit (red).
Lower panel: power spectrum of stimulus from F.
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Fig. 6. Failures of the linear reconstruction approach: comparison of information
rates from stimulus reconstruction and direct method measurements in the dGIs.
Error bars on the linear reconstruction information estimate are s.d. across
trials; error bars on direct method estimate represent 95% confidence.
I, information rate; dir., direct; lin., linear.
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© The Company of Biologists Ltd 2008
