A tecto-rotundo-telencephalic pathway in the rattlesnake: evidence for a forebrain representation of the infrared sense

Abstract

Rattlesnakes possess a sensory system specialized for the detection of infrared (IR) radiation. IR signals ascend as far as the optic tectum, where they generate a spatiotopic map. It is unknown if such signals reach the forebrain, but the existence of prominent tectothalamic pathways in other vertebrates makes this a distinct possibility. In nonmammalian forms, the major target of ascending tectal visual signals is nucleus rotundus, a thalamic nucleus that projects in turn to the subpallial telencephalon. We sought to determine whether a tecto-rotundo-telencephalic system exists in rattlesnakes and, if so, whether it carries IR as well as visual information. We have identified a thalamic nucleus in the rattlesnake Crotalus viridis that matches the n. rotundus of other reptiles in its topographic location, cytoarchitecture, and connections. Using anterograde and retrograde transport of HRP, we have demonstrated a strong ipsilateral and weaker contralateral tectorotundal projection. Tectorotundal cells lay primarily in the deeper tectal layers, which receive input from the IR system, but also in the superficial, visual layers. In n. rotundus, single units recorded extracellularly invariably responded to visual stimuli, but many were also sensitive to unimodal IR stimuli. IR and visual receptive fields were very large and often bilateral. Some rotundal units appeared sensitive to substrate vibration. Most habituated rapidly. Nucleus rotundus was found to project to a sector of the ipsilateral anterior dorsal ventricular ridge (ADVR) of the telencephalon. Single units in this region of the ADVR resembled those in rotundus, responding to visual, IR, and/or vibrational stimuli and possessing large, often bilateral receptive fields. These findings demonstrate the existence of a tecto-rotundo-telencephalic pathway in rattlesnakes and suggest that this system conveys IR as well as visual information to the forebrain. Ascending tectofugal pathways have been implicated in the discrimination of form. Thus, pattern recognition may have to be added to orientation as a proper function of the IR system of pit vipers.