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Synaptic properties of thalamic input to layers 2/3 and 4 of primary somatosensory and auditory cortices.

ABSTRACT: We studied the synaptic profile of thalamic inputs to cells in layers 2/3 and 4 of primary somatosensory (S1) and auditory (A1) cortices using thalamocortical slices from mice age postnatal days 10-18. Stimulation of the ventral posterior medial nucleus (VPM) or ventral division of the medial geniculate body (MGBv) resulted in two distinct classes of responses. The response of all layer 4 cells and a minority of layers 2/3 cells to thalamic stimulation was Class 1, including paired-pulse depression, all-or-none responses, and the absence of a metabotropic component. On the other hand, the majority of neurons in layers 2/3 showed a markedly different, Class 2 response to thalamic stimulation: paired-pulse facilitation, graded responses, and a metabotropic component. The Class 1 and Class 2 response characteristics have been previously seen in inputs to thalamus and have been described as drivers and modulators, respectively. Driver input constitutes a main information bearing pathway and determines the receptive field properties of the postsynaptic neuron, whereas modulator input influences the response properties of the postsynaptic neuron but is not a primary information bearing input. Because these thalamocortical projections have comparable properties to the drivers and modulators in thalamus, we suggest that a driver/modulator distinction may also apply to thalamocortical projections. In addition, our data suggest that thalamus is likely to be more than just a simple relay of information and may be directly modulating cortex.

SUBMITTER: Viaene AN

PROVIDER: S-EPMC3023380 | biostudies-literature | 2011 Jan

REPOSITORIES: biostudies-literature

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Synaptic properties of thalamic input to layers 2/3 and 4 of primary somatosensory and auditory cortices.

Viaene Angela N AN Petrof Iraklis I Sherman S Murray SM

Journal of neurophysiology 20101103 1

We studied the synaptic profile of thalamic inputs to cells in layers 2/3 and 4 of primary somatosensory (S1) and auditory (A1) cortices using thalamocortical slices from mice age postnatal days 10-18. Stimulation of the ventral posterior medial nucleus (VPM) or ventral division of the medial geniculate body (MGBv) resulted in two distinct classes of responses. The response of all layer 4 cells and a minority of layers 2/3 cells to thalamic stimulation was Class 1, including paired-pulse depress ...[more]

PMID: 21047937

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Project description:Rodents move rhythmically their facial whiskers and compute differences between signals predicted and those resulting from the movement to infer information about objects near their head. These computations are carried out by a large network of forebrain structures that includes the thalamus and the primary somatosensory (S1BF) and motor (M1wk) cortices. Spatially and temporally precise mechanorreceptive whisker information reaches the S1BF cortex via the ventroposterior medial thalamic nucleus (VPM). Other whisker-related information may reach both M1wk and S1BF via the axons from the posterior thalamic nucleus (Po). However, Po axons may convey, in addition to direct sensory signals, the dynamic output of computations between whisker signals and descending motor commands. It has been proposed that this input may be relevant for adjusting cortical responses to predicted vs. unpredicted whisker signals, but the effects of Po input on M1wk and S1BF function have not been directly tested or compared in vivo. Here, using electrophysiology, optogenetics and pharmacological tools, we compared in adult rats M1wk and S1BF in vivo responses in the whisker areas of the motor and primary somatosensory cortices to passive multi-whisker deflection, their dependence on Po activity, and their changes after a brief intense activation of Po axons. We report that the latencies of the first component of tactile-evoked local field potentials in M1wk and S1BF are similar. The evoked potentials decrease markedly in M1wk, but not in S1BF, by injection in Po of the GABAA agonist muscimol. A brief high-frequency electrical stimulation of Po decreases the responsivity of M1wk and S1BF cells to subsequent whisker stimulation. This effect is prevented by the local application of omega-agatoxin, suggesting that it may in part depend on GABA release by fast-spiking parvalbumin (PV)-expressing cortical interneurons. Local optogenetic activation of Po synapses in different cortical layers also diminishes M1wk and S1BF responses. This effect is most pronounced in the superficial layers of both areas, known to be the main source and target of their reciprocal cortico-cortical connections.

Project description:The traditional classification of primary motor cortex (M1) as an agranular area has been challenged recently when a functional layer 4 (L4) was reported in M1. L4 is the principal target for thalamic input in sensory areas, which raises the question of how thalamocortical synapses formed in M1 in the mouse compare with those in neighboring sensory cortex (S1). We identified thalamic boutons by their immunoreactivity for the vesicular glutamate transporter 2 (VGluT2) and performed unbiased disector counts from electron micrographs. We discovered that the thalamus contributed proportionately only half as many synapses to the local circuitry of L4 in M1 compared with S1. Furthermore, thalamic boutons in M1 targeted spiny dendrites exclusively, whereas ∼9% of synapses were formed with dendrites of smooth neurons in S1. VGluT2+ boutons in M1 were smaller and formed fewer synapses per bouton on average (1.3 vs 2.1) than those in S1, but VGluT2+ synapses in M1 were larger than in S1 (median postsynaptic density areas of 0.064 μm2 vs 0.042 μm2). In M1 and S1, thalamic synapses formed only a small fraction (12.1% and 17.2%, respectively) of all of the asymmetric synapses in L4. The functional role of the thalamic input to L4 in M1 has largely been neglected, but our data suggest that, as in S1, the thalamic input is amplified by the recurrent excitatory connections of the L4 circuits. The lack of direct thalamic input to inhibitory neurons in M1 may indicate temporal differences in the inhibitory gating in L4 of M1 versus S1.SIGNIFICANCE STATEMENT Classical interpretations of the function of primary motor cortex (M1) emphasize its lack of the granular layer 4 (L4) typical of sensory cortices. However, we show here that, like sensory cortex (S1), mouse M1 also has the canonical circuit motif of a core thalamic input to the middle cortical layer and that thalamocortical synapses form a small fraction (M1: 12%; S1: 17%) of all asymmetric synapses in L4 of both areas. Amplification of thalamic input by recurrent local circuits is thus likely to be a significant mechanism in both areas. Unlike M1, where thalamocortical boutons typically form a single synapse, thalamocortical boutons in S1 usually formed multiple synapses, which means they can be identified with high probability in the electron microscope without specific labeling.

Dataset Information

Synaptic properties of thalamic input to layers 2/3 and 4 of primary somatosensory and auditory cortices.

Publications

Synaptic properties of thalamic input to layers 2/3 and 4 of primary somatosensory and auditory cortices.

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