Electrophysiological and Morphological Properties of Neurons in the Rat Superior Colliculus. I. Neurons in the Intermediate Layer

Abstract

To begin characterizing the neural elements underlying the dynamic properties of local circuits in the mammalian superior colliculus (SC), electrophysiological and morphological properties of individual neurons in the intermediate layer [stratum griseum intermediale (SGI)] were investigated using whole cell patch-clamp recording and intracellular staining with biocytin in slice preparations from young (17–22 days old) and adult rats (7–8 wk old). Voltage responses to depolarizing current pulses of 223 neurons recorded in young rats were classified into six subclasses: regular-spiking neurons ( n = 113), interspike intervals during depolarizing current pulses were constant; late-spiking neurons ( n = 48), initiation of repetitive firing was delayed markedly from the onset of depolarizing pulses because of a transient hyperpolarization caused by A-like currents; burst-spiking neurons ( n = 29), transient burst firing due to low-threshold Ca2+ channels were observed at the firing threshold level; fast-spiking neurons ( n = 19), constant repetitive firings at frequencies >100 Hz were observed for the duration of the depolarizing pulse; neurons with marked spike frequency adaptation ( n = 11), interspike intervals more than doubled due to spike frequency adaptation during depolarizing pulses; and neurons with rapid spike inactivation ( n = 3), spike amplitude rapidly reduced, width increased during depolarizing pulses, and spiking was terminated after generating a few spikes. In response to hyperpolarizing current pulses, two different types of inward rectification were observed; time-dependent inward rectification by hyperpolarization-activated current ( I h; n = 29) and time-independent inward rectification ( n = 111). Morphological analysis showed that neurons expressing time-dependent inward rectification by I h had large somata, extended divergent dendrites dorsally into the superficial layers, and projected axons ventrally and sometimes dorsally, all characteristic features of wide-field vertical cells. Other neurons exhibited heterogeneous morphological properties, such as multipolar, fusiform, horizontal, or pyramidal-shaped cells. In adult rats, a total of 44 neurons showed similar electrophysiological properties except for the last type. These results indicate that the local circuits of the SC include neurons with at least five different firing properties and two different rectification properties; each with distinct electrophysiological and morphological characteristics that may be correlated with the functional output of the SC.