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Functional Connectivity in Layer IV Local Excitatory Circuits of Rat Somatosensory Cortex

¹Institute of Neuroinformatics, University of Zürich and Federal Institute of Technology (Eidgenössische Technische Hochschule), CH-8057 Zürich, Switzerland; ²Division of Neuroscience, John Curtin School of Medical Research, Canberra, ACT 0200; and ³Australian National University Medical School, Canberra, ACT 0200, Australia

Submitted 24 December 2003; accepted in final form 10 June 2004

There are two types of excitatory neurons within layer IV of rat somatosensory cortex: star pyramidal (SP) and spiny stellate cells (SS). We examined the intrinsic properties and connectivity between these neurons to determine differences in function. Eighty-four whole cell recordings of pairs of neurons were examined in slices of rat barrel cortex at 36 ± 1°C. Only minimal differences in intrinsic properties were found; however, differences in synaptic strength could clearly be shown. Connections between homonymous pairs (SS–SS or SP–SP) had a higher efficacy than heteronymous connections. This difference was mainly a result of quantal content. In 42 pairs, synaptic dynamics were examined. Sequences of action potentials (3–20 Hz) in the presynaptic neuron consistently caused synaptic depression (₂/₁ = 0.53 ± 0.18). The dominant component of depression was release-independent; this depression occurred even when preceding action potentials had failed to cause a response. The release-dependence of depression was target specific; in addition, release-independence was greater for postsynaptic SPs. In a subset of connections formed only between SP and any other cell type (43%), synaptic efficacy was dependent on the presynaptic membrane potential (V_m); at –55 mV, the connections were almost silent, whereas at –85 mV, transmission was very reliable. We suggest that, within layer IV, there is stronger efficacy between homonymous than between heteronymous excitatory connections. Under dynamic conditions, the functional connectivity is shaped by synaptic efficacy at individual connections, by V_m, and by the specificity in the types of synaptic depression.

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