Corticogeniculate neurons, corticotectal neurons, and suspected interneurons in visual cortex of awake rabbits: receptive-field properties, axonal properties, and effects of EEG arousal

Abstract

The intrinsic stability of the rabbit eye was exploited to enable receptive-field analysis of antidromically identified corticotectal (CT) neurons (n = 101) and corticogeniculate (CG) neurons (n = 124) in visual area I of awake rabbits. Eye position was monitored to within 1/5 degrees. We also studied the receptive-field properties of neurons synaptically activated via electrical stimulation of the dorsal lateral geniculate nucleus (LGNd). Whereas most CT neurons had either complex (59%) or motion/uniform (15%) receptive fields, we also found CT neurons with simple (9%) and concentric (4%) receptive fields. Most complex CT cells were broadly tuned to both stimulus orientation and velocity, but only 41% of these cells were directionally selective. We could elicit no visual responses from 6% of CT cells, and these cells had significantly lower conduction velocities than visually responsive CT cells. The median spontaneous firing rates for all classes of CT neurons were 4-8 spikes/s. CG neurons had primarily simple (60%) and concentric (9%) receptive fields, and none of these cells had complex receptive fields. CG simple cells were more narrowly tuned to both stimulus orientation and velocity than were complex CT cells, and most (85%) were directionally selective. Axonal conduction velocities of CG neurons (mean = 1.2 m/s) were much lower than those of CT neurons (mean = 6.4 m/s), and CG neurons that were visually unresponsive (23%) had lower axonal conduction velocities than did visually responsive CG neurons. Some visually unresponsive CG neurons (14%) responded with saccadic eye movements. The median spontaneous firing rates for all classes of CG neurons were less than 1 spike/s. All neurons synaptically activated via LGNd stimulation at latencies of less than 2.0 ms had receptive fields that were not orientation selective (89% motion/uniform, 11% concentric), whereas most cells with orientation-selective receptive fields had considerably longer synaptic latencies. Most short-latency motion/uniform neurons responded to electrical stimulation of the LGNd (and visual area II) with a high-frequency burst (500-900 Hz) of three or more spikes. Action potentials of these neurons were of short duration, thresholds of synaptic activation were low, and spontaneous firing rates were the highest seen in rabbit visual cortex. These properties are similar to those reported for interneurons in several regions in mammalian central nervous system. Nonvisual sensory stimuli that resulted in electroencephalographic arousal (hippocampal theta activity) had a profound effect on the visual responses of many visual cortical neurons.(ABSTRACT TRUNCATED AT 400 WORDS)