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First published online August 8, 2008
Journal of Experimental Biology 211, 2624-2637 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.019711

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Characterization of a descending pathway: activation and effects on motor patterns in the brachyuran crustacean stomatogastric nervous system

Ulrike B. S. Hedrich and Wolfgang Stein^*

Institute of Neurobiology, Ulm University, D-89069 Ulm, Germany

View larger version (36K): [in this window] [in a new window]   Fig. 1. Projections and activity patterns of the inferior ventricular (IV) neurons. (A) Schematic drawing of the foregut of the crab C. pagurus with the brain and the stomatogastric nervous system (STNS) attached. The foregut consists of four chambers with different functions: the esophagus (swallowing), the cardiac sac (storage of food), the gastric mill (chewing of food) and the pylorus (filtering of food). The STNS is located on the dorsal side of the foregut, and the brain on the dorsal side of the esophagus. The dorsal ventricular nerve (dvn) and the inferior ventricular nerve (ivn) were recorded extracellularly. For the ivn, we used a pair of hook electrodes to determine the direction of spike propagation. Adapted from Katz et al. (Katz et al., 1989). (B) Representation of the isolated STNS and the brain in C. pagurus. The STNS consists of four ganglia, including the unpaired stomatogastric ganglion (STG, 26 cells) and esophageal ganglion (OG, 15–16 cells) and the paired commissural ganglia (CoG, each about 500 cells). The brain and the STNS are connected via the unpaired ivn and the paired circumesophageal commissures (coc, dashed lines). In preparations using the isolated STNS, the coc were transected. dgn, dorsal gastric nerve; dpon, dorsal posterior esophageal nerve; ion, inferior esophageal nerve; lgn, lateral gastric nerve; lvn, lateral ventricular nerve; mvn, medial ventricular nerve; son, superior esophageal nerve; stn, stomatogastric nerve. (C) Extracellular recordings of the ivn (top and middle traces) and the dvn (bottom trace) in the intact animal. Both the ivn recording closer to the brain (ivn high; top trace) and the ivn recording closer to the STNS (ivn low; middle trace) show the activities of neurons that descend from and ascend to the brain. LP, lateral pyloric neuron; PD, pyloric dilator neurons; PY, pyloric constrictor neurons. (D) Magnification of Fig. 1C, showing the spikes of two neurons that descend from the brain to the STNS. The descending spikes first occurred on the ivn high recording (top trace) and then on the ivn low recording (lower trace).

View larger version (66K): [in this window] [in a new window]   Fig. 2. Anatomical features of IV neurons. (A) C. pagurus brain with stained IV neurons after backfilling the ivn with NiCl2. The areas indicated by the black boxes are magnified below the main image, and bottom right shows the somata of the IV neurons in area 17 [nomenclature after Sandeman et al. (Sandeman et al., 1992)]. No arborizations within the brain were observed. (B) Frontal section of a brain showing the dorso-medial location of the IV neuron somata. Somata were stained with a Lucifer Yellow backfill of the ivn. (C) Cross-section of the ivn. Eight axons were visible (arrows), two of which belonged to the IV neurons. (D) Schematic drawing of ivn projections in the brain, as revealed by ivn backfills. The somata of the IV neurons marked by the arrow were located in area 17 of the brain. Two (ascending) axons projected along the midline towards the anterior part of the brain, but could not be followed further than the AMPN (anterior medial protocerebral neuropil). The four other axons projected towards the coc. (E) Schematic drawing of IV neuron projections (summary). The IV neurons project via the son and the ion to the CoG and via the stn to the STG.

