Spatial and temporal integration in primary trigeminal nucleus of rattlesnake infrared system.

Abstract

The spatial and temporal characteristics of the infrared responses of single neurons in the nucleus of the lateral descending trigeminal tract (LTTD) of the rattlesnake were investigated. The LTTD is the sole projection site of trigeminal neurons that innervate the thermoreceptive pit organ. In contrast to the responses of the primary infrared neurons, which have phasic and tonic components, the neurons in the LTTD respond strictly phasically to a sustained infrared stimulus. During an excitatory stimulus, the transient burst is followed by suppression of firing or by reduction of the new rate below the rate that would have occurred in the absence of stimulation. The phasic character of the responses may enable these neurons to encode more accurately changes in the pattern of infrared stimuli. Neurons in the LTTD show adaptation within limited regions of their receptive fields, while responses in other regions remain undiminished. This indicates that each LTTD neuron receives input from a population of primary infrared neurons. LTTD neurons respond to infrared stimuli of intensity less than 0.01 mW/cm2, which is below the threshold reported for primary afferent neurons; this also suggests convergence of a number of primary infrared afferents onto each LTTD neuron. LTTD neurons have smaller excitatory receptive fields than do the primary afferent neurons in the infrared system, indicating that spatial sharpening also occurs in this nucleus. Receptive fields of LTTD neurons may have inhibitory areas flanking the excitatory area. Introduction of a stimulus into the inhibitory area results in depression of the background discharge; thus, the inhibition is due to an active process, not to rebound from excitation. Inhibition can also be demonstrated by simultaneous stimulation of the excitatory and inhibitory receptive-field areas, resulting in a decreased excitatory response. We suggest that convergence of antagonistic excitatory and inhibitory inputs can explain the time course of LTTD responses to infrared stimulation and the architecture of LTTD receptive fields. Such excitatory and inhibitory interaction, similar to that postulated for the responses of some vertebrate retinal ganglion cells, could function to provide the basis for directional selectivity, motion sensitivity, and border enhancement in the infrared system. Unlike the visual system, however, in the infrared system excitatory-inhibitory interactions allow the construction of small excitatory receptive fields in the LTTD from the larger receptive fields of the primary afferent neurons, resulting in a highly evolved trigeminal system with visionlike function.