Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex

Abstract

We used a thalamocortical slice preparation to record both spike trains and synaptically evoked responses from neurons of mouse barrel cortex. Cells were classified as regular spiking (RS), intrinsically bursting (IB), or fast spiking (FS) according to their temporal firing patterns when injected with current. RS cells were further separated into two subtypes, RS1 and RS2 cells, the latter encountered only in the infragranular layers. Synaptic responses were elicited by focal electrical stimuli in the ventrobasal nucleus of the thalamus (VB) while holding the cells at different membrane potentials. Postsynaptic potentials were classified as excitatory (EPSPs) or inhibitory (IPSPs), and their latencies were measured from the onset of the extracellularly recorded fiber volley in layer IV. EPSPs fell into three groups, according to latency. Those in the early cluster had latencies shorter than 1 msec and were coincident with the postsynaptic layer IV population response; they were considered monosynaptic. A second group, with latencies between 1.3 and 2.5 msec, were coincident with all IPSPs and were classified as disynaptic. The rest had latencies longer than 5 msec and were considered polysynaptic. The synaptic order of a cell was correlated with its laminar position and its electrophysiological class. Specifically, monosynaptic responses were restricted to infragranular RS cells and to FS cells, while disynaptic EPSPs were found in supragranular RS cells and in IB cells. Disynaptic IPSPs were found in both deep and superficial layers; in the deep layers they nearly always followed monosynaptic EPSPs, while in the superficial layers they were mostly found in isolation. We conclude that the intrinsic spiking characteristics of a neuron are an important determinant of its position in the cortical circuit and may have a substantial role in determining its response properties.

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

“…3C, middle and bottom traces) indicated that it received a thalamocortical input nearly coincident with the monosynaptic field potential. This coincidence, and the negligible sweep-tosweep variability in the onset of the whole-cell responses (note superimposed traces), indicate that these were monosynaptic EPSCs (Agmon and Connors, 1992;Agmon et al, 1996). This neuron discharged a single spike (Fig.…”

“…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.…”

Imaging synaptic inhibition in transgenic mice expressing the chloride indicator, Clomeleon

“…These recordings (Fig. 3b) revealed the two known types of layer 5 pyramidal neurons, bursting and regular firing (Agmon and Connors, 1992). Clomeleon-expressing neurons exhibited normal electrophysiological properties when compared to neurons from wildtype mice at P20 (Table 2, ANOVA, p > 0.05), suggesting that they were not compromised by long-term expression of Clomeleon.…”

“…Membrane potential recordings were corrected for the liquid junction potential (14 mV). Parameters for wild type tissue were taken from (Pérez-Garci et al, 2006) and (Agmon and Connors, 1992).…”

Mechanical resonance enhances the sensitivity of the vibrissa sensory system to near-threshold stimuli

“…There are drawbacks to MUA-this measure does not, for example, allow isolation of responses to specific cell types (Agmon and Connors 1992;Bruno and Simons 2002;Andermann et al 2004). That said, our use of MUA in SI facilitated obtaining consistent and high signal-to-noise responses across a large number of conditions (231), and is often employed in auditory studies that apply dense and broad stimulus sampling (Eggermont, 1999;Schreiner and Sutter, 1992).…”