View larger version (62K): [in this window] [in a new window]   Fig. 3. Sensory-induced activity in the intact animal. (A) Extracellular recordings of the ivn and the dvn before and after food injection. Top: ivn recording close to the brain. Middle: recording of the ivn close to the STNS. Bottom: pyloric rhythm on the dvn. Each dot labels the beginning of a new pyloric cycle. The pyloric period increased from 1.06 s before feeding to 0.77 s after feeding. (B) Left: phase plot of the pyloric neurons PD and LP before (open boxes) and after feeding (filled boxes). Medians of the beginning and end of the activity phase are given for each neuron. Black boxes show upper and lower quartiles. *P<0.05; **P<0.01 (Wilcoxon signed-rank test). Right: number of spikes per bin (250 ms) of the IV neurons before (open boxes) and after (filled boxes) feeding. (C) Extracellular recordings of ivn and dvn before (left) and after (right) chemosensory stimulation (upper two traces). In the two lower traces ivn activity was separated into the descending and ascending neurons by computer analysis. After chemosensory stimulation the descending (IV) neurons started to burst, whereas the activity of the ascending neurons appeared to remain unchanged. The bursts of the descending neurons were time locked with LG neuron bursts on the dvn. (D) Box plots (minimum, lower quartile, median, upper quartile, maximum) of period, burst duration and mean intraburst spike frequency of the rhythmic activity of the descending neurons. The square represents the mean. (E) Extracellular recordings of dvn and ivn in vivo (two bottom traces) during rhythmic IV neuron activity (top trace). LG neuron bursts coincided with each burst of the IV neurons that possessed a spike frequency of 30 Hz or more. The firing frequencies of LG and the IV neurons were measured as a sliding average with a bin width of 1 s (top two traces).

View larger version (37K): [in this window] [in a new window]   Fig. 4. IV neuron activity in the isolated STNS. (A) Multisweep recordings (n=39) of ivn high and low, son, stn and ion, triggered on the IV action potential on ivn high during rhythmic IV activity. The IV neuron action potential was observed in all nerves, except the ion. Action potentials on the stn are truncated. (B) Box plots (minimum, lower quartile, median, upper quartile, maximum) of period, burst duration and mean intraburst spike frequency of rhythmic IV activity in the isolated STNS. The square gives the mean. (C) Extracellular recordings of lgn and ivn in vitro during rhythmic IV activity (bottom two traces). With every IV burst, its spike frequency exceeding more than 30 Hz, a LG neuron burst occurred (sliding average with a bin width of 1 s). IV neuron bursts and LG neuron bursts were time locked.

View larger version (18K): [in this window] [in a new window]   Fig. 5. IV neuron effects on the pyloric rhythm. (A) Intracellular recordings of PD and LP neurons. The ivn was extracellularly stimulated at 40 Hz. The spike activities of both PD and LP neurons diminished during the stimulus. (B) Mean number of spikes per burst of the pyloric neurons PD, LP, PY, VD (ventricular dilator) and IC (inferior cardiac), and pyloric cycle period before (light gray boxes), during (open boxes) and after stimulation (dark gray boxes). *P<0.05, ***P<0.001, significantly different from pre- and post-control (ANOVA).

View larger version (31K): [in this window] [in a new window]   Fig. 6. ivn stimulation elicits gastric mill rhythms. (A) In preparations without spontaneous gastric mill rhythm, rhythmic ivn stimulation (40 Hz intratrain frequency) elicited a gastric mill rhythm which included activities of LG (lower trace, extracellular recording of lgn), DG (middle trace, extracellular recording of dgn) and gastric motor (GM) neurons (dgn recording and intracellular recording of GM neuron). The gastric mill rhythm lasted for the duration of the stimulation. (Bi) Stimulation period determined the period of the rhythm: plot of gastric mill period over stimulus period. Means of 6N32 animals. Regression line: slope 1.37, R2=0.98. (Bii) Phase plot of the gastric mill motor neurons LG, DG and GM during 40 Hz ivn stimulation with train durations and intertrain intervals of 6 s, respectively. (Biii) Burst durations (left) and mean intraburst spike frequencies (right) of LG, DG and GM neurons (stimulus parameters as in Bii). (C) Entrainment of the gastric mill rhythm. Extracellular recordings of lgn and dgn before (top) and during ivn stimulation. The period of the gastric mill rhythm fell into synchrony with the ivn stimulation; it was entrained. AGR, anterior gastric receptor.

View larger version (40K): [in this window] [in a new window]   Fig. 7. Effects of ivn stimulation on the esophageal rhythm. (A) Intracellular recordings of the VD motor neuron (lower trace) and the LG neuron (middle trace), and an extracellular recording of the ion, illustrating the activity of the esophageal motor neuron (OMN; upper trace). ivn stimulation enhanced OMN activity. (B) Box plots (minimum, lower quartile, median, upper quartile, maximum) of OMN activity (left, bin width 6 s) and maximum instantaneous firing frequency (right) before (open boxes) and during (filled boxes) ivn stimulation. (C) Box plots showing spikes per burst, period, burst duration, mean intraburst spike frequency and duty cycle of OMN before (open boxes) and after ivn stimulation (filled boxes). *P<0.05, **P<0.01, ***P<0.001 (Wilcoxon signed-rank test).

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