Neuronal Substrates for Infrared Contrast Enhancement and Motion Detection in Rattlesnakes

Pit vipers detect infrared (IR) radiation with loreal pit organs [1] that are connected to the hindbrain by trigeminal nerve fibers [2-4]. The pattern of central afferent termination forms a topographical representation of the sensory periphery within the nucleus of the lateral descending trigeminal tract (LTTD) [4-7]. All LTTD neurons project to another specialized, ipsilateral hindbrain area, the nucleus reticularis caloris (RC) [8-11], before IR signals are integrated with visual signals in the optic tectum [12, 13]. Pit-organ-innervating afferent fibers provoke in individual LTTD neurons a direct, robust spike activity upon peripheral activation [7, 14]. This discharge is truncated by an indirect, delayed synaptic inhibition from afferent fibers of adjacent sensory areas through parallel microcircuitry that converges with afferent fibers onto the same target neurons [7]. Here, we determined the impact of this interaction on IR contrast enhancement and/or motion detection in LTTD and RC neurons using isolated whole-brain preparations of rattlesnakes with intact pit organs. Simulated and real IR source motion provoked weak directional tuning of the discharge in LTTD neurons and RC neurons expressed a strong, motion-direction-differentiating activity. The hierarchically increasing motion sensitivity potentially derives from a direction-specific inhibition or spike frequency adaptation of LTTD neuronal discharge that becomes further pronounced by convergent projections onto individual RC neurons. The emerging signaling pattern complies with contrast enhancement (LTTD) and extraction of movement-related signals (RC), thereby forming a motion detection mechanism that encodes moving IR sources relative to the ambient temperature [14].