The anatomical connections from the whiskers to the rodent somatosensory (barrel) cortex form two parallel (lemniscal and paralemniscal) pathways. It is unclear whether the paralemniscal pathway is directly involved in tactile processing, because paralemniscal neuronal responses show poor spatial resolution, labile latencies and strong dependence on cortical feedback. Here we show that the paralemniscal system can transform temporally encoded vibrissal information into a rate code. We recorded the representations of the frequency of whisker movement along the two pathways in anaesthetized rats. In response to varying stimulus frequencies, the lemniscal neurons exhibited amplitude modulations and constant latencies. In contrast, paralemniscal neurons in both thalamus and cortex coded the input frequency as changes in latency. Because the onset latencies increased and the offset latencies remained constant, the latency increments were translated into a rate code: increasing onset latencies led to lower spike counts. A thalamocortical loop that includes cortical oscillations and thalamic gating can account for these results. Thus, variable latencies and effective cortical feedback in the paralemniscal system can serve the processing of temporal sensory cues, such as those that encode object location during whisking. In contrast, fixed time locking in the lemniscal system is crucial for reliable spatial processing.

In active sensation, sensory information is acquired via movements of sensory organs; rats move their whiskers repetitively to scan the environment, thus detecting, localizing, and identifying objects. Sensory information, in turn, affects future motor movements. How this motor-sensory-motor functional loop is implemented across anatomical loops of the whisker system is not yet known. While inducing artificial whisking in anesthetized rats, we recorded the activity of individual neurons from three thalamic nuclei of the whisker system, each belonging to a different major afferent pathway: paralemniscal, extralemniscal (a recently discovered pathway), or lemniscal. We found that different sensory signals related to active touch are conveyed separately via the thalamus by these three parallel afferent pathways. The paralemniscal pathway conveys sensor motion (whisking) signals, the extralemniscal conveys contact (touch) signals, and the lemniscal pathway conveys combined whisking–touch signals. This functional segregation of anatomical pathways raises the possibility that different sensory-motor processes, such as those related to motion control, object localization, and object identification, are implemented along different motor-sensory-motor loops.

How does processing of information change the internal representations used in subsequent stages of sensory pathways? To approach this question, we studied the representations of whisker movements in the lemniscal and paralemniscal pathways of the rat vibrissal system. We recently suggested that these two pathways encode movement frequency in different ways. We proposed that paralemniscal thalamocortical circuits, functioning as phase-locked loops (PLLs), translate temporally coded information into a rate code. Here we focus on the two major trigeminal nuclei of the brain stem, nucleus principalis and subnucleus interpolaris, and on their thalamic targets, the ventral posteromedial nucleus (VPM) and the medial division of the posterior nucleus (POm). This is the first study in which these brain stem and thalamic nuclei were explored together in the same animals and using the same stimuli. We studied both single- and multi-unit activity. We moved the whiskers both mechanically and by air puffs; here we present air-puff-induced movements because they are more similar to natural movements than movements induced by mechanical stimulations. We describe the basic properties of the responses in these brain stem and thalamic nuclei. The responses in both brain stem nuclei were similar; responses to air puffs were mostly tonic and followed the trajectory of whisker movement. The responses in the two thalamic nuclei were similar during low-frequency stimulations or during the first pulses of high-frequency stimulations, exhibiting more phasic responses than those of brain stem neurons. However, with frequencies >2 Hz, VPM and POm responses differed, generating different representations of the stimulus frequency. In the VPM, response amplitudes (instantaneous firing rates) and spike counts (total number of spikes per stimulus cycle) decreased as a function of the frequency. In the POm, latencies increased and spike count decreased as a function of the frequency. Having described the basic response properties in the four nuclei, we then focus on a specific test of our PLL hypothesis for coding in the paralemniscal pathway. We used short-duration air puffs, much shorter than whisker movements during natural whisking. The activity in this situation was consistent with the prediction we made on the basis of the PLL hypothesis.

The vibrissal system of the rat is an example of active tactile sensing, and has recently been used as a prototype in construction of touch-oriented robots. Active vibrissal exploration and touch are enabled and controlled by musculature of the mystacial pad. So far, knowledge about motor control of the rat vibrissal system has been extracted from what is known about the vibrissal systems of other species, mainly mice and hamsters, since a detailed description of the musculature of the rat mystacial pad was lacking. In the present work, the musculature of the rat mystacial pad was revealed by slicing the mystacial pad in four different planes, staining of mystacial pad slices for cytochrome oxidase, and tracking spatial organization of mystacial pad muscles in consecutive slices. We found that the rat mystacial pad contains four superficial extrinsic muscles and five parts of the M. nasolabialis profundus. The connection scheme of the three parts of the M. nasolabialis profundus is described here for the first time. These muscles are inserted into the plate of the mystacial pad, and thus, their contraction causes whisker retraction. All the muscles of the rat mystacial pad contained three types of skeletal striated fibers (red, white, and intermediate). Although the entire rat mystacial pad usually functions as unity, our data revealed its structural segmentation into nasal and maxillary subdivisions. The mechanisms of whisking in the rat, and hypotheses concerning biomechanical interactions during whisking, are discussed with respect to the muscle architecture of the rat mystacial pad. Anat Rec, 293:1192Rec, 293: -1206