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Local Spinal Cord Circuits and Bilateral Mauthner Cell Activity Function Together to Drive Alternative Startle Behaviors Yen-Chyi Liu, Melina E. Hale Current Biology Volume 27, Issue 5, Pages (March 2017) DOI: /j.cub Copyright © 2017 Elsevier Ltd Terms and Conditions
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Figure 1 Mauthner Cells Are Bilaterally Active in S-Starts, but Bilateral M-cell Firing through Intracellular Current Injection Does Not Result in an S-Start Motor Pattern (A) Simultaneous whole-cell current-clamp recordings were conducted on both M-cells while extracellular electrodes were positioned on opposite sides of the trunk (1, contralateral-rostral; 4, ipsilateral-caudal) to monitor motor output from peripheral nerves. An asterisk represents the electrical stimulus. (B) During an S-start, both M-cells always fired (left). During tail C-starts, bilateral M-cell firing was observed in some trials (middle), and single M-cell firing was observed in other trials (right). All M-cell firing was observed before motor activity in the trunk. (C) Current injection into M-cells to cause either bilateral firing (left) or unilateral firing (right) resulted in a C-start motor pattern but never an S-start motor pattern. (D) Representation of group data for all analyzed escapes elicited through tail stimulation. Dots represent the average latency for M-cell spikes to tail stimulation, bars represent the duration of motor activity, and error bars represent the SD. Averaged M-cell spike latencies and differences in timing between spikes are listed. (E) Group data for escapes elicited through suprathreshold current injection into M-cells. No S-starts were elicited in bilateral M-cell current injection trials. See also Figures S1 and S2 and Table S1. Current Biology , DOI: ( /j.cub ) Copyright © 2017 Elsevier Ltd Terms and Conditions
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Figure 2 Primary Motoneurons in the Caudal Spinal Cord Receive Short-Latency Inhibition before Receiving Mauthner Excitation during Tail Startles Current-clamp recordings were conducted on a contralateral caudal CaP (A and B), contralateral rostral CaP (C and D), or simultaneous ipsilateral M-cell and contralateral caudal CaP (F and G), while motor activity was monitored at rostral (electrode 1) and caudal (electrode 4) trunk through two extracellular electrodes. CaPs were depolarized from resting membrane potential (bottom potential in CaP traces) to just below firing threshold (top potential in CaP traces) to better visualize inhibition. (B) Left: during S-starts, short-latency inhibition was observed in caudal CaPs, and CaPs fired with a delay, out of sync with motor activity in the rostral trunk (electrode 1). Right: during C-starts, short-latency inhibition was also observed in caudal CaPs following the stimulus, but motoneurons fired simultaneously with motor activity in the rostral trunk. Numbers from top to bottom represent: sub-threshold potential cell was depolarized to, most negative potential of inhibition, and resting membrane potential. (D) During both S-starts and tail C-starts, no inhibition was observed in rostral CaPs contralateral to the stimulus. (E) Group data for escapes elicited through tail stimulation where caudal CaPs were recorded from. Solid bars represent duration of motor activity, and open bars represent duration of inhibition for CaPs; error bars represent the SD. Numbers represent the average onset latency and duration for CaP inhibition. (G) During both S-starts and tail C-starts, the M-cell fired before motor activity at both rostral and caudal trunk (electrodes 1 and 4), but after the onset of short-latency inhibition in caudal CaPs. The gray line marks the timing of the M-cell spike. (H) Group data for escapes elicited through tail stimulation where M-cells and caudal CaPs were recorded. Red numbers represent the average latency for M-cell spikes; blue numbers represent average onset latency and duration of inhibition of caudal CaPs; error bars represent the SD. M-cells always fired after the onset of inhibition observed in CaPs in both S- and C-starts. See also Figures S1 and S2 and Table S1. Current Biology , DOI: ( /j.cub ) Copyright © 2017 Elsevier Ltd Terms and Conditions
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Figure 3 CoLo Interneurons Fire Bilaterally during Tail Startles and Can Be Activated by Sensory Rohon-Beard Cells (A–G) Current-clamp recordings were conducted simultaneously on a M-cell and a CoLo (A–D), CoLos on opposite sides of the spinal cord (E), and a CoLo and a RB (F and G). (B) A single M-cell spike elicited through suprathreshold current injection can elicit a C-start motor pattern. The gray line marks the timing of the M-cell spike. (C) During both S-starts and tail C-starts, caudal CoLos were active before the M-cell fired. The gray line marks the timing of the M-cell spike. (D) Group data for escapes elicited through tail stimulation where M-cells and CoLos were recorded. Red numbers represent the average latency for M-cell spikes; blue numbers represent average onset latency and duration of CoLo spikes; error bars represent the SD. M-cells always fired after the first CoLo spike in both S- and C-starts. (E) During both S-starts and tail C-starts, CoLos on both sides of the caudal spinal cord are active continuously shortly following the stimulus. The initiation of CoLo activity corresponds to the short-latency inhibition observed in caudal CaPs. (F) During both S-starts and tail C-starts, RBs fired with a short latency following the tail stimulation. CoLo spikes can sometimes be observed before the spike of the patched RB, suggesting excitatory inputs from other RBs or other types of neurons. (G) Activity of CoLos in response to suprathreshold current injection in RBs. Some RBs can elicit CoLo spikes when fired. (G1) An overlay of seven trials of current injection elicited RB spikes and the elicited activity in CoLos. Some RBs do not elicit any activity in CoLos when fired. (G2) An overlay of 11 trials of current injection elicited RB spikes and the negligible CoLo response. See also Figures S1–S3 and Table S1. Current Biology , DOI: ( /j.cub ) Copyright © 2017 Elsevier Ltd Terms and Conditions
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Figure 4 Proposed S-Start Neural Circuit
Proposed neural circuitry for generating S-starts (A) and C-starts (B) through tail stimulation as described in text. Open half circles represent excitatory inputs, filled half circles represent inhibitory inputs. Red cells are active while white cells are inhibited. Red arrowheads represent M-cell spikes. Red lines in the fish silhouette schematic represent motor activity, asterisk represents stimulus. (A) An S-start motor pattern is generated as follows: a stimulus to the tail causes RBs in the caudal spinal cord to be activated (1), which in turn activates CoLos on both sides of the cord (2). CoLos in the ipsilateral caudal spinal cord inhibit motoneurons and their counterparts on the contralateral side. (3). Sensory information from RBs is also relayed to the M-cells to fire the ipsilateral and contralateral M-cells within short latencies of each other (4). In the rostral spinal cord, the ipsilateral M-cell activates CoLos and motoneurons on the contralateral side, causing motor output on the contralateral side and inhibiting motor output that would be otherwise generated by the contralateral M-cell (5). In the caudal spinal cord, inhibition from CoLos reduces the likelihood of motoneuron activity on the contralateral side; thus, the descending M-cell spikes are more likely to fire motoneurons on the ipsilateral side (6). This causes bilateral motor activity on opposite sides of the rostral and caudal trunk. (B) An alternative C-start can be elicited when motoneurons in the caudal cord are inhibited on the opposite side as rostral motor activity, allowing motor activity in the caudal trunk and tail to match with that in the rostral trunk (2). The ipsilateral M-cell fires slightly before the contralateral and causes motor activity on the rostral contralateral side (4). In the caudal spinal cord, motoneurons on the contralateral side are more likely to fire due to inhibition from CoLos to motoneurons on the ipsilateral side (6), thus causing unilateral motor activity on the contralateral side. See also Figures S1 and S4. Current Biology , DOI: ( /j.cub ) Copyright © 2017 Elsevier Ltd Terms and Conditions
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