Activity in the barrel cortex during active behavior and sleep

Abstract

The rate at which neurons fire has wide-reaching implications for the coding schemes used by neural systems. Despite the extensive use of the barrel cortex as a model system, relatively few studies have examined the rate of sensory activity in single neurons in freely moving animals. We examined the activity of barrel cortex neurons in behaving animals during sensory cue interaction, during non-stimulus-related activity, during various states of sleep, and during the administration of isoflurane. The activity of regular-spiking units (RSUs: predominantly excitatory neurons) and fast spiking units (FSUs: a subtype of inhibitory interneurons) was examined separately. We characterized activity by calculating neural firing rates, because several reports have emphasized the low firing rates in this system, reporting that both baseline activity and stimulus evoked activity is <1 Hz. We report that, during sensory cue interaction or non-stimulus-related activity, the majority of RSUs in rat barrel cortex fired at rates significantly >1 Hz, with 27.4% showing rates above 10 Hz during cue interaction. Even during slow wave sleep, which had the lowest mean and median firing rates of any nonanesthetized state observed, 80.0% of RSUs fired above 1 Hz. During all of the nonanesthetized states observed 100% of the FSUs fired well above 1 Hz. When rats were administered isoflurane and at a depth of anesthesia used in standard in vivo electrophysiological preparations, all of the RSUs fired below 1 Hz. We also found that >80% of RSUs either upmodulated or downmodulated their firing during cue interaction. These data suggest that low firing rates do not typify the output of the barrel cortex during awake activity and during sleep and indicate that sensory coding at both the individual and population levels may be nonsparse.

Fig. 1.

Example showing the activity pattern of 1 somatosensory cortex (SI) regular-spiking unit (RSU) within and outside of the texture. A: cartoon of the circular track. The rat's task was to run [¾] of the way around the track at a time for a food reward. There are 4 such unique [¾] turns. For data presentation, the circular track was “cut” at an arbitrary point and linearized as shown. B: raster plot from 1 cell during a single run session. Each of the 4 sets of rows corresponds to 1 of the unique types of [¾] laps. In 1 type (2nd set from the bottom), the rat does not run through the texture. Note that the cell fires consistently outside of the texture and increases firing within the texture. C: rate map formed by collapsing data across all trials. This cell fires around 8.3 Hz outside of the texture and reaches a peak firing rate within the texture >35 Hz. D: firing rate of the cell relative to position when the spiking of the cell has been modeled as a function of position and spiking history.

Fig. 2.

Classification of units as either RSUs or fast spiking units (FSUs) and the distribution of firing rates within and outside of texture. A: each unit's average firing rate over the entire track is plotted against the peak to trough width of the average waveform of that unit. All units that had a peak to trough width <370 μs and a firing rate >10 Hz were considered FSUs (n = 10). All units with width >370 μs were considered RSUs (n = 95). B: distribution of both RSU (n = 95) and FSU (n = 10) firing rates, outside of the texture. C: distribution of both RSU and FSU firing rates, within the texture. D: each point on the graph represents the fraction of RSUs that fire at or below a given firing rate. The horizontal gray line (black line) represents the fraction of cells that fire <1 Hz within the texture (outside of texture). Total neurons (n = 95). E: each point on the graph represents the fraction of FSUs that fire at or below a given firing rate (n = 10).

Fig. 3.

Distribution of slow wave sleep (SWS) firing rates. A: distribution of both RSU (n = 95) and FSU (n = 10) firing rates during SWS. B: each point on the graph represents the fraction of RSUs that fire at or below a given firing rate. The black horizontal line (gray line, gray dotted line) represents the fraction of cells that fire below 1 Hz during SWS (during awake activity outside of texture, during awake activity inside of texture). The firing rate during SWS is significantly less than the rate outside of the texture or within the texture. (K-S test, 1-tail test P = 0.0031 and P = 0.0050, n = 95). C: each point on the graph represents the fraction of FSUs that fire at or below a given firing rate (n = 10). The firing rate during SWS is significantly less than the rate outside of the texture or within the texture (K-S test, 1-tail test P = 0.0155 and P = 0.0006, n = 10).

Fig. 4.

Distribution of firing rates of RSUs (n = 40) during maze running and during the isoflurane condition. A: each point on the graph represents the fraction of RSUs that fire at or below a given firing rate. The gray horizontal line represents the fraction of cells that fire below 1 Hz during maze running. The firing rates of the RSUs were significantly lower during the isoflurane condition than during maze running (K-S test, 1-tail test P = 0.000000015, n = 40). Inset: average firing rates during maze running and during the isoflurane condition.

Fig. 5.

Activity of RSU and FSU cells within the textured region of the track. A: the average firing rate outside and inside of the texture when rates for all RSUs (n = 95) are averaged. This average is also calculated separately for cells that are either upmodulated (n = 49) or downmodulated (n = 36). B: the average firing rate outside and inside of the texture when rates for all FSUs (n = 10) are averaged. This average is also calculated separately for cells that are either upmodulated (n = 2) or downmodulated (n = 2). C: the average firing rate of all RSUs inside and outside of the texture with respect to position. D: the average firing rate of all FSUs inside and outside of the texture with respect to position. E: the percentage of RSUs that are either upmodulated or downmodulated by ≥20% throughout the texture or in the beginning, middle, or end sections of the texture. F: the percentage of FSUs that are either upmodulated or downmodulated by ≥20% throughout the texture or in the beginning, middle, or end sections of the texture.