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.

Analytical methods for the geometric optics of thermal vision illustrated with four species of pitvipers

“…The explicit hypotheses that the facial pit is an imaging system (Otto, 1972;Stanford and Hartline, 1980) and that pitvipers perceive a visual-thermal multispectral image (Newman and Hartline, 1982) are supported by reports that neural image processing (image sharpening) in the medulla improves the resolution of the thermal image (Stanford and Hartline, 1980), neurons in the optic tectum respond to both thermal and visual signals (Hartline et al, 1978), and a common pathway transmits thermal and visual information to the forebrain (Berson and Hartline, 1988). Further, reports of neurons responding to ipsilateral, contralateral and bilateral stimulation suggest binocular thermal stereopsis (Berson and Hartline, 1988;Goris and Terashima, 1973).…”

“…Further, reports of neurons responding to ipsilateral, contralateral and bilateral stimulation suggest binocular thermal stereopsis (Berson and Hartline, 1988;Goris and Terashima, 1973).…”

Auditory and Multisensory Responses in the Tectofugal Pathway of the Barn Owl

“…However, several exceptions from this rule can be found in the literature. The tectofugal pathway in rattlesnakes, for example, carries infrared information as well as visual (Berson and Hartline, 1988). This raises the possibility that the tectofugal pathway may have a yet undiscovered multisensory function in other species.…”

Rattlesnake orientation to prey as a function of thermal backgrounds and edges

“…Crotaline infrared receptors project to the tectum, whence receptor cells also contain excitatory centers and lateral inhibitory surrounds (Hartline, 1974;Hartline, Kass, & Loop, 1978;Haseltine, 1978). In recent years, the interactions of visual and infrared receptors have been of greatest interest to investigators (Berson & Hartline, 1988;Goris & Terashima, 1973;Hartline et aI., 1978;Terashima & Goris, 1975), giving rise to the discovery of several classes of bimodal cells in the tectum (Newman & Hartline, 1981). On balance, all of this interest in modality interaction has forestalled analysis of interactions between excitatory and inhibitory afferents within either the infrared or the visual system.…”