Improved stimulus representation by short interspike intervals in primary auditory cortex

Abstract

We analyzed the receptive field information conveyed by interspike intervals (ISIs) in the auditory cortex. In the visual system, different ISIs may both code for different visual features and convey differing amounts of stimulus information. To determine their potential role in auditory signal processing, we obtained extracellular recordings in the primary auditory cortex (AI) of the cat while presenting a dynamic moving ripple stimulus and then used the responses to construct spectrotemporal receptive fields (STRFs). For each neuron, we constructed three STRFs, one for short-ISI events (ISI < 15 ms); one for isolated, long-ISI events (ISI > 15 ms); and one including all events. To characterize stimulus encoding, we calculated the feature selectivity and event information for each of the STRFs. Short-ISI spikes were more feature selective and conveyed information more efficiently. The different ISI regimens of AI neurons did not represent different stimulus features, but short-ISI spike events did contribute over-proportionately to the full spike train STRF information. Thus short-ISIs constitute a robust representation of auditory features, and they are particularly effective at driving postsynaptic activity. This suggests that short-ISI events are especially suited to provide noise immunity and high-fidelity information transmission in AI.

Fig. 1.

Example interspike interval (ISI) histograms. Each histogram has 50 bins logarithmically spaced from ISIs of 1 ms up to 10,000 ms. Arrows indicate manually selected borders between the 2 peaks of each distribution. Cell IDs are shown at top right each histogram.

Fig. 2.

Real and Poisson (simulated) ISI histograms. A: ISI histogram of a real spike train (cell c117 from Fig. 1A). Dotted line indicates the static division between the short- and long-ISI categories at 15 ms. B: ISI histogram of the simulated spike train obtained from the rate-coded Poisson model of the same neuron. Total number of simulated spikes matches that of the real spike train. C: relative numbers of short and long ISI events in real vs. Poisson-simulated spike trains across the population of neurons. Positive values indicate that there are more of those events in the real spike train. Standard error bars are shown.

Fig. 3.

Synergy in ISI patterns. A: comparison of information conveyed by short- and long-ISI events to 2 times the information conveyed by single spikes. Points above the dotted line indicate that the 2 spikes that constitute the ISI event are synergistic; i.e., the ISI event conveys more information than the sum of the information conveyed by the 2 spikes independently. Points below the dotted line indicate the 2 spikes in the ISI event contribute redundant information. Points directly on the dotted line indicate the 2 spikes in the ISI event convey independent information. B: mean synergy values for short- and long-ISI events. Spikes in short-ISI events are significantly synergistic (P < 0.01, t-test) while spikes in long-ISI events are not (P > 0.1, t-test). SE bars are shown.

Fig. 4.

Example spectrotemporal receptive fields (STRFs) based on different ISIs. Each column contains the STRFs for one neuron; cell IDs are shown in the top right of the first row. First row: STRFs constructed from all the spikes in the response; second row: STRFs for short-ISI (<15 ms) spikes; third row: STRFs for long-ISI (>15 ms) spikes. A1–A3: example neuron where the long-ISI STRF shares minor inhibitory sideband structures with the full-response STRF that are absent in the short-ISI STRF. B1–B3: example neuron where the short-ISI STRF has an excitatory sideband structure absent in the long-ISI STRF. C1–C3: example neuron where the full-response, short-ISI, and long-ISI STRFs are largely similar.

Fig. 5.

Comparison of STRF and spike-triggered stimulus similarity to full-response STRFs. A: comparison of ISI-specific STRF similarity to mean similarity of 50 resampled spike trains. Resampled spike trains consist of spikes randomly selected (without replacement) from the full spike train matching the number of events in the ISI-specific spike trains. Points above the dotted diagonal line indicate that the ISI-specific STRF was more similar than expected to the full-response STRF while points below the dotted line indicate the ISI-specific STRF was less similar than expected. B: comparison of mean similarity of stimuli triggered to either short or long-ISI spikes to the full-response STRF. Stimuli associated with short-ISI events are on average more similar to the full-response STRF than those associated with long-ISI events. SI, similarity index.

Fig. 6.

Comparison of STRF feature selectivity and event information for short- and long-ISI events. A: comparison of short- and long-ISI feature selectivity index values. Short-ISI events are significantly more feature selective than long-ISI events (P < 0.01, signed-rank test). B: comparison of short- and long-ISI event information. Short-ISI events convey more bits per spike than long-ISI events (P < 0.01, signed-rank test). FSI, feature selectivity index.

Fig. 7.

Relationship between increases in feature selectivity and increases in event information. These 2 measures were not significantly correlated (P > 0.1, t-test).