Role of the trigeminal mesencephalic nucleus in rat whisker pad proprioception

Abstract

BackgroundTrigeminal proprioception related to rodent macrovibrissae movements is believed to involve skin receptors on the whisker pad because pad muscles operate without muscle spindles. This study was aimed to investigate in rats whether the trigeminal mesencephalic nucleus (TMnu), which provides proprioceptive feedback for chewing muscles, may be also involved in whisker pad proprioception.MethodsTwo retrograde tracers, Dil and True Blue Chloride, were injected into the mystacial pad and the masseter muscle on the same side of deeply anesthetized rats to label the respective projecting sensory neurons. This double-labeling technique was used to assess the co-innervation of both structures by the trigeminal mesencephalic nucleus (TMnu).In a separate group of anesthetized animals, the spontaneous electrical activities of TMnu neurons were analyzed by extracellular recordings during spontaneous movements of the macrovibrissae. Mesencephalic neurons (TMne) were previously identified by their responses to masseter muscle stretching. Changes in TMne spontaneous electrical activities, analyzed under baseline conditions and during whisking movements, were statistically evaluated using Student's t-test for paired observations.ResultsNeuroanatomical experiments revealed different subpopulations of trigeminal mesencephalic neurons: i) those innervating the neuromuscular spindles of the masseter muscle, ii) those innervating the mystacial pad, and iii) those innervating both structures. Extracellular recordings made during spontaneous movements of the macrovibrisae showed that whisking neurons similar to those observed in the trigeminal ganglion were located in the TMnu. These neurons had different patterns of activation, which were dependent on the type of spontaneous macrovibrissae movement. In particular, their spiking activity tonically increased during fan-like movements of the vibrissae and showed phasic bursting during rhythmic whisking. Furthermore, the same neurons may also respond to masseter muscle stretch.Conclusionsresults strongly support the hypothesis that the TMnu also contains first-order neurons specialized for relaying spatial information related to whisker movement and location to trigeminal-cortical pathways. In fact, the TMnu projects to second-order trigeminal neurons, thus allowing the rat brain to deduce higher-order information regarding executed movements of the vibrissae by combining touch information carried by trigeminal ganglion neurons with proprioceptive information carried by mesencephalic neurons.

Whisking mechanics and active sensing

“…The rat has thus no direct access to (θ w , φ w , ζ w ), though some information may be available through the mesencephalic nuclei [60,61]. Recent studies have suggested that reafferent signals reporting whisking phase could be combined with an efferent copy of whisking midpoint and amplitude to estimate angular whisker position θ w [62,63,64].…”

Neurons within the trigeminal mesencephalic nucleus encode for the kinematic parameters of the whisker pad macrovibrissae

“…Altogether, for the first time, these studies demonstrated that besides the TG, even the Me5 neurons are involved in macrovibrissae innervation, which role we speculated to be related with encoding spatial information relative to vibrissae movements (Mameli et al. , ).…”

“…The goal of this part of the study was to investigate whether the Me5 neurons, which, as previously demonstrated responded to spontaneous and artificial movements of the vibrissae (Mameli et al. , ), are also involved in encoding the related kinematic parameters and specifically the direction, frequency, and amplitude of single displacements.…”

“…It has been demonstrated in fact that spontaneous and artificial movements of the macrovibrissae, without touching any object, elicited significant responses in the rat Me5 nucleus (Mameli et al. , ). Moreover, neuroanatomical procedures showed that a retrograde tracer injected into the mystacial pad extensively labeled a discrete number of Me5 neurons, while the injection of an anterograde tracer into the Me5 nucleus demonstrated that the peripheral terminals of these same neurons targeted the upper part of the macrovibrissae with fibers spiraling around the circumference of the vibrissae shaft (Mameli et al.…”

The effect of whisker movement on radial distance estimation: a case study in comparative robotics

“…Objects in the environment sometimes move and, for example, when a shrew is hunting crickets it needs to determine both the location and movement of that prey animal to execute an accurate fatal attack (Anjum et al, 2006). Another consideration is that rats have no spindles in their whisking muscles, and therefore do not have accurate proprioception of their whiskers (Diamond et al, 2008; Mameli et al, 2010). Since accurate radial distance estimation is dependent on well characterized contact speed, a signal-based method, such as the contact duration feature approach presented here, is of potentially great importance.…”