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

Abstract

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.

Selective, State-Dependent Activation of Somatostatin-Expressing Inhibitory Interneurons in Mouse Neocortex

“…Thus they seem to be ideal for responding to sudden, brief changes in cortical activity such as incoming sensory information (Simons 1978;Simons and Carvell 1989;Swadlow and Gusev 2000;Swadlow et al 1998), but not to slow changes in ongoing activity. In this respect, they act as a sort of filter of incoming excitatory activity, faithfully transmitting abrupt increases in input, but not persistent firing (Abbott and Regehr 2004).…”

“…Inhibition plays important roles in the feedforward control of sensory information (Cruikshank et al 2007;Simons 1978;Simons and Carvell 1989 ;Swadlow and Gusev 2000;Swadlow et al 1998), the overall control of cortical tone (ChagnacAmitai and Connors 1989), the generation of oscillatory activity at a range of frequencies (Beierlein et al 2000;Blatow et al 2003;Whittington et al 1995), and synchronization of spiking in excitatory pyramidal neurons (Cobb et al 1995;Long et al 2005). However, it has been very difficult to assign particular cortical functions to specific interneuron types.…”

Functional Properties of Electrical Synapses Between Inhibitory Interneurons of Neocortical Layer 4

“…At least one type of inhibitory interneuron in layer 4 has been observed to fire together in precise synchrony in vivo (Swadlow et al 1998), and it is likely that electrical synapses play a role in this synchrony. Among the variety of inhibitory interneuron subtypes in neocortex (Cauli et al 2000;Gupta et al 2000;Kawaguchi and Kubota 1997;Thomson and Deuchars 1997), we focus here on 2: fast-spiking (FS) and low threshold-spiking (LTS) cells.…”

Diverse Types of Interneurons Generate Thalamus-Evoked Feedforward Inhibition in the Mouse Barrel Cortex

“…Although the thalamocortical input to the neocortex is purely excitatory (glutamatergic), as determined by electrophysiological, electron microscopic, and immunocytochemical evidence (White, 1978;Ferster and Lindstrom, 1983;Agmon and Connors, 1992;Kharazia and Weinberg, 1993), inhibitory (GABAergic) mechanisms are recruited from the very first stage of intracortical processing. Indeed, electrical stimulation of thalamocortical afferents in vivo (Ferster and Lindstrom, 1983;Swadlow, 1989Swadlow, , 1990 or in vitro (Agmon and Connors, 1992;Gil and Amitai, 1996), as well as controlled sensory stimulation (Simons and Carvell, 1989;Simons, 1995;Brumberg et al, 1996;Swadlow et al, 1998;Zhu and Connors, 1999), result in a brief excitation of neocortical neurons, immediately followed by a pronounced inhibitory response mediated by intracortical inhibitory interneurons. The short latency of the inhibitory response indicates that the inhibitory interneurons eliciting it must be excited directly by the thalamocortical afferents, consistent with anatomical data (White, 1978;Fairén and Valverde, 1979;Freund et al, 1985;Keller and White, 1987), and in turn inhibit other cortical neurons disynaptically.…”