Synaptic Properties of Thalamic and Intracortical Inputs to Layer 4 of the First- and Higher-Order Cortical Areas in the Auditory and Somatosensory Systems

Abstract

Lee CC, Sherman SM. Synaptic properties of thalamic and intracortical inputs to layer 4 of the first-and higher-order cortical areas in the auditory and somatosensory systems. J Neurophysiol 100: 317-326, 2008. First published April 24, 2008 doi:10.1152/jn.90391.2008. The thalamus is an essential structure in the mammalian forebrain conveying information topographically from the sensory periphery to primary neocortical areas. Beyond this initial processing stage, "higherorder" thalamocortical connections have been presumed to serve only a modulatory role, or are otherwise functionally disregarded. Here we demonstrate that these "higher-order" thalamic nuclei share similar synaptic properties with the "first-order" thalamic nuclei. Using whole cell recordings from layer 4 neurons in thalamocortical slice preparations in the mouse somatosensory and auditory systems, we found that electrical stimulation in all thalamic nuclei elicited large, glutamatergic excitatory postsynaptic potentials (EPSPs) that depress in response to repetitive stimulation and that fail to activate a metabotropic glutamate response. In contrast, the intracortical inputs from layer 6 to layer 4 exhibit facilitating EPSPs. These data suggest that higher-order thalamocortical projections may serve a functional role similar to the first-order nuclei, whereas both are physiologically distinct from the intracortical layer 6 inputs. These results suggest an alternate route for information transfer between cortical areas via a corticothalamocortical pathway.

Topography and physiology of ascending streams in the auditory tectothalamic pathway

“…Interestingly, these physiological characteristics resemble the driver and modulator properties found in the somatosensory thalamus (8) and layer 4 cells in the auditory and somatosensory cortices (28,29). In this framework, driver inputs are physiologically characterized by large EPSPs, paired-pulse depression, and no mGlu receptor component, whereas modulator inputs demonstrate paired-pulse facilitation and an mGlu receptor component (5).…”

“…Whole-cell recordings of MGB neurons in response to photostimulation and electrical stimulation, pharmacology, and the histological processing of tissue were carried out using standard procedures, as described in our related studies of cortical synapses (28,29). For detailed procedures, see SI Materials and Methods.…”

Properties of the thalamic projection from the posterior medial nucleus to primary and secondary somatosensory cortices in the mouse

“…Attention has been focused recently on the role of higher order thalamic nuclei, such as POm, as an integral link in a transthalamic route for corticocortical communication (10). Implicit in this concept is the idea that these transthalamic circuits are feed forward, such as from S1 to S2, and there is indeed evidence for this (38).…”

“…The synaptic properties of the VPM or lemniscal projection to S1 have been described (9)(10)(11)(12). VPM inputs to layer 4 and the subgranular layers have Class 1* (or driver) properties, suggesting that they are main information routes, whereas the projections to layers 2/3 have predominantly Class 2 properties, suggesting a modulatory rather than information-bearing function.…”

“…11-13). POm is known to provide Class 1A input to layer 4 of secondary somatosensory cortex (S2) (10), but the POm projection to S1 has yet to be described. We thus studied the properties of the POm thalamocortical projection and found that the POm projection to S1 is entirely Class 2 in nature, suggesting that it provides modulatory inputs to S1 rather than functioning as a parallel information pathway.…”