Angular Tuning Bias of Vibrissa-Responsive Cells in the Paralemniscal Pathway

Abstract

One of the most salient features of primary vibrissal afferents is their sensitivity to the direction in which the vibrissae move. Directional sensitivity is also well conserved in brainstem, thalamic, and cortical neurons of the lemniscal pathway, indicating that this property plays a key role in the organization of the vibrissal system. Here, we show that directional tuning is also a fundamental feature of second-order interpolaris neurons that give rise to the paralemniscal pathway. Quantitative assessment of responses to vibrissa deflection revealed an anisotropic organization of receptive fields with regard to topography, response magnitude, and the degree of angular tuning. Responses evoked by all vibrissae within the receptive field of each cell exhibited a high consistency of direction preference, but a striking difference in angular tuning preference was found among cells that reside in the rostral and caudal divisions of the interpolaris nucleus. Although in caudal interpolaris vectors of angular preference pointed in all directions, in rostral interpolaris virtually all vectors pointed upward, revealing a strong preference for this direction. Control experiments showed that the upward bias did not rely on a preferential innervation of rostral cells by upwardly tuned primary vibrissa afferents, nor did it rely on a direction-selective recruitment of feedforward inhibition. We thus propose that the upward preference bias of rostral cells, which project to the posterior group of the thalamus, emerges from use-dependent synaptic processes that relate to the kinematics of whisking.

Consistency of Angular Tuning in the Rat Vibrissa System

“…Both of these structures are considered part of the paralemniscal system in that both receive most of their trigeminal inputs from the spinal trigeminal interpolaris nucleus (SpVi) (Bruce et al 1987;Huerta et al 1983;Killackey and Erzurumlu 1981;Pierret et al 2000;Zhang and Deschenês 1997). SpVi neurons display conserved angular preferences when the vectors for angular preference were compared using four angles of deflection (Furuta et al 2006). This is consistent with the idea that the relatively high similarity indices in superior colliculus and second somatosensory cortex reflect the properties of input cells in SpVi.…”

“…Inputs from adjacent vibrissae can evoke different response magnitudes in central neurons with some evoking responses that are similar in magnitude to those evoked by the principal vibrissa and others producing negligible responses (trigeminal ganglion: Lichtenstein et al 1990; principal trigeminal nucleus: Minnery and Simons 2003; Veinante and Deschênes 1999; trigeminal nucleus interpolaris: Furuta et al 2006;VPM: Minnery et al 2003;Simons and Carvell 1989;Timofeeva et al 2004;Po thalamus: Diamond et al 1992;Furuta et al 2006;barrel cortex: Simons 1978;Simons and Carvell 1989; second somatosensory cortex: Kwegyir-Afful and Keller 2004; superior colliculus: Hemelt and Keller 2007). While overall similarity indices were low (Ͻ0.4) in all four brain regions, this may be of little functional consequence if the adjacent vibrissae were contributing little to the activity of the neuron in comparison to the activity evoked by the principal vibrissa.…”

“…One system in which neurons display angular tuning is the vibrissa system in the rodent. Neurons in all stations along this pathway have varying levels of angular tuning [trigeminal ganglion : Lichtenstein et al 1990; principal trigeminal nucleus: ; trigeminal nucleus interpolaris: Furuta et al 2006; ventroposterior medial nucleus of the thalamus (VPM): Simons and Carvell 1989;Timofeeva et al 2003;barrel cortex: Bruno et al 2003;Simons 1978;Simons and Carvell 1989; second somatosensory cortex: Kwegyir-Afful and Keller 2004; superior colliculus: Hemelt and Keller 2007]. Typically, analysis of angular tuning has been performed only on responses to deflections of the principal vibrissae, which evoke the largest magnitude responses in their associated neurons.…”

“…Angular tuning is largely conserved across the receptive fields of neurons in the trigeminal interpolaris nucleus (Furuta et al 2006). In the somatosensory (barrel) cortex, angular consistency is preserved when broad tuning angles (i.e., rostral vs. caudal) are considered (Kida et al 2005;Shimegi et al 2000).…”

Inhibitory Gating of Vibrissal Inputs in the Brainstem

“…Yet, none of the interpolaris or caudalis neurons retrogradely labeled from the PrV were reported to be immunoreactive for GABA or glutamic acid decarboxylase (GAD) (Haring et al, 1990). This is somehow intriguing because singlecell labeling studies already showed that the SpVi projection to the PrV arises principally from small-sized local circuit cells (Jacquin et al, 1989a), and in situ hybridization of the GAD67 mRNA has revealed a large number of small-sized GABAergic cells in the SpVi (Furuta et al, 2006). Moreover, electron microscopic studies already documented a rich network of synaptic contacts with numerous axodendritic and axoaxonic GABAergic synapses in sensory trigeminal nuclei (Ide and Killackey, 1985;Bae et al, 2000Bae et al, , 2005.…”