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. 2004 Nov 24;24(47):10731-40.
doi: 10.1523/JNEUROSCI.3059-04.2004.

Encoding of Natural Scene Movies by Tonic and Burst Spikes in the Lateral Geniculate Nucleus

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Free PMC article

Encoding of Natural Scene Movies by Tonic and Burst Spikes in the Lateral Geniculate Nucleus

Nicholas A Lesica et al. J Neurosci. .
Free PMC article

Abstract

The role of the lateral geniculate nucleus (LGN) of the thalamus in visual encoding remains an open question. Here, we characterize the function of tonic and burst spikes in cat LGN X-cells in signaling features of natural stimuli. A significant increase in bursting was observed during natural stimulation (relative to white noise stimulation) and was linked to the strong correlation structure of the natural scene movies. Burst responses were triggered by specific stimulus events consisting of a prolonged inhibitory stimulus, followed by an excitatory stimulus, such as the movement of an object into the receptive field. LGN responses to natural scene movies were predicted using an integrate-and-fire (IF) framework and compared with experimentally observed responses. The standard IF model successfully predicted LGN responses to natural scene movies during tonic firing, indicating a linear relationship between stimulus and response. However, the IF model typically underpredicted the LGN response during periods of bursting, indicating a nonlinear amplification of the stimulus in the actual response. The addition of a burst mechanism to the IF model was necessary to accurately predict the entire LGN response. These results suggest that LGN bursts are an important part of the neural code, providing a nonlinear amplification of stimulus features that are typical of the natural environment.

Figures

Figure 5.
Figure 5.
IF predictions of the LGN response to natural scene movies. a, A block diagram of the LGN encoding model. The spatiotemporal natural scene movie is passed through the spatiotemporal RF (STRF) of the neuron, then through a light adaptation stage, and used to drive a stochastic IF or IFB spike generator. b, The predicted response to a single trial of a 500 msec segment of the natural scene movie stimulus from the IF model and IFB models for a typical cell. c, A raster plot of the predicted and actual responses to eight repeats of the 500 msec segment of the natural scene movie stimulus. d, A histogram of actual and predicted responses to the segment of natural scene movie averaged across eight repeats. The prediction from the IF model is shown in solid black, the prediction from the IFB model is shown in dashed black, and the actual response of the neuron is shown in gray. Intervals in the actual response at which a burst event occurred on two or more trials are indicated by asterisks. Spike times were collected into 7.8 msec bins.
Figure 6.
Figure 6.
The standard IF model underpredicts the LGN response during periods of bursting. a, A series of two-dimensional histograms comparing the actual and predicted LGN responses during burst and tonic firing intervals for a typical ON cell (averaged across 8 repeats). Dark areas indicate a large number of occurrences, and light areas indicate a small number of occurrences. Histograms were normalized so that the bin with the largest number of occurrences was shown in black. On each histogram, the equality line is shown. Histograms were calculated using responses to a different 48 sec segment of the natural scene movie from that used to optimize the model parameters. Burst intervals were defined as those intervals during which a burst occurred on at least two of eight trials. Tonic intervals were all other intervals that contained at least one spike on any of the eight trials. Intervals during which no spikes occurred on any of the eight trials were not included in the analysis. b, Scatter plots of the correlation coefficients (CC) between actual and predicted responses to natural scene movies during burst and tonic firing intervals for the sample of 18 LGN X-cells. Coefficients for the IF model are shown in the top plot, and coefficients for the IFB model are shown in the bottom plot. Error bars represent one SD of the distribution of correlation coefficients generated for each neuron, as described in Materials and Methods.
Figure 1.
Figure 1.
White noise and natural scene movie stimuli. The stimuli used in this study were spatiotemporal white noise and grayscale video recordings. a, Sample frames of the stimuli. The white noise (m-sequence) was displayed in a 16 × 16 grid. The natural scene movies were displayed in a 64 × 64 grid that covered the entire screen. The square on the first example frame of the movie indicates an example of the corresponding region of the screen that was covered by the white noise stimulus. The movies included a range of time-varying images, from a set of home video recordings taken in the forest (first example) to Hollywood movies (second example, from the movie Raiders of the Lost Ark). b, The temporal variations in the intensity of one pixel of the stimulus. The vertical scale is the same for the white noise and movie stimuli. c, The temporal frequency power spectral densities of the white noise (black) and movie (gray) stimuli. Movie spectra were averaged over six different movies. Spectra were normalized so that both stimuli had the same total power. The white noise spectrum was truncated at 16 Hz for plotting. Spectra were calculated as described in Materials and Methods. The power spectra of spatiotemporal natural scene movies are not space-time separable (Dong and Atick, 1995). Thus, the temporal power spectra are shown at a range of spatial frequencies (thin lines), with the mean across all spatial frequencies denoted by the thick lines. d, The spatial frequency power spectra of the white noise and movie stimuli. The spatial power spectra are shown at a range of temporal frequencies (thin lines), with the mean across all temporal frequencies denoted by the thick lines.
Figure 2.
Figure 2.
The responses of LGN neurons to white noise and movie stimuli. a, A raster plot containing the responses of a typical LGN X-cell to eight repeats of a 250 msec segment of the natural scene stimulus. Responses were separated into tonic and burst components according to an ISI criterion. For a response event to be classified as a burst, it must be preceded by at least 100 msec of silence (no spikes in the interval denoted by the long gray band under first spike train). The event must also contain at least two spikes, separated by <4 msec each (successive spikes must fall within the intervals denoted by short gray bands under first spike train). Spikes belonging to burst events are gray, whereas tonic spikes are black. b, A scatter plot of the mean firing rates for the sample of 18 LGN cells in response to white noise and movie stimuli. c, A scatter plot of the percentage of white noise and movie responses belonging to burst events for the sample of 18 LGN cells. d, Scatter plots showing the distribution of successive ISIs from 1000 successive spikes in the responses of an LGN neuron to the white noise and movie stimuli. The intervals denoted by black lines indicate candidate burst spikes, as described in Results.
Figure 3.
Figure 3.
Burst events are triggered by the appearance of objects during natural stimulation. a, Frames 1, 3, 5, and 7 of an eight-frame (256 msec) sequence of the natural scene movie stimulus corresponding to the responses in b. The white circle indicates the RF of the neuron, the responses of which are shown in b. A 48 × 48 pixel region of the entire stimulus for each frame is shown. The inset shows the magnified stimulus inside the RF center. The timeline indicates the onset of each frame (F1-F8). b, A raster plot of the response of a typical neuron to eight repeats of the stimulus shown in a. Spikes that are part of burst events are gray. c-f, Two other stimulus-response pairs for this neuron. Again, for each eight-frame (256 msec) sequence of the stimulus, frames 1, 3, 5, and 7 are shown.
Figure 4.
Figure 4.
Burst events and tonic spikes are triggered by different stimulus features. a, The temporal evolution of the average white noise stimulus (triggered average) in the center of the RF preceding burst events (gray) and tonic spikes (black) for a sample of 18 cells. Burst events were marked by the time of the first spike in the burst. Triggered averages from OFF cells were reflected about the mean luminance. Error bars represent one SD. b, The power spectra of the average stimulus preceding burst events (gray) and tonic spikes (black) shown in a. c, The power spectra of the white noise (dashed) and natural scene movie (solid) stimuli after averaging over all pixels in the center of the RF for each neuron. The spectral products of the normalized stimuli and burst- and tonic-triggered averages (denoted BTA and TTA, respectively) are given in the inset.

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