Effects of Focal Ionizing Radiation of the Squid Stellate Ganglion on Synaptic and Axonal Transmission in the Giant-Fiber Pathway

William F Gilly; P Teal; Edward E Graves; Jackei Lo; M Bret Schneider; Reese Zasio; John R Adler Jr

doi:10.7759/cureus.13110

Effects of Focal Ionizing Radiation of the Squid Stellate Ganglion on Synaptic and Axonal Transmission in the Giant-Fiber Pathway

Cureus. 2021 Feb 3;13(2):e13110. doi: 10.7759/cureus.13110.

Authors

William F Gilly¹, P Teal¹, Edward E Graves², Jackei Lo³, M Bret Schneider^{4

5}, Reese Zasio⁶, John R Adler Jr^{7

4}

Affiliations

¹ Biology, Hopkins Marine Station, Stanford University, Pacific Grove, USA.
² Radiation Oncology, Stanford University School of Medicine, Stanford, USA.
³ Radiation Oncology, Stanford Health Care, Stanford, USA.
⁴ Neurosurgery, Stanford University School of Medicine, Stanford, USA.
⁵ Psychiatry, Stanford University School of Medicine, Stanford, USA.
⁶ Veterinary Service Center, Stanford University School of Medicine, Stanford, USA.
⁷ Radiation Oncology, Stanford University Medical Center, Stanford, USA.

Abstract

Ionizing radiation is clinically used to treat neurological problems and reduce pathological levels of neural activity in the brain, but its cellular-level mechanisms are not well understood. Although spontaneous and stimulated synaptic activity has been produced in rodents by clinically and environmentally relevant doses of radiation, the effects on basic excitability properties of neurons have seldom been reported. This study examined the effects of focused ionizing radiation on synaptic transmission and action potential generation in the squid giant-fiber system, which includes the giant synapse between a secondary interneuron and the tertiary giant motor axons. Radiation of 140-300 Gy was delivered to a stellate ganglion of a living squid over several minutes, with the contralateral stellate ganglion serving as an internal control. No qualitative changes in the efficacy of synaptic transmission were noted in conjunction with stimulation of the input to the giant synapse, although in one irradiated ganglion, the refractory period increased from about 5 ms to more than 45 seconds. Small but significant changes in the action potential recorded from the giant motor axon in response to electrical stimulation were associated with an increased maximum rate of fall and a shortened action potential duration. Other action-potential parameters, including resting potential, overshoot, the maximum rate of the rise, and the refractory period were not significantly changed. Attempts to account for the observed changes in the action potential were carried through a Hodgkin-Huxley model of the action potential. This approach suggests that an increase in the maximum voltage-gated potassium conductance of about 50% mimics the action potential shortening and increased rate of fall that was experimentally observed. We propose that such an effect could result from phosphorylation of squid potassium channels.

Keywords: action potential; axon; glutamatergic synaptic transmission; irradiation; potassium conductance; squid; synapse.

Grants and funding

Gift funds supporting this work were donated by ZAP Surgical Systems, Inc. 590 Taylor Way, San Carlos, CA 94070.