Article Figures & Data
Figures
- Figure 1.
Variability in spike-time autocorrelations of neurons recorded in the superficial layers of the MEC. A, Sagittal brain sections stained with cresyl violet showing tetrode tracks reaching the superficial layers of the MEC. Tetrode tips are indicated by red arrows. B, Firing rate maps, spatial autocorrelations, and spike-time autocorrelations of four neurons. Note the variability in the shape of the spike-time autocorrelations. Peak firing rates and grid scores are displayed above the firing rate maps and spatial autocorrelations, respectively. C, Left, Unfiltered local field potentials of two 1 s time windows recorded on the same tetrode. The spikes of two neurons are depicted as red lines below the field potentials. Right, Spike-time autocorrelations of the two neurons. The autocorrelations on the left contain the spikes of the 1 s traces, whereas those on the right are for spikes of the entire recording session. Only the neuron on the top trace fired bursts of spikes with interspike intervals of ∼4 ms.
- Figure 2.
Identification of bursty and non-bursty neurons from spike-time autocorrelations. A, A principal component analysis was performed on the first 12 ms of the spike-time autocorrelations. The scatter plot shows the first two principal components. Neurons form a C-shaped structure with two main axes. A 2D kernel smoothed density estimate indicates centers of mass. Inset, Weights of the first three principal components for the autocorrelation time vector. B, 3D scatter plot of the first three principal components with k-means assignment of class membership (k = 2). Red, Bursty neurons; black, non-bursty neurons. Above the scatter plot are four examples of spike-time autocorrelations, ranging from bursty (left) to non-bursty (right). C, Left, Linear discriminant analysis of the spike-time autocorrelations to separate bursty and non-bursty neurons. All principal neurons are shown. Inset, Examples of spike-time autocorrelations of neurons with different scores. Right, Same as on the left but without the “intermediate” neurons falling in the region of the x-axis where bursty and non-bursty neurons overlap. D, Mean spike-time autocorrelation of bursty and non-bursty neurons. E, Cumulative distribution of interspike intervals. Bursty neurons emitted more spikes with interspike intervals shorter than 20 ms. F, Classification accuracy of bursty and non-bursty neurons when shorter recording periods are considered to calculate the spike-time autocorrelations. The gray line indicates classification accuracy when all principal neurons are included. The dotted blue line indicates accuracy if a 0.3 exclusion zone is present on both sides of the hyperplane separating bursty and non-bursty neurons.
- Figure 3.
Spike waveform, interspike interval adaptation, and distribution across recording sites of bursty and non-bursty neurons. A–D, Mean spike waveform (A), spike duration (B), spike asymmetry (C), and mean firing rate (D) of bursty and non-bursty neurons. E, Mean first and second interspike intervals during spike triplets (3 spikes within 50 ms) for bursty and non-bursty neurons. F, Ratio of the first and second interspike intervals during spike triplets. G, Clustering of bursty neurons around recording sites. The vertical bars indicate the number of cell pairs recorded. The neurons in each pair were simultaneously recorded on the same tetrode. Red, Pairs of bursty neurons; black, pairs of non-bursty neurons; gray, mixed pairs. The distributions represent the number of pairs expected if bursty and non-bursty neurons were randomly distributed across the recording sites. More pairs of bursty neurons and fewer mixed pairs were observed than expected by chance. H, Ratio of bursty to non-bursty neurons during the first 3 and the last 3 recording days. The ratio was relatively stable throughout the experiment. ** p < 10−3, *** p < 10−10. isi, Interspike interval.
- Figure 4.
Grid cell spatial periodicity of bursty and non-bursty neurons. A, Firing rate maps, spatial autocorrelations, and spike-time autocorrelations at two different time scales for six neurons with grid periodicity. The three neurons on the left are bursty neurons, whereas those on the right are non-bursty neurons. B, Distribution of grid scores for bursty and non-bursty neurons. The gray line indicates the distribution expected by chance. C, Proportion of grid cells for bursty and non-bursty neurons. D, Distribution of spatial information scores for both classes of neurons. E–G, Mean spike-time autocorrelation, mean spike waveform, and distribution of spatial information scores for bursty and non-bursty grid cells. **p < 10−4; ***p < 10−5.
- Figure 5.
Head-direction selectivity is stronger in non-bursty than in bursty neurons. A, Spike-time autocorrelations, firing rate maps, and head-direction rate polar plots of four bursty and four non-bursty neurons. The peak firing rate is indicated above each firing rate map and head-direction polar plot. vl, Mean vector length of the head-direction polar plot. B, Distribution of head-direction mean vector length for bursty and non-bursty neurons. C, Proportion of head-direction cells in bursty and non-bursty neurons. D, Head-direction vector length for bursty and non-bursty neurons with high (>0.48) and low (<0.48) spatial information scores. E, Head-direction vector length for neurons with and without grid cell spatial periodicity. Grid cells had lower head-direction selectivity. **p < 10−4; ***p < 10−5.
