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. 2005 Aug 3;25(31):7179-90.
doi: 10.1523/JNEUROSCI.1445-05.2005.

Short-term depression in thalamocortical synapses of cat primary visual cortex

C Elizabeth Boudreau  1 , David Ferster
Affiliations

Short-term depression in thalamocortical synapses of cat primary visual cortex

C Elizabeth Boudreau et al. J Neurosci. .

Abstract

Neurons in primary visual cortex exhibit several nonlinearities in their responses to visual stimuli, including response decrements to repeated stimuli, contrast-dependent phase advance, contrast saturation, and cross-orientation suppression. Thalamocortical synaptic depression has been implicated in these phenomena but has not been examined directly in visual cortex in vivo. We assessed depression of visual thalamocortical synapses in vivo using 20-100 Hz trains of electrical stimuli delivered to the LGN. Cortical cells receiving direct input from the LGN, identified by short latency and low jitter of LGN-evoked PSPs, showed moderate reductions in PSP amplitude during the fastest trains. Cells receiving indirect input from the thalamus via other cortical excitatory neurons show a marked reduction in PSP amplitude during a train, which could be explained either by synaptic depression in corticocortical synapses or by an inhibition-mediated suppression of the firing of their afferents. Reducing spontaneous activity in the LGN (by retinal blockade) unmasked additional depression at the thalamocortical synapse but only for the first stimulus in the train. That is, the first PSP was increased in amplitude relative to the unblocked condition, but subsequent responses were essentially unchanged. Thus, the synapses are maintained at significant levels of depression by spontaneous activity. These findings constrain the role that thalamocortical depression can play in shaping cortical responses to visual stimuli.

