Temporal frequency of whisker movement. I. Representations in brain stem and thalamus

How does processing of information change the internal representations used in subsequent stages of sensory pathways? To approach this question, we st udied the representations of whisker movements in the lemniscal and paralem niscal pathways of the rat vibrissal system. We recently suggested that the se two pathways encode movement frequency in different ways. We proposed th at paralemniscal thalamocortical circuits, functioning as phase-locked loop s (PLLs), translate temporally coded information into a rate code. Here we focus on the two major trigeminal nuclei of the brain stem, nucleus princip alis and subnucleus interpolaris, and on their thalamic targets, the ventra l posteromedial nucleus (VPM) and the medial division of the posterior nucl eus (POm). This is the first study in which these brain stem and thalamic n uclei were explored together in the same animals and using the same stimuli . We studied both single- and multi-unit activity. We moved the whiskers bo th mechanically and by air puffs; here we present air-puff-induced movement s because they are more similar to natural movements than movements induced by mechanical stimulations. We describe the basic properties of the respon ses in these brain stem and thalamic nuclei. The responses in both brain st em nuclei were similar; responses to air puffs were mostly tonic and follow ed the trajectory of whisker movement. The responses in the two thalamic nu clei were similar during low-frequency stimulations or during the first pul ses of high-frequency stimulations, exhibiting more phasic responses than t hose of brain stem neurons. However, with frequencies >2 Hz, VPM and POm re sponses differed, generating different representations of the stimulus freq uency. In the VPM, response amplitudes (instantaneous firing rates) and spi ke counts (total number of spikes per stimulus cycle) decreased as a functi on of the frequency. In the POm, latencies increased and spike count decrea sed as a function of the frequency. Having described the basic response pro perties in the four nuclei, we then focus on a specific test of our PLL hyp othesis for coding in the paralemniscal pathway. We used short-duration air puffs, much shorter than whisker movements during natural whisking. The ac tivity in this situation was consistent with the prediction we made on the basis of the PLL hypothesis.