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

Abstract

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.

Anisotropic Distribution of Thalamocortical Boutons in Barrels

“…2 A) (Simons and Carvell, 1989;Minnery et al, 2003). The mean tuning ratio, defined as the average ON response (all angles) divided by the ON response at the best angle was 0.54 Ϯ 0.10, indicating a maximum angle ON response that was approximately double that of the average ON response.…”

Comprehensive mapping of whisker-evoked responses reveals broad, sharply tuned thalamocortical input to layer 4 of barrel cortex

“…Posterior nucleus neurons respond weakly and with long (Ͼ20 ms) latencies to whisker deflections under anesthesia (Diamond et al 1992a;Lavallee et al 2005), so their activity is unlikely to contribute to the responses we observed. Early studies emphasized that RFs in VPM were dominated by the PW (Waite 1973b;Shosaku 1985;Rhoades et al 1987;Sumitomo and Iwama 1987;Chiaia et al 1991), but there is extensive evidence that many VPM neurons have multiwhisker RFs, particularly under light anesthesia (Waite 1973a;Simons and Carvell 1989;Armstrong-James and Callahan 1991;Lee et al 1994a,b;Bruno and Simons 2002;Minnery et al 2003;Timofeeva et al 2004;Aguilar and Castro-Alamancos 2005). Thorough mapping of VPM RFs in awake animals or those under light anesthesia yields large mean RF sizes and maximal RFs of 10 or more whiskers, consistent with our findings (Ito 1988;Diamond et al 1992a;Nicolelis et al 1993;Nicolelis and Chapin 1994;Friedberg et al 1999Friedberg et al , 2004.…”

A Critical Window for Experience-Dependent Plasticity at Whisker Sensory Relay Synapse in the Thalamus

“…Previous studies in the rat have shown that neurons in a single whisker-specific unit in the VPm (barreloid) have different angular preferences to whisker motion, although they all receive inputs from the same whisker (Brecht and Sakmann, 2002;Temereanca and Simons, 2003;Timofeeva et al, 2003). This angular preference is likely to arise from selective innervation by directional sensitive neurons in the Pr5 (Minnery et al, 2003). The remodeling process at VPm relay synapses may play a key role in establishing angular selectivity of VPm neurons within the same barreloid.…”