Cell Type–Specific Thalamic Innervation in a Column of Rat Vibrissal Cortex

Meyer, Hans Jonas; Wimmer, Verena C.; Hemberger, Mike; Bruno, Randy M.; Kock, De; Frick, Andreas; Sakmann, Bert; Helmstaedter, Moritz

doi:10.1093/cercor/bhq069

Cited by 191 publications

(235 citation statements)

References 93 publications

(160 reference statements)

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“…Our most recent estimates indicate that there are only an average of between 100 and 300 thalamic synapses per SS cell (Peters and Payne, 1993;Ahmed et al, 1994;Anderson et al, 1994;Binzegger et al, 2004). This contrasts with the rat barrel cortex, where the thalamic axons (Boudreau and Ferster, 2005;Banitt et al, 2007) are estimated to form ϳ600 synapses with their targets (Bruno and Sakmann, 2006; but see Meyer et al, 2010).…”

Section: Introductionmentioning

confidence: 81%

“…The number of thalamocortical synapses per neuron is also small for the primate visual cortex:18 -188 synapses (Peters et al, 1994;Latawiec et al, 2000). By contrast Bruno and Sakmann (2006) estimated that there were ϳ600 synapses per neuron in the rat barrel cortex, although they have since revised this number down to ϳ90 -580 synapses per layer 4 neuron (Meyer et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

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How Thalamus Connects to Spiny Stellate Cells in the Cat's Visual Cortex

Costa¹,

Martin²

2011

J. Neurosci.

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In the cat's visual cortex, the responses of simple cells seem to be totally determined by their thalamic input, yet only a few percent of the excitatory synapses in layer 4 arise from the thalamus. To resolve this discrepancy between structure and function, we used correlated light and electron microscopy to search individual spiny stellate cells (simple cells) for possible structural features that would explain the biophysical efficacy of the thalamic input, such as synaptic location on dendrites, size of postsynaptic densities, and postsynaptic targets. We find that thalamic axons form a small number of synapses with the spiny stellates (188 on average), that the median size of the synapses is slightly larger than that of other synapses on the dendrites of spiny stellates, that they are not located particularly proximal to the soma, and that they do not cluster on the dendrites. These findings point to alternative mechanisms, such as synchronous activation of the sparse thalamic synapses to boost the efficacy of the thalamic input. The results also support the idea that the thalamic input does not by itself determine the cortical response of spiny stellate cells, allowing the cortical microcircuit to amplify and modulate its response according to the particular context and computation being performed.

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Section: Introductionmentioning

confidence: 81%

Section: Discussionmentioning

confidence: 99%

How Thalamus Connects to Spiny Stellate Cells in the Cat's Visual Cortex

Costa¹,

Martin²

2011

J. Neurosci.

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“…An important proviso is that we recorded the location of cell bodies, and because most of these were pyramidal cells (the most common excitatory cell type in cortex; ref 23) with apical dendrites spanning many layers dorsally, the actual laminar location of the synaptic input cannot be specified. Indeed, on the basis of anatomical studies, all excitatory neurons in layers 2-6 of S1 potentially receive synaptic inputs from POm (7,24).…”

Section: Discussionmentioning

confidence: 99%

“…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)(4)(5)(6)(7)(8).…”

mentioning

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.

147

133

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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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“…Importantly, experience-dependent plasticity in S1 is poorly affected in layer 5 after removal of supragranular layers (Huang et al, 1998). These data, together with the observation of the discrepancy of MD-driven ocular preference shift between AP responses of 2/3Ps and PSP responses of 5TPs, should prompt future studies to study whether 5TPs receive in vivo prominent visual inputs from thalamus (Ferster and Lindström, 1983;Martin and Whitteridge, 1984;Weyand et al, 1986; see also Meyer et al, 2010) in S1. One could speculate that these synapses could be relatively refractory to undergo experiencedependent depression.…”

Section: Can L5 Be Driven By L2/3 (After Md)?mentioning

confidence: 95%

Layer- and Cell-Type-Specific Subthreshold and Suprathreshold Effects of Long-Term Monocular Deprivation in Rat Visual Cortex

Medini¹

2011

J. Neurosci.

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Connectivity and dendritic properties are determinants of plasticity that are layer and cell-type specific in the neocortex. However, the impact of experience-dependent plasticity at the level of synaptic inputs and spike outputs remains unclear along vertical cortical microcircuits. Here I compared subthreshold and suprathreshold sensitivity to prolonged monocular deprivation (MD) in rat binocular visual cortex in layer 4 and layer 2/3 pyramids (4Ps and 2/3Ps) and in thick-tufted and nontufted layer 5 pyramids (5TPs and 5NPs), which innervate different extracortical targets. In normal rats, 5TPs and 2/3Ps are the most binocular in terms of synaptic inputs, and 5NPs are the least. Spike responses of all 5TPs were highly binocular, whereas those of 2/3Ps were dominated by either the contralateral or ipsilateral eye. MD dramatically shifted the ocular preference of 2/3Ps and 4Ps, mostly by depressing deprived-eye inputs. Plasticity was profoundly different in layer 5. The subthreshold ocular preference shift was sevenfold smaller in 5TPs because of smaller depression of deprived inputs combined with a generalized loss of responsiveness, and was undetectable in 5NPs. Despite their modest ocular dominance change, spike responses of 5TPs consistently lost their typically high binocularity during MD. The comparison of MD effects on 2/3Ps and 5TPs, the main affected output cells of vertical microcircuits, indicated that subthreshold plasticity is not uniquely determined by the initial degree of input binocularity. The data raise the question of whether 5TPs are driven solely by 2/3Ps during MD. The different suprathreshold plasticity of the two cell populations could underlie distinct functional deficits in amblyopia.

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Cell Type–Specific Thalamic Innervation in a Column of Rat Vibrissal Cortex

Cited by 191 publications

References 93 publications

How Thalamus Connects to Spiny Stellate Cells in the Cat's Visual Cortex

How Thalamus Connects to Spiny Stellate Cells in the Cat's Visual Cortex

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

Layer- and Cell-Type-Specific Subthreshold and Suprathreshold Effects of Long-Term Monocular Deprivation in Rat Visual Cortex

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