Parallel Thalamic Pathways for Whisking and Touch Signals in the Rat

Abstract

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.

Developmental and comparative aspects of posterior medial thalamocortical innervation of the barrel cortex in mice and rats

“…Although the significance of such differences is unknown, one possibility is that mice have different demands on sensory-motor integration that underlies active whisking in comparison with rats. The POm nucleus transmits signals related to whisker movement (Yu et al, 2006). The speed of whisker movements is faster in mice than in rats, a reflection of species differences in the composition of fiber types of which the intrinsic whisker muscles are composed (Jin et al, 2004).…”

“…In both rats and mice, afferents from the ventral posterior medial (VPM) nucleus form dense, whisker-related clusters of terminations that target the barrels. This pathway—the so-called lemniscal pathway—conveys signals related to both vibrissal movement and touch (Yu et al, 2006). Developmentally, the temporal and spatial progression of VPM thalamocortical axon (TCA) ingrowth into barrel cortex, colonization of layer IV, and formation of whisker-related clusters that match emergence of layer IV barrels have been well-described during the early postnatal period in both rats and mice (Wise and Jones, 1978; Erzurumlu and Jhaveri, 1990; Catalano et al, 1991; Senft and Woolsey, 1991; Agmon et al, 1993; Schlaggar and O’Leary, 1994; Rebsam et al, 2002).…”

“…Such POm TCAs also terminate in the dysgranular cortex that separates major body parts within the somatosensory cortex. This pathway—the so-called paralemniscal pathway—conveys signals related to vibrissal movement (Ahissar et al, 2000; Yu et al, 2006). Thus, in rats the two thalamic streams form largely non-overlapping, complementary patterns of terminations in and outside of layer IV, thereby establishing semi-independent circuits for tactile information processing (Koralek et al, 1988; Chmielowska et al, 1989; Lu and Lin, 1993; Kim and Ebner, 1999; Ahissar et al, 2001; Bureau et al, 2006).…”

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“…Even though the precise relationship between form and function in this case is still not determined, it has been proposed that Bt could be more involved with presynaptic facilitation and show more structural plasticity than Bp In rodents, tactile information from the whiskers is conveyed to S1 by at least 3 pathways (Pierret et al, 2000;Alloway, 2008;Pouchelon et al, 2012;Ahissar et al, 2000;Yu et al, 2006). These pathways have been implicated with carrying information about distinct whisking attributes and remain relatively segregated in S1 (Yu et al, 2006). However, very little is known about their relative contribution to feedforward projections from S1 to S2, PV, PR, S1c.…”

“…and plays a role in object localization and identification (Yu et al, 2006). The modulatory role of the paralemniscal pathway (Viaene et al, 2011) is also under the influence of the locus coeruleus (Simpson et al, 1999).…”