Different Topography of the Reticulothalmic Inputs to First- and Higher-Order Somatosensory Thalamic Relays Revealed Using Photostimulation

Lam, Ying‐Wan; Sherman, S. Murray

doi:10.1152/jn.00782.2007

Cited by 57 publications

(70 citation statements)

References 31 publications

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“…In addition, stimulation of the ICc did not result in spiking of ICl neurons (20), suggesting that the intrinsic collicular projections are either not intact in this slice plane or are not sufficiently robust to exceed threshold. These results validated the specificity of stimulation via glutamate uncaging (17)(18)(19).…”

Section: Resultssupporting

confidence: 70%

“…Biocytin injections in the IC labeled fibers that terminated in the MGB, and electrical and photostimulation of the IC produced robust excitatory and inhibitory responses in recorded MGB neurons. In particular, photostimulation only results in neuronal activation at the cell body or proximal dendrites (17,18) (Fig. S2), thus confirming that intact tectothalamic projections were present in the slice.…”

Section: Discussionsupporting

confidence: 57%

“…S1D), which readily enabled the identification of subregions during physiological recordings. Intact projections in the slice were further verified using photostimulation (17)(18)(19), which was found to activate spiking only in IC neurons within ∼100 μm of the soma (ICc: n = 5, ICl: n = 5) (Fig. S2), validating the specificity of photostimulation in the IC.…”

Section: Resultsmentioning

confidence: 59%

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Topography and physiology of ascending streams in the auditory tectothalamic pathway

Lee

Sherman

2009

Proc. Natl. Acad. Sci. U.S.A.

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Auditory information is relayed from the cochlea along parallel pathways and reaches the inferior colliculus (IC) and the medial geniculate body (MGB) en route to the cortex. Although the ascending tectothalamic pathway to the ventral division of the MGB is regarded as a high-fidelity information-bearing channel, the roles of the pathways to the dorsal and medial divisions are more opaque. Here, we show fundamental differences between these ascending pathways using an in vitro slice preparation. Using photostimulation, we found three main patterns of input (excitatory, inhibitory, and mixed) that differed in each pathway. Furthermore, electrical stimulation of the central nucleus of the IC evoked a depressing response in the MGB with no metabotropic glutamate (mGlu) receptor component, whereas stimulation of the lateral cortex of the IC evoked a facilitating response with an mGlu receptor component. These data suggest that the ascending tectothalamic pathways are functionally distinct from one another.A uditory information ascends from the sensory periphery along parallel pathways, synapsing in the inferior colliculus (IC) and then the medial geniculate body (MGB) en route to the cortex. At the tectothalamic synapse, the IC central nucleus (ICc) reliably transmits excitatory and inhibitory information to the ventral division of the MGB (MGBv) (1, 2). However, the role of the tectothalamic projections from the lateral (ICl), dorsal (ICd), and caudal cortices of the IC [collectively referred to here as the shell region (ICs)] to the dorsal (MGBd) and medial (MGBm) divisions of the MGB are less well understood and may serve either a driving or modulatory role, or both (3, 4). 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 (5-7). 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). However, if the cortex provides the principal driving input to the higher order nuclei of the MGB, what is the role of the ascending tectal inputs?Another issue of interest is the observation that auditory tectothalamic inputs are composed of both excitatory and inhibitory pathways. Anatomical studies suggest that the inhibitory feedforward projections to the MGB arise throughout the IC (9, 10), and physiological investigations find several distinct classes of excitatory and inhibitory inputs (11-13). However, the topographic organization of excitatory and inhibitory inputs in the tectothalamic pathways is largely undefined. Are these pathways organized similarly across collicular and thalamic nuclei? Do they align topographically with the anisotropi...

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Section: Resultssupporting

confidence: 70%

Section: Discussionsupporting

confidence: 57%

Section: Resultsmentioning

confidence: 59%

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Topography and physiology of ascending streams in the auditory tectothalamic pathway

Lee

Sherman

2009

Proc. Natl. Acad. Sci. U.S.A.

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“…Nitroindolinyl-caged glutamate (Sigma-Aldrich) was added to the recirculating artificial cerebrospinal fluid (0.4 mM) for the experiments requiring glutamate photo-uncaging. A UV laser beam (DPSS Laser) was used to locally photolyse the caged compound over an 8 × 8 grid in a pseudorandom order (40)(41)(42)(43). The laser beam had an intensity of 20-80 mW, and the laser illumination lasted 2 ms (355 nm wavelength, frequencytripled Nd:YVO4, 100-kHz pulse repetition rate).…”

Section: Methodsmentioning

confidence: 99%

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

Viaene

Petrof

Sherman

2011

Proc. Natl. Acad. Sci. U.S.A.

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Primary somatosensory cortex (S1) receives two distinct classes of thalamocortical input via the lemniscal and paralemniscal pathways, the former via ventral posterior medial nucleus (VPM), and the latter, from the posterior medial nucleus (POm). These projections have been described as parallel thalamocortical pathways. Although the VPM thalamocortical projection has been studied in depth, several details of the POm projection to S1 are unknown. We studied the synaptic properties and anatomical features in the mouse of the projection from POm to all layers of S1 and to layer 4 of secondary somatosensory cortex (S2). Neurons in S1 responded to stimulation of POm with what has been termed Class 2 properties (paired-pulse facilitation, small initial excitatory postsynaptic potentials (EPSPs), a graded activation profile, and a metabotropic receptor component; thought to be modulatory), whereas neurons in layer 4 of S2 responded with Class 1A properties (paired-pulse depression, large initial EPSPs, an all-or-none activation profile, and no metabotropic receptor component, thought to be a main information input). Also, labeling from POm produced small boutons in S1, whereas both small and large boutons were found in S2. Our data suggest that the lemniscal and paralemniscal projections should not be thought of as parallel information pathways to S1 and that the paralemniscal projection may instead provide modulatory inputs to S1. driver | modulator | glutamatergic | barrel cortex | synapse P rimary somatosensory (also barrel or S1) cortex in rodents receives two distinct types of input from thalamus that are thought to convey different types of sensory information (1, 2). The lemniscal projection is relayed through the ventral posterior medial nucleus (VPM), whereas the paralemniscal projection is routed through posterior medial nucleus (POm) (3, 4). These projections are not only separated in thalamus, but remain largely segregated across cortical layers and in barrels and septa (3-8).The synaptic properties of the VPM or lemniscal projection to S1 have been described (9-12). 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. If the paralemniscal projection to S1 is a parallel information route (3, 4), the prediction is that the synaptic properties of this pathway should be largely or exclusively Class 1A (for detailed explanation of classification terms, see refs. 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. ResultsGlutamate Uncaging...

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“…1, A and B). In addition, photostimulation of POm resulted in EPSCs in SII (n ϭ 4), which must originate from intact thalamocortical neurons in POm, since photostimulation activates only the soma or proximal dendrites of neurons and not fibers of passage or axons antidromically (Lam and Sherman 2007;Shepherd et al 2003). POm is thus at least partly connected to SII in the slice.…”

Section: R E S U L T Smentioning

confidence: 99%

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

Lee

Sherman²

2008

Journal of Neurophysiology

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186

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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.

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Different Topography of the Reticulothalmic Inputs to First- and Higher-Order Somatosensory Thalamic Relays Revealed Using Photostimulation

Cited by 57 publications

References 31 publications

Topography and physiology of ascending streams in the auditory tectothalamic pathway

Topography and physiology of ascending streams in the auditory tectothalamic pathway

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

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

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