- Figure 6.
Border proximity preferentially encoded by non-bursty neurons. A, Spike-time autocorrelations, firing rate maps, and head-direction polar plots of six neurons firing predominantly along one of the environment walls. vl, Mean vector length of the head-direction polar plot. B, Distribution of border scores for bursty and non-bursty neurons. C, Proportion of border cells in bursty and non-bursty neurons. D, Head-direction vector length plotted against the border score. E, Percentages of the different spatially selective cell types in bursty and non-bursty neurons. Grid, Grid cells (grid score >0.54); Hd, head-direction cells (Hd vector length >0.4); Conj, conjunctive grid × head-direction cells (grid score >0.54; Hd vector length >0.4); Border, border cells (border score >0.528; grid score <0.54); Irregular, irregular spatially selective cells (spatial information >0.48; grid score <0.54; Hd vector length <0.4); Non-spatial, nonspatially selective cell (spatial information <0.48; grid score <0.54; Hd vector length <0.4). The data of four mice for which head direction was not available were not included. *p < 0.05; ***p < 10−9.
- Figure 7.
Different temporal properties of bursty and non-bursty neurons during theta oscillations. A, Polar plots showing the preferred theta phase and theta mean vector length of bursty and non-bursty neurons. B, Probability distribution of preferred theta phase for bursty and non-bursty neurons. C, Distribution of theta vector length for bursty and non-bursty neurons. Asterisks indicate that the two distributions were significantly different. There was no significant difference between the medians of the two groups (Wilcoxon rank sum test, W = 86,154, p = 0.385). D, Power spectra of the instantaneous firing rate of bursty and non-bursty neurons. E, Mean theta peak frequency of bursty and non-bursty neurons. F, Distribution of the theta rhythmicity index. G, Firing probability as a function of theta phase for both classes of neurons. H, Theta vector length of bursty and non-bursty neurons divided into different spatially defined cell types. Grid, Grid cells (grid score >0.54); Hd, head-direction cells (Hd vector length >0.4); Conj, conjunctive grid × head-direction cells (grid score >0.54; Hd vector length >0.4); Border, border cells (border score >0.528; grid score <0.54); Irregular, irregular spatially selective cells (spatial information >0.48; grid score <0.54; Hd vector length <0.4); Non-spatial, nonspatially selective cell (spatial information <0.48; grid score <0.54; Hd vector length <0.4); Int, interneurons (mean firing rate >10 Hz). I, Classification of neurons as putative calbindin+ (pCalb+) and calbindin− (pCalb−) cells based on their preferred theta phase and coupling strength. The data from Tang et al. (2014) were used to construct the classifier. J, Left, Proportion of neurons falling into the four possible cell categories (pCalb+/bursty, pCalb+/non-bursty, pCalb−/bursty, pCalb−/non-bursty). Right, Proportion of pCalb− and pCalb+ neurons that were grid cells, head-direction cells, and border cells. *p < 0.01; **p < 10−5; ***p < 10−8.
- Figure 8.
Spike transmission from excitatory neurons to putative interneurons preferentially involves bursty neurons. A, Two examples of putative connection between a bursty neuron and an interneuron. Top two rows, Firing rate maps and spike-time autocorrelations of the bursty neurons and interneurons. Numbers above the maps indicate peak firing rates. Bottom row, Spike-time crosscorrelations at two different time scales between the bursty neurons and interneurons. The sharp peaks (>5 SDs) with a latency between 1 and 4 ms suggest the presence of excitatory connectivity between the neurons. The lower bins near time 0 in the crosscorrelations are attributable to a refractory period in the spike detection algorithm and affect only pairs of neurons recorded on the same tetrode. B, Same as in A but for two pairs of non-bursty neurons and interneurons. C, Left, Probability that neurons excite (significant peak in crosscorrelation) other neurons, shown separately for bursty and non-bursty neurons. Right, Mean amplitude of peaks (peak − baseline) at a short latency, shown for bursty and non-bursty neurons. Mean ± SEM. D, Crosscorrelation of a bursty (left) and a non-bursty (right) neuron with the same putative interneuron (middle). *p < 0.01. Int., Interneurons.
- Figure 9.
Distribution of bursty and non-bursty neurons in layers II and III of rats. A, A 3D scatter plot of the first three principal components of the spike-time autocorrelations (first 12 ms). k-means clustering (k = 2) was used to assign the class membership of neurons. Bursty and non-bursty neurons of both layers are shown in different colors. B, Proportion of bursty and non-bursty neurons in layers II and III of the MEC. C, Mean spike-time autocorrelation (±12 or +300 ms) of bursty and non-bursty neurons. D, Mean spike-time autocorrelation for bursty and non-bursty neurons in layers II and III. ***p < 10−4.
