Somatosensory Corticothalamic Projections: Distinguishing Drivers From Modulators

Abstract

. We used a juvenile mouse thalamocortical slice preparation with whole cell recording to investigate synaptic properties of corticothalamic inputs from somatosensory cortex to the ventral posterior medial and posterior medial nuclei (98 cells). We compared these data to those obtained from activating retinal and cortical inputs to the lateral geniculate nucleus (8 cells), the former representing a prototypical driver input and the latter, a typical modulator. Retinogeniculate activation evoked large, all-or-none excitatory postsynaptic potentials (EPSPs) that showed paired-pulse depression antagonized by N-methyl-D-aspartate (NMDA) and AMPA receptor blockers but with no sign of a metabotropic glutamate receptor (mGluR) component. Corticogeniculate activation evoked small, graded EPSPs showing paired-pulse facilitation, and the EPSPs showed both NMDA and AMPA receptor component plus an mGluR1 component. In the somatosensory thalamic relays, cortical stimulation elicited glutamatergic EPSPs in all thalamic cells, and these EPSPs fell into two groups. One, elicited from cortical layer 6 to cells of both nuclei, involved small, graded EPSPs with paired-pulse facilitation, and most also showed an mGluR1 component. The other, elicited from layer 5 to cells only of the posterior medial nucleus, involved large, all-ornone EPSPs with paired-pulse depression, and none showed an mGluR component. By analogy with results from the lateral geniculate nucleus, we conclude that the input from layer 6 to both nuclei acts as a modulator but that the layer 5 input to the posterior medial nucleus serves as a driver. Our data extend a common organizing principle from first-order nuclei to higher-order thalamic relays and further implicate the latter in corticocortical communication. I N T R O D U C T I O NGuillery and Sherman have recently proposed that thalamic relays can be divided into two types: first order and higher order Sherman and Guillery 2001, 2002). First-order relays represent the first transmission to cortex of particular type of information from the periphery, and higher-order relays serve to transmit information between cortical areas via a cortico-thalamo-cortical route. Examples of the former are the lateral geniculate nucleus for vision (relaying retinal input) and the ventral posterior nucleus for somesthesis (relaying medial lemniscal input); examples of the latter are most or all of pulvinar for vision and the posterior medial nucleus for somesthesis.A key to this hypothesis is identifying the information actually relayed through thalamus. To do so, Guillery and Sherman have divided inputs to relay cells into drivers, which bring the information to be relayed, and modulators, which serve to modulate thalamic transmission of the driver input (Sherman and Guillery 1998, 2001). Examples of the former are the retinal and medial lemniscal input to the lateral geniculate nucleus and ventral posterior nucleus, respectively. Examples of the latter are brain stem cholinergic inputs from the parabrachial region and feed...

Drivers from the deep: the contribution of collicular input to thalamocortical processing

“…The speed is necessarily related to the structure, which is why these points are combined. While direct evidence is not available concerning the anatomical arrangement of synapses on MD neurons comparable to that in other thalamic regions (e.g., the pulvinar, Guillery, 1995;Reichova and Sherman, 2004), there are a few observations that suggest that the SC to MD synapses are strong and secure, which make them reasonable candidates for drivers. First of all, it was found that single pulse stimulation in the SC activated MD neurons with short latency (median 1.4 ms, including a presumed synaptic delay of only 0.57 ms) and required normal current thresholds for this type of study (mean 264 mA).…”

Fewer driver synapses in higher order than in first order thalamic relays

“…Examples of these higher order relays are the pulvinar for vision, the posterior nucleus for somesthesia, and the magnocellular portion of the medial geniculate nucleus for hearing (Sherman andGuillery, 1996, 2006;Sherman, 2005). Central to this view is evidence showing that synaptic properties of corticothalamic input from layer 5 to higher order nuclei share the same driver properties measured anatomically, physiologically, and pharmacologically as do retinogeniculate input and medial lemniscal input to the ventral posterior nucleus (Schwartz et al, 1991;Hoogland et al, 1991;Deschênes et al, 1994;Ojima, 1994;Rockland, 1996;Rouiller and Welker, 2000;Bartlett et al, 2000;Guillery et al, 2001;Li et al, 2003b;Reichova and Sherman, 2004). These higher order relays have only been recently recognized, and they seem to occupy the majority of thalamus (Sherman and Guillery, 2006).…”

Topography and physiology of ascending streams in the auditory tectothalamic pathway

“…Do they align topographically with the anisotropic frequency organization in the ICc and MGBv (1, 2)? Do excitatory and inhibitory inputs arise from the same loci, or are they topographically segregated?To investigate these issues of auditory tectothalamic organization, we developed an in vitro tectothalamic slice preparation in the mouse containing parts of the ascending pathways to the MGB.Whole-cell recordings of MGB neurons in response to photostimulation in the IC with caged glutamate were used to map the topography of excitatory and inhibitory inputs and to identify loci for subsequent electrical stimulation as well as to identify these tectothalamic synaptic inputs as drivers or modulators (5,8,12). …”

“…Whole-cell recordings of MGB neurons in response to photostimulation in the IC with caged glutamate were used to map the topography of excitatory and inhibitory inputs and to identify loci for subsequent electrical stimulation as well as to identify these tectothalamic synaptic inputs as drivers or modulators (5,8,12).…”

“…Based on the presence or absence of a cortical layer 5 input, these MGB divisions have been termed first order (MGBv; no layer 5 input) or higher order (MGBd and MGBm; having a layer 5 input), and it is thought that the higher order nuclei play an important role as part of corticothalamocortical circuits (5)(6)(7). Previous work in the somatosensory thalamus suggests that the principal driving input to higher order thalamic nuclei arises from this layer 5 input (8). In the auditory system, the anatomical substrates supporting such a driving corticothalamic pathway from layer 5 are also present (6,7).…”