Volume 79, Issue 3, Pages (August 2013)

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Volume 79, Issue 3, Pages 555-566 (August 2013) Formation and Reverberation of Sequential Neural Activity Patterns Evoked by Sensory Stimulation Are Enhanced during Cortical Desynchronization  Edgar J. Bermudez Contreras, Andrea Gomez Palacio Schjetnan, Arif Muhammad, Peter Bartho, Bruce L. McNaughton, Bryan Kolb, Aaron J. Gruber, Artur Luczak  Neuron  Volume 79, Issue 3, Pages 555-566 (August 2013) DOI: 10.1016/j.neuron.2013.06.013 Copyright © 2013 Elsevier Inc. Terms and Conditions

Figure 1 Experimental Protocol for Somatosensory Stimulation, and Synchronized and Desynchronized Brain States (A) Example LFP in S1 under urethane anesthesia. The gray shaded area indicates the period of tactile stimulation consisting of 1 s long periods of vibration at 20 Hz (inset). (B) Example LFP in S1 under urethane anesthesia after injection of amphetamine. (C) Example LFP and unit activity under urethane anesthesia shown at a higher temporal resolution. Note prominent UP and DOWN states characteristic of the synchronized brain state. (D) Example LFP and unit activity after amphetamine injection. Note that, in the desynchronized state, fluctuations of LFP and unit activity are of smaller amplitude. (E) Mean stimulus-triggered LFP across animals in S1 in urethane only and urethane plus amphetamine conditions. (F) The same as (E) for average spiking activity. PSTH, peristimulus time histogram. Neuron 2013 79, 555-566DOI: (10.1016/j.neuron.2013.06.013) Copyright © 2013 Elsevier Inc. Terms and Conditions

Figure 2 Similarity between Spontaneous and Evoked Temporal Patterns Is Enhanced by Amphetamine (A) The latency of a neuron is defined as the center of mass of the cross-correlogram of the neuron with the summed activity of all other simultaneously recorded cells (MUA). (B) Example of temporal patterns before, during, and after tactile stimulation in amphetamine condition from a representative experiment. Each row represents a cross-correlogram of a neuron with the summed activity of all other neurons normalized between zero and one. Neurons are ordered according to their latency (red dot) during stimulation (middle panel). The same order was used to plot the latency of the neurons before stimulation (top panel) and after stimulation (bottom). (C) Left: Scatter plot of the latencies of neurons for evoked activity and spontaneous activity before stimulation plotted for the same neurons as in (B). Right: Scatter plot of the latencies for the same neurons for evoked and spontaneous activity after stimulation. Note that the distribution of points is closer to the identity line, indicating higher similarity between latencies for evoked and spontaneous period after stimulation. (D) Similarity of spontaneous activity patterns to evoked activity patterns (quantified by latency correlation) before (blue) and after (orange) tactile stimulation for amphetamine (left) and urethane-only (right) conditions. Connected dots represent one animal. Note that, in the amphetamine condition, the similarity of spontaneous sequences to evoked sequences increases for all rats after stimulation. Rats that show latency correlation increase under urethane are shown in magenta, and rats that show latency correlation decrease under urethane are depicted with light blue lines. (E) Average change in similarity to evoked patterns based on amphetamine and urethane data from (D); red and blue bar, respectively. White bars show average change in similarity to evoked patterns calculated from pair-wise cross-correlograms. Error bars represent the SEM. (F) Synchronized brain state reduces formation of reverbatory activity in somatosensory cortex. x axis shows the percentage of time that the population activity spent in DOWN states; y axis units are the same as in (E). Rats that show latency correlation increase under urethane (Ureth ▴) are marked with magenta color, and rats that show latency correlation decrease under urethane (Ureth ▾) are shown in light blue. Red color denotes rats after amphetamine injection. (G) Latency correlation evolution in time in S1 before, during, and after stimulation (each dot represents the average from all rats; error bars denote SEM). The shaded area corresponds to the stimulation period. The insets at the top show the slope distribution of latency correlations in the corresponding period of the experiment for each rat. Note how the spontaneous activity becomes gradually more similar to evoked patterns during stimulation and how the similarity slowly decreases after stimulation. Stars denote points significantly different from spontaneous activity before stimulation (p < 0.05; t test). See also Figures S2, S3, and S4. Neuron 2013 79, 555-566DOI: (10.1016/j.neuron.2013.06.013) Copyright © 2013 Elsevier Inc. Terms and Conditions

