Neuronal sequences during theta rely on behavior-dependent spatial maps

  1. Eloy Parra-Barrero
  2. Kamran Diba
  3. Sen Cheng  Is a corresponding author
  1. Institute for Neural Computation, Ruhr University Bochum, Germany
  2. International Graduate School of Neuroscience, Ruhr University Bochum, Germany
  3. Department of Anesthesiology, University of Michigan, Michigan Medicine, United States
9 figures and 2 additional files

Figures

Figure 1 with 1 supplement
Simulated effect of running speed on population and single-cell properties in spatial sweep and temporal sweep models.

Certain findings in previous studies (green) paradoxically support the spatial sweep at the single-cell level, but the temporal sweep at the population level. (A) Left. At different phases of theta, …

Figure 1—figure supplement 1
Schematic illustration of the relationship between place fields, theta phase precession, and theta sequences.

Illustration of theta phase coding in spatial navigation. (A) A rat is running from left to right on a linear track. The firing rate of three place cells are indicated in different colors. (B) The …

The behavior-dependent sweep integrates aspects of both spatial and temporal sweeps.

Simulated data plotted as in Figure 1A and C. (A) Different phases of theta represent positions reached at different time intervals into the past or future assuming the animal ran at the …

Theta trajectory lengths increase proportionally with running speed.

(A) A random sample of theta sequences from a representative experimental session, with position probabilities decoded from the population spikes. Zero corresponds to the actual position of the rat …

Figure 4 with 1 supplement
Place field size increases with running speed when combining data across fields, but not for individual fields.

(A) The size of a given place field remains roughly constant regardless of running speed in examples from three individual place fields (one per column). Dashed gray lines represent the extent of …

Figure 4—figure supplement 1
Restricting the theta trajectory length analysis to areas covered by the place fields analyzed does not change the results meaningfully.

Theta trajectory lengths remain unchanged when restricting the analysis to theta cycles occurring in areas covered by place field analyses. Same analysis as in Figure 3D, but pooling only theta …

Phase precession slope increases with running speed when combining data across fields, but not for individual fields.

(A) Example phase precession slopes at different speeds for three fields. Instantaneous speeds when the spikes where emitted are color coded. Thin gray line displays the occupancy. At the bottom, …

Figure 6 with 3 supplements
Structured place field and theta trajectory heterogeneity correlates with characteristic speed.

(A) Potential explanation for the increase in average theta trajectory length, place field size and phase precession slopes with speed despite the lack of systematic within-field changes. The …

Figure 6—figure supplement 1
Like D, G, separated by animal.

Theta trajectory lengths vary across the track and correlate with characteristic running speed. Histograms of theta trajectory lengths as a function of normalized distance from the start of the run …

Figure 6—figure supplement 2
Like E, F, H, and I, separated by animal.

Place field sizes and phase precession slopes vary across the track and correlate with characteristic running speed. (A) Place field sizes as a function of distance from the start of the run (first …

Figure 6—figure supplement 3
Linear relationships between place field sizes, phase precession slopes, and theta trajectory lengths.

Place field sizes, phase precession slopes, and theta trajectory lengths correlate with one another. (A) The inverse of phase precession slope correlates strongly with place field size. Colored dots …

Figure 7 with 2 supplements
Only the behavior-dependent sweep model accounts for all experimental observations.

(A) Summary of experimental results from Figures 35. Results from all animals are combined. Only one animal featured more than three sessions. For this animal, we sub-selected three sessions at …

Figure 7—figure supplement 1
The behavior-dependent sweep model captures changes in place field skewness with acceleration.

The behavior-dependent sweep model captures changes in place field skewness with acceleration. Place field skewness is correlated with the mean acceleration through the field in the experimental …

Figure 7—figure supplement 2
The behavior-dependent sweep model captures changes in peak firing rates with speed.

The behavior-dependent sweep model replicates the experimentally observed increase in firing rates with running speed. Analyses and plotting conventions as for Figure 4B & C, for the peak firing …

Appendix 1—figure 1
Variable theta phase locking fails to account for the combination of population and single-cell results.

(A, B) Comparison of experimental and simulated data produced by a model with constant dθ but variable theta phase noise. Plotting conventions as in Figure 7. The variable noise model does a good …

Appendix 1—figure 2
Theta phase locking and theta timescale coordination between cells vary with speed in the variable noise model but not in the experimental data.

(A, B) The effect of speed on the residuals of the phase precession cloud fits (i.e. mean squared orthogonal distances from the points to the fitting line). The fits are calculated after normalizing …

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