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Asymmetries in sensory pathways from skin to motoneurons on each side of the body determine the direction of an avoidance response in hatchling Xenopus tadpoles

Fei-Yue Zhao, Brian G. Burton, Ervin Wolf and Alan Roberts

1. When swimming is initiated by tail stimulation in hatchling Xenopus tadpoles, the first trunk contraction is usually on the opposite side and directs the animal away from the stimulus. We have investigated how asymmetries in the skin sensory pathways mediate this response.

2. In -bungarotoxin-immobilized tadpoles, intracellular recordings were made of responses to ipsilateral (ISS) and contralateral skin stimulation (CSS) in thirty-two presumed motoneurons. ISS evokes an inhibitory postsynaptic potential (IPSP) followed by an excitatory postsynaptic potential (EPSP) whereas CSS only evokes an EPSP. Blocking the short latency IPSP evoked by ISS with strychnine reduced the difference in spike latency on the two sides but spikes still occurred first to CSS.

3. Motoneuron EPSPs evoked by ISS and CSS were therefore recorded during microperfusion of strychnine to block the short latency IPSP. We found: (a) the CSS-EPSPs have lower threshold, larger amplitude at a given intensity of stimulus, faster rising phase, and shorter latencies than those of ISS-EPSPs; (b) the ISS-EPSP onset latencies were longer than CSS-EPSPs and became shorter as the stimulus intensity increased while those of CSS-EPSPs remained little changed. At high stimulus intensities, EPSPs caused by CSS and ISS became similar; and (c) onset latencies of ISS-EPSPs had higher variance than those of CSS-EPSPs. However, this difference was reduced as the stimulus intensity was increased.

4. Since motoneuron EPSP onset latencies varied with stimulus intensity, we proposed that the pathway from the opposite side had stronger synapses from afferents to sensory interneurons. To test this proposal we built a neuronal population model of the spinal pathway from skin afferents, via sensory interneurons to ipsilateral and contralateral motoneurons incorporating this asymmetry. Inhibition was omitted from the model.

5. Simulated motoneuron EPSPs in response to skin stimulation on each side of the body showed the major asymmetries found experimentally. If the distribution and axonal projections of the interneurons in the two sensory pathways were made the same these differences remained. However, if the synaptic strength from sensory afferents onto interneurons projecting to the two sides were made equal, the differences between the two sides were lost.

6. We propose that the sensory pathway to contralateral motoneurons has more effective excitation from afferents to sensory interneurons which leads to these motoneurons firing first. At higher stimulus strengths, when population recruitment can blur these subtle differences in excitation between the two sides, inhibition normally plays a significant role to ensure that most first responses are still contralateral.

This article has been cited by other articles:

				W.-C. Li, S. R. Soffe, and A. Roberts Dorsal Spinal Interneurons Forming a Primitive, Cutaneous Sensory Pathway J Neurophysiol, August 1, 2004; 92(2): 895 - 904. [Abstract] [Full Text] [PDF]

				W.-C. Li, S. R. Soffe, and A. Roberts Spinal Inhibitory Neurons that Modulate Cutaneous Sensory Pathways during Locomotion in a Simple Vertebrate J. Neurosci., December 15, 2002; 22(24): 10924 - 10934. [Abstract] [Full Text] [PDF]