Figure 3 Template Matching (A) Raster plot of representative 2 s of spontaneous activity before tactile stimulation. Blue traces at the top of rasters show matching score, and stars indicate “good matches”, defined as above 95% of matching score. TM, template matching. (B) Raster plot of 2 s of spontaneous activity after tactile stimulation. Note the greater number of good matches (denoted by stars) after stimulation than before. (C) Stimulus-triggered activity used as a template. In (A) and (B), template is superimposed on sample activity windows, showing good match. (D) Example of template-matching histograms for representative data from one rat injected with amphetamine. The solid blue (orange) line shows the frequency of the matching values before (after) stimulation. The shaded regions denote the 0.1% of the highest matching values. The dotted lines represent the mean of such values. (E) Box plot of differences between the highest matching values for spontaneous activity after and before stimulation, which corresponds to the differences between the dotted lines in (D) for all rats. On each box, the central mark denotes the median, the edges of the box are the 25th and 75th percentiles, and the whiskers extend to the most extreme data points. In the amphetamine condition, the template matching between spontaneous and evoked patterns increases after stimulation, which is consistent with latency analyses shown in Figure 2. See also Figure S6. Neuron 2013 79, 555-566DOI: (10.1016/j.neuron.2013.06.013) Copyright © 2013 Elsevier Inc. Terms and Conditions

Figure 4 Persistence of Firing Rate Correlation in S1 (A) Pair-wise firing rate correlation matrices for the neurons in S1 before, during, and after tactile stimulation for a representative animal injected with amphetamine. To facilitate visual comparison of the matrices, the elements were sorted to group together neurons with similar correlations (for sorting, we used values of the first principal component calculated for the matrix from the stimulation period). The same order was used for the other matrices. (B) Scatter plot of the similarities (measured as the Euclidean distance) between firing rate correlation matrices for each animal. Distribution of points above the identity line indicates that spontaneous firing rate correlations after stimulation become more similar to stimulus-evoked correlations. Inset shows the distribution of differences between distances in the corresponding scatter plots. D, Euclidian distance. (C) Changes in firing rate correlations over time analyzed with EV in the amphetamine condition. The gray shaded area corresponds to the stimulation period. The error bars correspond to the SEM. Solid lines represent the explained variance and dotted lines represent the reversed explained variance (REV; see Supplemental Experimental Procedures). Stars indicate points significantly different from REV (control) values (p < 0.05; t test). Neuron 2013 79, 555-566DOI: (10.1016/j.neuron.2013.06.013) Copyright © 2013 Elsevier Inc. Terms and Conditions

Figure 5 Experimental Protocol for Auditory Experiments (A–D) Example LFP (top) and unit activity (bottom) in auditory cortex under urethane anesthesia alone (A) and after infusion of carbachol (B), amphetamine injection (C), and NMDA antagonist injection (D). Grey shaded area indicates the period of auditory stimulation consisting of 500 ms long tones interspersed with 1 s of silence (inset). (E) Same type of plot as (A)–(D) for awake, head-restrained rat. (F) Brain state in each condition measured as % of down states duration. Error bars denote the SEM. (G) Stimulus-triggered LFP in A1 averaged across all animals for each experimental condition. The bars on top represent the stimulation duration for the awake and anaesthetized cases, respectively. (H) The same as (G) for average spiking activity. See also Figures S1 and S5. Neuron 2013 79, 555-566DOI: (10.1016/j.neuron.2013.06.013) Copyright © 2013 Elsevier Inc. Terms and Conditions

Figure 6 Changes in Similarity between Spontaneous and Evoked Temporal Patterns in Auditory Cortex for Different Experimental Conditions (A–D) Similarity of spontaneous activity patterns to evoked activity patterns (quantified by latency correlation) before and after tactile stimulation during pharmacological treatments. Connected dots represent one animal. (E) Similarity of spontaneous activity patterns to evoked activity patterns during first and last 10 min of tactile stimulation for awake rats. (F–J) Color bars: average change in similarity of spontaneous and evoked patterns based on data from (A)–(E). White bars: average change in similarity of spontaneous and evoked patterns based on latencies calculated from pairwise cross-correlograms. Gray bars: average change in similarity of spontaneous and evoked patterns when latencies from stimulation periods were shuffled between experimental conditions. Values close to zero for gray bars in carbachol and amphetamine conditions indicate that reverberation was stimulus specific. Error bars denote SEM. (K–O) Time course of changes in similarity between spontaneous and evoked patterns during experimental periods (each line represents the average from all rats; dashed lines denote SEM). Similarity is measured by correlation coefficient between latencies calculated from pairwise cross-correlograms. The shaded area corresponds to the stimulation period. Consistent with results from S1, in desynchronized brain state (except MK case), the spontaneous activity becomes gradually more similar to evoked patterns during stimulation, and this similarity slowly decreases after stimulation. Neuron 2013 79, 555-566DOI: (10.1016/j.neuron.2013.06.013) Copyright © 2013 Elsevier Inc. Terms and Conditions