Response Transformation and Receptive-Field Synthesis in the Lemniscal Trigeminothalamic Circuit

To understand how the lemniscal trigeminothalamic circuit (PrV → VPM) of the rodent whisker-to-barrel pathway transforms afferent signals, we applied ramp-and-hold deflections to individual whiskers of lightly narcotized rats while recording the extracellular responses of neurons in either the ventroposterior medial (VPM) thalamic nucleus or in brain stem nucleus principalis (PrV). In PrV, only those neurons antidromically determined to project to VPM were selected for recording. We found that VPM neurons exhibited smaller response magnitudes and greater spontaneous firing rates than those of their PrV inputs, but that both populations were similarly well tuned for stimulus direction. In addition, fewer VPM (74%) than PrV neurons (93%) responded with sustained, or tonic, discharges during the plateau phase of the stimulus. Neurons in both populations responded most robustly to deflections of a single, “principal whisker” (PW), and the majority of cells in both PrV (90%) and VPM (73%) also responded to deflections of at least one adjacent whisker (AW). AW responses in both nuclei occurred on average at longer latencies and were more temporally dispersed than PW responses. Lateral inhibition, as evidenced by AW-evoked activity suppression, was rare in PrV but prevalent in VPM. In both nuclei, however, suppression was weak, with AW responses being on average excitatory. Our results suggest that the receptive-field structures and response properties of individual VPM neurons can be explained in large part by input from one or a small number of PrV neurons, but that intrathalamic mechanisms act to further transform the afferent signal.

Response Properties of Whisker-Associated Trigeminothalamic Neurons in Rat Nucleus Principalis

Nucleus principalis (PrV) of the brain stem trigeminal complex mediates the processing and transfer of low-threshold mechanoreceptor input en route to the ventroposterior medial nucleus of the thalamus (VPM). In rats, this includes tactile information relayed from the large facial whiskers via primary afferent fibers originating in the trigeminal ganglion (NV). Here we describe the responses of antidromically identified VPM-projecting PrV neurons ( n = 72) to controlled ramp-and-hold deflections of whiskers. For comparison, we also recorded the responses of 64 NV neurons under identical experimental and stimulus conditions. Both PrV and NV neurons responded transiently to stimulus onset (on) and offset (off), and the majority of both populations also displayed sustained, or tonic, responses throughout the plateau phase of the stimulus (75% of NV cells and 93% of PrV cells). Averageon and off response magnitudes were similar between the two populations. In both NV and PrV, cells were highly sensitive to the direction of whisker deflection. Directional tuning was slightly but significantly greater in NV, suggesting that PrV neurons integrate inputs from NV cells differing in their preferred directions. Receptive fields of PrV neurons were typically dominated by a “principal” whisker (PW), whose evoked responses were on average threefold larger than those elicited by any given adjacent whisker (AW; n = 197). However, of the 65 PrV cells for which data from at least two AWs were obtained, most (89%) displayed statistically significanton responses to deflections of one or more AWs. AW response latencies were 2.7 ± 3.8 (SD) ms longer than those of their corresponding PWs, with an inner quartile latency difference of 1–4 ms (±25% of median). The range in latency differences suggests that some adjacent whisker responses arise within PrV itself, whereas others have a longer, multi-synaptic origin, possibly via the spinal trigeminal nucleus. Overall, our findings reveal that the stimulus features encoded by primary afferent neurons are reflected in the responses of VPM-projecting PrV neurons, and that significant convergence of information from multiple whiskers occurs at the first synaptic station in the whisker-to-barrel pathway.

