Sharp, Local Synchrony Among Putative Feed-Forward Inhibitory Interneurons of Rabbit Somatosensory Cortex

Abstract

Swadlow, Harvey A., Irina N. Beloozerova, and Mikhail G. Sirota. Sharp, local synchrony among putative feed-forward inhibitory interneurons of rabbit somatosensory cortex. J. Neurophysiol. 79: 567–582, 1998. Many suspected inhibitory interneurons (SINs) of primary somatosensory cortex (S1) receive a potent monosynaptic thalamic input (thalamocortical SINs, SINstc). It has been proposed that nearly all such SINstc of a S1 barrel column (BC) receive excitatory synaptic input from each member of a subpopulation of neurons within the topographically aligned ventrobasal (VB) thalamic barreloid. Such a divergent and convergent network leads to several testable predictions: sharply synchronous activity should occur between SINstc of a BC, sharp synchrony should not occur between SINstc of neighboring BCs, and sharp synchrony should not occur between SINs or other neurons of the same BC that do not receive potent monosynaptic thalamic input. These predictions were tested by cross-correlating the activity of SINstc of the same and neighboring BCs. Correlations among descending corticofugal neurons of layer 5 (CF-5 neurons, identified by antidromic activation) and other neurons that receive little or no monosynaptic VB input also were examined. SINs were identified by a high-frequency (>600 Hz) burst of three or more spikes elicited by VB stimulation and had action potentials of short duration. SINstc were further differentiated by short synaptic latencies to electrical stimulation of VB thalamus (<1.7 ms) and to peripheral stimulation (<7.5 ms). The above predictions were confirmed fully. 1) Sharp synchrony (±1 ms) was seen between all SINstc recorded within the same BC (a mean of 4.26% of the spikes of each SINtc were synchronized sharply with the spikes of the paired SINtc). Sharp synchrony was not dependent on peripheral stimulation, was not oscillatory, and survived general anesthesia. Sharp synchrony was superimposed on a broader synchrony, with a time course of tens of milliseconds. 2) Little or no sharp synchrony was seen when CF-5 neurons were paired with SINstc or other neurons of the same BC. 3) Little or no sharp synchrony was seen when SINstc were paired with other SINstc located in neighboring BCs. Intracellular recordings obtained from three SINs in the fully awake state supported the assertion that SINs are GABAergic interneurons. Each of these cells met our extracellular criteria for identification as a SIN, each had a spike of short duration (0.4–0.5 ms), and each responded to a depolarizing current pulse with a nonadapting train of action potentials. These results support the proposed network linking VB barreloid neurons with SINstc within the topographically aligned BC. We suggest that sharp synchrony among SINstc results in highly synchronous inhibitory postsynpatic potentials (IPSPs)in the target neurons of these cells and that these summated IPSPs may be especially effective when excitatory drive to target cells is weak and asynchronous.