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. 2002 Jul 15;542(Pt 2):599-617.
doi: 10.1113/jphysiol.2001.012759.

Frequency-selective augmenting responses by short-term synaptic depression in cat neocortex

Arthur R Houweling  1 , Maxim Bazhenov, Igor Timofeev, François Grenier, Mircea Steriade, Terrence J Sejnowski
Affiliations

Frequency-selective augmenting responses by short-term synaptic depression in cat neocortex

Arthur R Houweling et al. J Physiol. .

Abstract

Thalamic stimulation at frequencies between 5 and 15 Hz elicits incremental or 'augmenting' cortical responses. Augmenting responses can also be evoked in cortical slices and isolated cortical slabs in vivo. Here we show that a realistic network model of cortical pyramidal cells and interneurones including short-term plasticity of inhibitory and excitatory synapses replicates the main features of augmenting responses as obtained in isolated slabs in vivo. Repetitive stimulation of synaptic inputs at frequencies around 10 Hz produced postsynaptic potentials that grew in size and carried an increasing number of action potentials resulting from the depression of inhibitory synaptic currents. Frequency selectivity was obtained through the relatively weak depression of inhibitory synapses at low frequencies, and strong depression of excitatory synapses together with activation of a calcium-activated potassium current at high frequencies. This network resonance is a consequence of short-term synaptic plasticity in a network of neurones without intrinsic resonances. These results suggest that short-term plasticity of cortical synapses could shape the dynamics of synchronized oscillations in the brain.

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Figures

Figure 1
Figure 1
Cortical network models A, responses of a model PY cell (top) and IN cell (bottom) to a 0.1 nA current injection. B, excitatory and inhibitory PSPs resulting from activation of AMPA and GABAA receptors. C, schematic representation of the reduced model. D, schematic representation of the full network model.
Figure 8
Figure 8
Parameter dependence of incremental responses in the cortical network model Frequency dependence of average response increment (RI). For each panel a different parameter was varied: maximal conductance of IN-PY synapses (A), PY-IN synapses (B), extrinsic afferent synapses onto IN cells (C), and PY-PY synapses (D); time constants of IN-PY synapses (E), PY-IN synapses (F), extrinsic afferent synapses (G), and PY-PY synapses (slow component) (H); peak conductance of IK(Ca) in PY cells (I); intensity of stimulation in the grey matter (J) and in the white matter (K); and time constants of IN-PY and PY-PY synapses (single depression component, U = 0.3) (L). Parameter values are indicated on the graphs. The thick curve corresponds to the original set of parameters and is the same in all panels.
Figure 2
Figure 2
Augmenting responses in the intact brain and the isolated neocortical slab A, dual intracellular recordings from cortical area 4 and thalamic VL nucleus, together with field potentials from the depth of area 4. Stimulation consisted of a pulse-train at 10 Hz. Augmenting responses were elicited by thalamic VL stimulation (left) or area 4 stimulation (right) in the intact thalamocorticothalamic network. B, intracortical augmenting responses in the slab. Left, a single stimulus (0.15 mA) to the slab elicited a depolarizing response. Middle, a 10 Hz pulse-train resulted in augmenting responses. Right, 15 stimuli at 40 Hz resulted in temporal summation at the beginning of the pulse-train and depression of PSPs close to the end of the train. C, the first and the last responses to 10 Hz stimuli (left) and 40 Hz stimuli (right) from B are superimposed and expanded in time and amplitude.
Figure 3
Figure 3
Dependence of intracortical augmenting responses on intensity of stimulation and distance from stimulating electrode Simultaneous dual intracellular recordings from an acutely isolated neocortical slab. Cell 1 was located in the vicinity (< 0.5 mm) of the stimulating electrode. Cell 2 was recorded 2 mm anterior to the stimulating electrode. A, low-intensity stimulation (0.05 mA) elicited decremental responses in cell 1 and no response in cell 2. B, a slightly higher intensity of stimulation (0.07 mA) resulted in almost equal responses in cell 1 but decremental responses in cell 2. C, higher intensity of stimulation (0.30 mA) produced augmenting responses in cell 1 and equal responses in cell 2.
Figure 4
Figure 4
Incremental responses in the network model with short-term plasticity of cortical synapses In this and subsequent colour figures the centre 81 (out of 121) cells were lined up along the vertical axis and activity was ‘imaged’ in time. Membrane potentials are colour-coded from dark blue (hyperpolarization) to red (depolarization). Action potentials are indicated by black dots. A, responses of PY cells in the network with fixed synapses were similar for shocks at 10 Hz. B, responses of PY cells (top) and IN cells (bottom) in the network with short-term synaptic plasticity were progressively enhanced during the first few shocks at 10 Hz. C, responses of PY cells were not incremental when the network was spontaneously active. D, incremental PY responses were reduced at high and low frequencies of stimulation. Top, PY cell responses to stimulation at 2 Hz (time between shocks is truncated). Bottom, PY cell responses to stimulation at 30 Hz. The time scale is identical for all plots. E, left: average response increment (RI) as a function of stimulation frequency. Right, frequency dependence of the average increase in membrane depolarization of the centre 51 PY cells.
Figure 5
Figure 5
Incremental responses in individual PY cells in the cortical network model Left, membrane potentials for five cortical shocks at 10 Hz from site of stimulation (PY61) to periphery (PY25). Right, overlaid and expanded voltage traces for the first shock (thick line), and second and third shocks (thin lines).
Figure 6
Figure 6
Influence of stimulation intensity on incremental responses in the network model A, responses of PY cells in the network for five shocks at 10 Hz at increasing stimulation intensities (centre 65 cells are shown). B, voltage traces of a single PY cell (PY52) at the same stimulation intensities. Stimulation intensity was changed by scaling the peak conductances of the extrinsic afferents and the fraction of intrinsic synapses activated by the electrical stimulus from 10 % up to 200 %.
Figure 7
Figure 7
Dependence of transient incremental responses on the rate of depression of afferent excitatory synapses From top to bottom, responses at a stimulation frequency of 40 Hz in the network model for decreasing rates, r, of depression of extrinsic afferents (centre 65 cells are shown). The indicated parameter values resulted in a similar steady-state depression but different rates of convergence to steady state.
Figure 9
Figure 9
Incremental responses in the reduced model The reduced model consisted of a single PY-IN cell pair, an inhibitory IN-PY synapse and extrinsic afferent synapses (Fig. 1C). A, top: PY and IN cell responses to five shocks at 2 Hz (time between shocks is truncated) and 10 Hz, and ten shocks at 40 Hz. Synaptic conductance values were: g_ext-PY = 60 nS, g_ext-IN = 60 nS and g_IN-PY = 100 nS. Synaptic plasticity parameters were the same as in the full network model. All synapses were stimulated by the electrical stimulus. Bottom, synaptic conductance traces of the inhibitory and extrinsic afferent synapses onto the PY cell and the conductance of the calcium-activated potassium current in the PY cell. B, top: PY cell responses to five shocks at 2 Hz and 10 Hz, and ten shocks at 40 Hz when a self-excitatory synapse was included for the PY cell (g_PY-PY = 25 nS). Bottom, synaptic conductance trace of the self-excitatory PY-PY synapse. The time scale is identical for all plots.
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