Neonatal Deafferentation Does Not Alter Membrane Properties of Trigeminal Nucleus Principalis Neurons

In the brain stem trigeminal complex of rats and mice, presynaptic afferent arbors and postsynaptic target cells form discrete modules (“barrelettes”), the arrangement of which duplicates the patterned distribution of whiskers and sinus hairs on the ipsilateral snout. Within the barrelette region of the nucleus principalis of the trigeminal nerve (PrV), neurons participating in barrelettes and those with dendritic spans covering multiple barrelettes (interbarrelette neurons) can be identified by their morphological and electrophysiological characteristics as early as postnatal day 1. Barrelette cells have focal dendritic processes, are characterized by a transient K+ conductance ( I A), whereas interbarrelette cells with larger soma and extensive dendritic fields characteristically exhibit low-threshold T-type Ca2+ spikes (LTS). In this study, we surveyed membrane properties of barrelette and interbarrelette neurons during and after consolidation of barrelettes in the PrV and effects of peripheral deafferentation on these properties. During postnatal development (PND1–13), there were no changes in the resting potential, composition of active conductances and Na+ spikes of both barrelette and interbarrelette cells. The only notable changes were a decline in input resistance and a slight increase in the amplitude of LTS. The infraorbital (IO) branch of the trigeminal nerve provides the sole afferent input source to the whisker pad. IO nerve transection at birth abolishes barrelette formation as well as whisker-related neuronal patterns all the way to the neocortex. Surprisingly this procedure had no effect on membrane properties of PrV neurons. The results of the present study demonstrate that distinct membrane properties of barrelette and interbarrelette cells are maintained even in the absence of input from the whiskers during the critical period of pattern formation.

C-Fiber Depletion Alters Response Properties of Neurons in Trigeminal Nucleus Principalis

Kwan, C. L., J. A. Demaro, J. W. Hu, M. F. Jacquin, and B. J. Sessle. C-fiber depletion alters response properties of neurons in trigeminal nucleus principalis. J. Neurophysiol. 81: 435–446, 1999. The effects of C-fiber depletion induced by neonatal capsaicin treatment on the functional properties of vibrissa-sensitive low-threshold mechanoreceptive (LTM) neurons in the rat trigeminal nucleus principalis were examined in adult rats. Neonatal rats were injected either with capsaicin or its vehicle within 48 h of birth. The depletion of unmyelinated afferents was confirmed by the significant decrease in plasma extravasation of Evan's blue dye induced in the hindlimb skin of capsaicin-treated rats by cutaneous application of mustard oil and by the significant decrease of unmyelinated fibers in both the sciatic and infraorbital nerves. The mechanoreceptive field (RF) and response properties of 31 vibrissa-sensitive neurons in capsaicin-treated rats were compared with those of 32 vibrissa-sensitive neurons in control (untreated or vehicle-treated) rats. The use of electronically controlled mechanical stimuli allowed quantitative analysis of response properties of vibrissa-sensitive neurons; these included the number of center- and surround-RF vibrissae within the RF (i.e., those vibrissae which when stimulated elicited ≥1 and <1 action potential per stimulus, respectively), the response magnitude and latency, and the selectivity of responses to stimulation of vibrissae in different directions with emphasis on combining both the response magnitude and direction of vibrissal deflection in a vector analysis. Neonatal capsaicin treatment was associated with significant increases in the total number of vibrissae, in the number of center-RF vibrissae per neuronal RF, and in the percentage of vibrissa-sensitive neurons that also responded to stimulation of other types of orofacial tissues. Compared with control rats, capsaicin-treated rats showed significant increases in the response magnitude to stimulation of surround-RF vibrissae as well as in response latency variability to stimulation of both center- and surround-RF vibrissae. C-fiber depletion also significantly altered the directional selectivity of responses to stimulation of vibrissae. For neurons with multiple center-RF vibrissae, the proportion of center-RF vibrissae with net vector responses oriented toward the same quadrant was significantly less in capsaicin-treated compared with control rats. These changes in the functional properties of principalis vibrissa-sensitive neurons associated with marked depletion of C-fiber afferents are consistent with similarly induced alterations in LTM neurons studied at other levels of the rodent somatosensory system, and indeed may contribute to alterations previously described in the somatosensory cortex of adult rodents. Furthermore, these results provide additional support to the view that C fibers may have an important role in shaping the functional properties of LTM neurons in central somatosensory pathways.