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Figures

Figure 1.
Figure 1.
Goodness-of-fit of linear conductance model. A, The average measured voltage response (solid lines) and the linear prediction of average voltage response based on our conductance estimates (dotted lines) are shown for each level of current injection in an example cell. B, Predicted and measured Vm, binned at a resolution of 1 ms, are plotted against one another for each point in time and each injected current (n = 39,150). Resting potential for this cell was -55.4 mV (vertical line). The model accounted for 78% of the variance in the data. C, D, As in A and B, for an example cell for which the linear prediction accounted for 97% of the variance in the data set (resting potential of -54.5 mV, vertical line; n = 13,920).
Figure 2.
Figure 2.
Responses to repeated LGN stimulation. A, Top trace, Voltage response of a cortical cell that received monosynaptic input from the LGN to a five impulse, 50 Hz train of electrical stimuli. Bottom trace, Same traces, with slow trends removed as described in Materials and Methods. Average of 16 trials. LGN stimulus amplitude of 200 μA. Resting potential of -60 mV. B, PSPs from A, bottom trace, aligned on the LGN stimulus. The thick trace is the first PSP. C, As in A, for a cell that received only polysynaptic input from the LGN. Average of 16 trials. LGN stimulus amplitude of 225 μA. Resting potential of -71 mV. D, Superimposed responses to individual stimuli, aligned on the LGN stimulus. E, PSP amplitude as a function of stimulus position in the train. Filled symbols, Data for the monosynaptic cell in A and B; open symbols, data for the polysynaptic cell in C and D. Error bars are SE. F, Diagram showing the connectivity of monosynaptic and polysynaptic neurons. Both cell types are thought to receive input from cortical inhibitory interneurons. Monosynaptic cells receive substantial excitatory input from the LGN, whereas polysynaptic cells receive little direct thalamic input and are primarily driven by excitatory input from other cortical cells.
Figure 3.
Figure 3.
Relationship between latency and PSP decrement. A, At all frequencies tested, there was a significant negative correlation between PSP latency and paired-pulse ratio. Dashed lines show our criteria for putative monosynaptic and polysynaptic neurons. Cells tested at more than one frequency are represented more than once. B, Histogram of the latency of the first PSP for all 70 cells tested. Latency was determined from the response to the first stimulus at all frequencies combined. Dashed lines show the same criteria as those in A.
Figure 4.
Figure 4.
Effects of stimulus frequency on PSP decrement. A, Responses of a second putative monosynaptic cell to stimulation at 20, 50, and 100 Hz (resting potential of -75.5 mV; average of 16 trials). B, C, Normalized PSP size as a function of stimulus number for two classes of cells defined by our criteria. D, Normalized PSP size as a function of stimulus number averaged across cells for 20, 50, and 100 Hz. Filled symbols, Monosynaptic neurons; open symbols, polysynaptic neurons (20 Hz, n = 24 monosynaptic, n = 5 polysynaptic; 50 Hz, n = 30 monosynaptic, n = 15 polysynaptic; 100 Hz, n = 23 monosynaptic, n = 5 polysynaptic). Error bars are SE.
Figure 5.
Figure 5.
Response to repeated LGN stimulation after a single shock to the cortex. A, Response of a monosynaptic cell to LGN stimulation alone (black) and LGN and cortical stimulation together (gray); resting potential of -72 mV. The relative timing of the stimuli is shown above the traces. Traces show the average of 16 trials. The cortical shock amplitude was 200 μA. B, Superimposed response to the LGN stimuli, with slow trends removed. The thick trace shows the first LGN-evoked response; thinner traces show subsequent responses. As in A, gray and black traces were collected with and without preceding cortical stimulation. D, E, Same as A and B for a polysynaptic cell, average of nine trials; resting potential of -61 mV. The cortical shock amplitude was 200 μA. C, F, Amplitude of the LGN-evoked response as a function of stimulus position in the train with cortical stimulation (gray plots) or without (black plots). Filled symbols, Monosynaptic cell; open symbols, polysynaptic cell. Ctx, Cortex.
Figure 6.
Figure 6.
Effects of cortical stimulation on the responses to rapid LGN stimulation averaged over the sample. A, Average amplitude of LGN responses of monosynaptic cells (filled symbols) and polysynaptic cells (open symbols) at 20, 50, and 100 Hz with preceding cortical stimulation (gray) and without (black). B, Comparison of effects of preceding shocks. The schematic shows which PSPs are being compared in the graphs below. Gray symbols compare the response to an LGN shock given 20 ms after cortical stimulation with the response to the LGN shock alone. Black symbols compare the response to the second stimulus in a 50 Hz LGN train (with no cortical stimulation) to the response to the first LGN shock in the train. Top, Monosynaptic cells; there was a good correlation for both sets of points. Bottom, Polysynaptic cells; there was no correlation for either set of points in the polysynaptic data. Ctx, Cortex.
Figure 7.
Figure 7.
Conductance measurements. A, Voltage response (gray) and estimated total conductance (black) evoked in a monosynaptic cell by 50 Hz stimulation of the LGN (average of 30 trials). Time 0 is the time of the first LGN stimulus. Conductance was calculated in 1 ms bins. B, Top, Excitatory and inhibitory components of conductance change for the cell in A. Shaded 95% confidence intervals were calculated from 1000 repetitions of a nonparametric bootstrap analysis but are barely visible on the excitatory traces because they are only slightly thicker than the trace itself. Bottom, Superimposed conductance changes associated with each LGN-evoked response, with the first response shown as a thick trace. D, E, As in A and B for a polysynaptic cell, average of 30 trials. E, F, Relative size of the conductance changes after each LGN stimulus, normalized to the size of the conductance change after the first stimulus. Green, Excitatory conductance changes; red, inhibitory conductance changes; filled symbols, monosynaptic (mono) cell; open symbols, polysynaptic (poly) cell.
Figure 8.
Figure 8.
LGN-evoked excitatory and inhibitory conductance for the sample. A, The size of the conductance change after each LGN stimulus in a 50 Hz train is shown, normalized to the size of the first response, for monosynaptic cells (green, excitatory; red, inhibitory).B, As in A, but for polysynaptic cells. C, Averages of the data in A and B. Filled symbols, Monosynaptic (mono) cells; open symbols, polysynaptic (poly) cells. Error bars are SE.
Figure 9.
Figure 9.
Effects of LGN activity reduction on response to LGN stimulation. A, Spontaneous activity in single-unit LGN recordings before, during, and after a period of increased intraocular pressure (80-150 mmHg for 5 s; gray shaded region). B, Spontaneous activity in single-unit LGN recordings showing full recovery after increased IOP (150-200 mmHg) for 30 s. Dashed line shows time at which normalized firing rate is no longer significantly different from initial firing rate. Mean firing rate before inactivation was 8.8 ± 1.3 spikes/s and after inactivation was 10.1 ± 3.0 spikes/s. C, Response to 50 Hz train of LGN stimuli in a monosynaptic neuron with LGN activity reduction (gray) and without (black); resting potential of -73 mV. Average of 80 traces. D, Data in C, with slow trends subtracted and aligned on LGN stimulus. Thick traces show first PSPs, and thin traces show subsequent PSPs. E, Average PSP size as a function of position in the stimulus train for the cell in C and D for control condition (black) and reduced LGN activity (gray). Error bars are SE. F, Average PSP size for our sample of monosynaptic cells, normalized to the size of the first PSP in the control condition. Error bars are SE. Dotted gray line shows predictions from in vitro experiments (Stratford et al., 1996; Kayser et al., 2001); for details, see Discussion.
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