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 tecto-bulbo-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 less than 1.5. Input resistances of TBSNs range from 0.9 to 4.6 M omega. 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 omega cm2 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 tau 0/tau 1. 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 tau F = 1.5 ms and tau 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 HAPS. 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.(ABSTRACT TRUNCATED AT 400 WORDS)