Passive membrane properties, afterpotentials and repetitive firing of superior colliculus neurons studied in the anesthetized cat

Abstract

Intracellular recording and staining with HRP were used to characterize cat superior colliculus neurons with identified projection into the tectobulbo-spinal tract (TBSNs). TBSNs are large multipolar neurons with heavy stem dendrites. First and second order dendrites bifurcate with an average branch power n of about 3/2. More peripheral branch points have n < 1.5. Input resistances of TBSNs range from 0.9 to 4.6 MΩ. Most TBSNs display ‘anomalous rectification’. Based on Rall's steady-state cable equations, input resistances were calculated for 3 TBSNs labelled with HRP. Assuming a specific membrane resistance of 2,300–2,600 Ωcm2 the calculated values agree well with the experimentally determined estimates from another set of non-stained TBSNs. Membrane time constants of TBSNs range from 3.0 to 5.6 ms. The electrotonic length was calculated using the ratio τ₀/τ₁. The respective average value was 1.13. TBSNs respond to orthodromic, antidromic and direct stimulation with action potentials of 60–80 mV, composed of IS- and SD-components. The critical interval for IS-SD-invasion was on average 1.6 ms. Spike decomposition occurs usually at M-level. The postspike conductance increase underlying hyperpolarizing afterpotentials (HAP) decays exponentially, with the time constants τ_F = 1.5 ms and τ_s = 13 ms. The HAP was equilibrated at membrane potentials of -73 to -90 mV. When tested by antidromic stimuli at varying intervals most TBSNs show very poor “summation” of HAP_s. A pronounced depolarizing hump (DD) follows antidromic action potentials. Discharging at short intervals leads to a substantial increase and prolongation of DD. This apparent DD-potentiation is interpreted as a phenomenon secondary to the reduction of hyperpolarizing currents. In response to directly injected currents, TBSNs discharge with frequencies up to 1,100 imp/s. The frequency-current curves of TBSNs are characterized by 3 ranges. The average f-i-slopes of the adapted discharge were 19.2 imp/s/nA and 56.4 imp/s/nA for the 1st and 2nd range, respectively. At intermediate current intensities (2nd range) TBSNs discharge in groups of 2 to 7 action potentials, following each other at intervals of 1.0–2.8 ms. The spike groups are separated by pauses of 3.5–6.3 ms duration. The transition from 1st (low frequency continuous) discharge range to 2nd (grouped) discharge range is related to the appearance of extra-spikes. Extra-spikes are generated from a decreased firing level, from the peak of an enhanced DD. During injection of depolarizing steps or ramps the firing level of TBSNs increases within 15–20 ms by 3–5 mV. A minimal current gradient requirement is absent. Short hyperpolarizations return the elevated voltage threshold back to normal and favor generation of extra-spikes. The transition from the 2nd (grouped) discharge range to the 3rd (high frequency continuous) discharge range is related to a saturation of HAP-summation. Below this level pause duration is a function of the amplitude of the hyperpolarizing potential shift between the spikes which, in turn, depends on the number and frequency of preceding spikes. It is concluded that TBSNs generate high-frequency grouped discharge as a consequence of subtle changes of excitability. Of importance are electrotonic events in connection with spike generation and invasion, changes in the spike generation mechanism itself, and changes in the state of the repolarizing systems.