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Intracortical circuits of pyramidal neurons reflect their long-range axonal targets.

Brown SP, Hestrin S - Nature (2009)

Bottom Line: We recorded simultaneously from up to four retrogradely labelled pyramidal neurons that projected to the superior colliculus, the contralateral striatum or the contralateral cortex to assess their synaptic connectivity.We first found that the frequency of monosynaptic connections among corticostriatal pyramidal neurons is significantly higher than among corticocortical or corticotectal pyramidal neurons.Moreover, we found that the average axodendritic overlap of the presynaptic and postsynaptic pyramidal neurons could not fully explain the differences in connection probability that we observed.

View Article: PubMed Central - PubMed

Affiliation: Department of Comparative Medicine, Stanford University School of Medicine, 300 Pasteur Drive, Edwards Building, R314, Stanford, California 94305-5342, USA.

ABSTRACT
Cortical columns generate separate streams of information that are distributed to numerous cortical and subcortical brain regions. We asked whether local intracortical circuits reflect these different processing streams by testing whether the intracortical connectivity among pyramidal neurons reflects their long-range axonal targets. We recorded simultaneously from up to four retrogradely labelled pyramidal neurons that projected to the superior colliculus, the contralateral striatum or the contralateral cortex to assess their synaptic connectivity. Here we show that the probability of synaptic connection depends on the functional identities of both the presynaptic and postsynaptic neurons. We first found that the frequency of monosynaptic connections among corticostriatal pyramidal neurons is significantly higher than among corticocortical or corticotectal pyramidal neurons. We then show that the probability of feed-forward connections from corticocortical neurons to corticotectal neurons is approximately three- to fourfold higher than the probability of monosynaptic connections among corticocortical or corticotectal cells. Moreover, we found that the average axodendritic overlap of the presynaptic and postsynaptic pyramidal neurons could not fully explain the differences in connection probability that we observed. The selective synaptic interactions we describe demonstrate that the organization of local networks of pyramidal cells reflects the long-range targets of both the presynaptic and postsynaptic neurons.

Show MeSH
Different frequencies of monosynaptic connections between corticotectal, corticostriatal or corticocortical neurons. Presynaptic action potentials elicit a synaptic response in a postsynaptic cell during simultaneous recordings from two monosynaptically-connected corticotectal neurons (a), corticostriatal neurons (b) and corticocortical neurons (c). d, The frequency of identified monosynaptic connections among connections tested is shown for corticotectal connections, corticostriatal connections and corticocortical connections; **P < 0.05.
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Figure 1: Different frequencies of monosynaptic connections between corticotectal, corticostriatal or corticocortical neurons. Presynaptic action potentials elicit a synaptic response in a postsynaptic cell during simultaneous recordings from two monosynaptically-connected corticotectal neurons (a), corticostriatal neurons (b) and corticocortical neurons (c). d, The frequency of identified monosynaptic connections among connections tested is shown for corticotectal connections, corticostriatal connections and corticocortical connections; **P < 0.05.

Mentions: To assay the synaptic connectivity among pyramids projecting to the same long-range target, we recorded simultaneously from multiple fluorescently-labelled neurons using whole-cell patch clamp techniques. Action potentials were generated with brief current injections in each neuron in turn while recording the synaptic responses in the other neurons. In synaptically connected cells, these presynaptic action potentials elicited monosynaptic unitary excitatory postsynaptic potentials (EPSPs) in the postsynaptic partner. Monosynaptic connections were identified between neurons for all three cell types (Fig. 1a–c). The synaptic properties including the mean amplitudes and the paired-pulse ratio were similar among the three types of connections (Supplementary Table 2).


Intracortical circuits of pyramidal neurons reflect their long-range axonal targets.

Brown SP, Hestrin S - Nature (2009)

Different frequencies of monosynaptic connections between corticotectal, corticostriatal or corticocortical neurons. Presynaptic action potentials elicit a synaptic response in a postsynaptic cell during simultaneous recordings from two monosynaptically-connected corticotectal neurons (a), corticostriatal neurons (b) and corticocortical neurons (c). d, The frequency of identified monosynaptic connections among connections tested is shown for corticotectal connections, corticostriatal connections and corticocortical connections; **P < 0.05.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2727746&req=5

Figure 1: Different frequencies of monosynaptic connections between corticotectal, corticostriatal or corticocortical neurons. Presynaptic action potentials elicit a synaptic response in a postsynaptic cell during simultaneous recordings from two monosynaptically-connected corticotectal neurons (a), corticostriatal neurons (b) and corticocortical neurons (c). d, The frequency of identified monosynaptic connections among connections tested is shown for corticotectal connections, corticostriatal connections and corticocortical connections; **P < 0.05.
Mentions: To assay the synaptic connectivity among pyramids projecting to the same long-range target, we recorded simultaneously from multiple fluorescently-labelled neurons using whole-cell patch clamp techniques. Action potentials were generated with brief current injections in each neuron in turn while recording the synaptic responses in the other neurons. In synaptically connected cells, these presynaptic action potentials elicited monosynaptic unitary excitatory postsynaptic potentials (EPSPs) in the postsynaptic partner. Monosynaptic connections were identified between neurons for all three cell types (Fig. 1a–c). The synaptic properties including the mean amplitudes and the paired-pulse ratio were similar among the three types of connections (Supplementary Table 2).

Bottom Line: We recorded simultaneously from up to four retrogradely labelled pyramidal neurons that projected to the superior colliculus, the contralateral striatum or the contralateral cortex to assess their synaptic connectivity.We first found that the frequency of monosynaptic connections among corticostriatal pyramidal neurons is significantly higher than among corticocortical or corticotectal pyramidal neurons.Moreover, we found that the average axodendritic overlap of the presynaptic and postsynaptic pyramidal neurons could not fully explain the differences in connection probability that we observed.

View Article: PubMed Central - PubMed

Affiliation: Department of Comparative Medicine, Stanford University School of Medicine, 300 Pasteur Drive, Edwards Building, R314, Stanford, California 94305-5342, USA.

ABSTRACT
Cortical columns generate separate streams of information that are distributed to numerous cortical and subcortical brain regions. We asked whether local intracortical circuits reflect these different processing streams by testing whether the intracortical connectivity among pyramidal neurons reflects their long-range axonal targets. We recorded simultaneously from up to four retrogradely labelled pyramidal neurons that projected to the superior colliculus, the contralateral striatum or the contralateral cortex to assess their synaptic connectivity. Here we show that the probability of synaptic connection depends on the functional identities of both the presynaptic and postsynaptic neurons. We first found that the frequency of monosynaptic connections among corticostriatal pyramidal neurons is significantly higher than among corticocortical or corticotectal pyramidal neurons. We then show that the probability of feed-forward connections from corticocortical neurons to corticotectal neurons is approximately three- to fourfold higher than the probability of monosynaptic connections among corticocortical or corticotectal cells. Moreover, we found that the average axodendritic overlap of the presynaptic and postsynaptic pyramidal neurons could not fully explain the differences in connection probability that we observed. The selective synaptic interactions we describe demonstrate that the organization of local networks of pyramidal cells reflects the long-range targets of both the presynaptic and postsynaptic neurons.

Show MeSH