Hidden synaptic differences in a neural circuit underlie differential behavioral susceptibility to a neural injury

  1. Akira Sakurai  Is a corresponding author
  2. Arianna N Tamvacakis
  3. Paul S Katz
  1. Neuroscience Institute, Georgia State University, United States
10 figures

Figures

The Tritonia swim central pattern generator.

(A) A schematic diagram of the swim central pattern generator (CPG). The CPG consists of three types of interneurons: C2, cerebral cell 2; DSI, dorsal swim interneuron; VSI, ventral swim …

https://doi.org/10.7554/eLife.02598.003
Individual variability in the extent of swim impairment by a lesion.

(A) Nerve-transected animals were blindly paired with sham-operated animals. Two examples (Pair 1 and Pair 2) show different effects on the number of body flexions during the escape swim behavior …

https://doi.org/10.7554/eLife.02598.004
Individuals differed in the extent of motor pattern impairment by disconnection of PdN6.

(A) A schematic drawing of the Tritonia brain showing how axonal impulse propagation was blocked in PdN6 either by delivering TTX (1 × 10−4M) into a suction pipette or by physical transection. The …

https://doi.org/10.7554/eLife.02598.006
Individual variability in the extent of motor pattern impairment by disconnection of PdN6.

(A) The number of VSI bursts per swim motor pattern episode recorded from Animal 1 was more affected by blocking PdN6 than that from Animal 2 (same individuals as in Figure 3B). The swim motor …

https://doi.org/10.7554/eLife.02598.007
The extent of motor impairment showed little or no correlation with the C2-evoked VSI spiking recorded before blocking PdN6.

(A) A schematic illustration showing the stimulus (C2) and recording (VSI) microelectrodes, the direction of action potential propagation (dashed arrows) in C2 and VSI, and synaptic action (+, …

https://doi.org/10.7554/eLife.02598.009
Figure 6 with 1 supplement
The extent of motor impairment showed a strong correlation with C2-evoked VSI depolarization recorded after blocking PdN6.

(A) A schematic illustration showing the stimulus (C2) and recording (VSI) microelectrodes, the direction of action potential propagation (dashed arrows) in C2, and synaptic action (+, excitatory; …

https://doi.org/10.7554/eLife.02598.011
Figure 6—source data 1

Source data for panels C and D.

https://doi.org/10.7554/eLife.02598.012
Figure 6—source data 2

Source data for figure supplement 1 panel B.

https://doi.org/10.7554/eLife.02598.013
Figure 6—figure supplement 1
C2 recruited unidentified neurons to excite VSI.

(A) C2 stimulation caused a bombardment of small EPSPs that lasted longer than the duration of stimulation (black trace). Recruitment of these polysynaptic EPSPs was minimized by superfusion of …

https://doi.org/10.7554/eLife.02598.014
Figure 7 with 1 supplement
The extent of motor impairment correlated with the inhibitory component of C2-to-VSI synapse.

(A) Two examples (Animals 5 and 6) of VSI membrane potential responses to C2 stimulation recorded with PdN6 disconnected in normal saline (left) and in high divalent cation (Hi-Di) saline (right) to …

https://doi.org/10.7554/eLife.02598.015
Figure 7—source data 1

Source data for panel B.

https://doi.org/10.7554/eLife.02598.016
Figure 7—source data 2

Source data for figure supplement 1.

https://doi.org/10.7554/eLife.02598.017
Figure 7—figure supplement 1
The magnitude of C2-evoked depolarization in VSI in normal saline correlated with the amplitude of hyperpolarizing phase of C2-to-VSI synaptic potential.

The magnitude of C2-evoked VSI depolarization in normal saline did not correlate to the direct C2-evoked depolarization measured in Hi-Di saline (A, R2 = 0.04, p=0.37 by linear regression, N = 24), …

https://doi.org/10.7554/eLife.02598.018
Figure 8 with 1 supplement
The direction of spike propagation in VSI axon was predictive of susceptibility of the swim motor pattern to PdN6 disconnection.

(A) A schematic diagram showing the recording configuration. VSI action potentials were recorded with an intracellular microelectrode in the soma and an extracellular en passant suction electrode on …

https://doi.org/10.7554/eLife.02598.019
Figure 8—source data 1

Source data for panel D.

https://doi.org/10.7554/eLife.02598.020
Figure 8—source data 2

Source data for figure supplement 1 panels B and C.

https://doi.org/10.7554/eLife.02598.021
Figure 8—figure supplement 1
Inter- and intra-individual variation in the direction of VSI spike propagation during the swim motor pattern.

(A) Individual bursts were categorized into three groups: (i) burst with all antidromic spikes, (ii) burst with mixture of antidromic and orthodromic spikes, and (iii) burst with all orthodromic …

https://doi.org/10.7554/eLife.02598.022
An artificial synaptic conductance created a hidden circuit change that caused no motor impairment with PdN6 intact.

A) Recordings of a five-cycle swim motor pattern with PdN6 intact (Ai). Introduction of an artificial synaptic conductance from C2 to VSI using dynamic clamp (D.C.) had no effect on the number of …

https://doi.org/10.7554/eLife.02598.023
Figure 9—source data 1

Source data for panels B and C.

https://doi.org/10.7554/eLife.02598.024
With PdN6 disconnected, an artificial synaptic conductance reduced the number of VSI bursts.

(A) Recordings from the same preparation as Figure 9, but with PdN6 disconnected. PdN6 disconnection reduced the number of VSI bursts from five to four bursts per swim episode (Ai) (Compare with Figu…

https://doi.org/10.7554/eLife.02598.025

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