Impaired trigeminal control of ingestive behavior in the Prrxl1-/- mouse is associated with a lemniscal-biased orosensory deafferentation

Abstract

Although peripheral deafferentation studies have demonstrated a critical role for trigeminal afference in modulating the orosensorimotor control of eating and drinking, the central trigeminal pathways mediating that control, as well as the timescale of control, remain to be elucidated. In rodents, three ascending somatosensory pathways process and relay orofacial mechanosensory input: the lemniscal, paralemniscal, and extralemniscal. Two of these pathways (the lemniscal and extralemniscal) exhibit highly structured topographic representations of the orofacial sensory surface, as exemplified by the one-to-one somatotopic mapping between vibrissae on the animals’ face and barrelettes in brainstem, barreloids in thalamus, and barrels in cortex. Here we use the Prrxl1 knockout mouse model (also known as the DRG11 knockout) to investigate ingestive behavior deficits that may be associated with disruption of the lemniscal pathway. The Prrxl1 deletion disrupts somatotopic patterning and axonal projections throughout the lemniscal pathway but spares patterning in the extralemniscal nucleus. Our data reveal an imprecise and inefficient ingestive phenotype. Drinking behavior exhibits deficits on the timescales of milliseconds to seconds. Eating behavior shows deficits over an even broader range of timescales. An analysis of food acquisition and consummatory rate showed deficits on the timescale of seconds, and analysis of body weight suggested deficits on the scale of long term appetitive control. We suggest that ordered assembly of trigeminal sensory information along the lemniscal pathway is critical for the rapid and precise modulation of motor circuits driving eating and drinking action sequences.

Long and short whiskers differently guide snout/pellet interaction in rat oral grasping

“…Previous studies have shown that ingestive behaviour involved a continuous flow of somatosensory input from the oral region, which is used to guide oral grasping (Zeigler, Jacquin, & Miller, 1984). Orosensory deafferentation induces persistent hypophagia and a reduction in body weight, whereas whisker deafferentation appears to make little or no contribution to food intake and body weight regulation (Resulaj et al, 2022; Zeigler, Semba, et al, 1984). Although the experimental context was different, some of our findings were comparable, as initial snout contact with the nose tip and the contact phase duration lengthened after injury.…”

“…Stimulation and lesion experiments have shown that trigeminal orosensory inputs provide an essential link in the stimulus–response chain mediating eating in the rat (Resulaj et al, 2022; Zeigler, Jacquin, & Miller, 1984). Trigeminal orosensory deafferentation in the rat decreases responsiveness to food and water, disrupting sensorimotor control of eating and drinking.…”