Working memory capacity of crows and monkeys arises from similar neuronal computations
- Neural Basis of Learning, Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum, Germany
- Animal Physiology, Institute of Neurobiology, University of Tübingen, Germany
Figures
Figure 1 with 1 supplement
Behavioral overview.
(A) Behavioral paradigm (reproduced from Balakhonov and Rose, 2017). The birds had to center and hold their gaze for the duration of the sample and delay period, and subsequently indicate which colored square had changed. (B) Boxplot of performance for different ipsilateral loads (i.e., on the side where the change occurred). Horizontal lines indicate significant differences between loads, box indicates the median, 1st, and 3rd quartile (whiskers extend to 1.5 times the inter-quartile range). (C) Mean performance matrix for ipsi- and contralateral load combinations (values are rounded to the nearest integer). Additional contralateral items at an ipsilateral load of 1 barely affected performance (bottom row). At higher ipsilateral loads additional contralateral items reduced performance more clearly (middle and top row). Statistical modeling revealed an interaction at these higher loads (see text).
Figure 1—figure supplement 1
Capacity of crow working memory (WM).
Line indicates capacity K at different loads. The peak at four items indicates the capacity. Dashed lines indicate maximum capacity and fixed capacity of 1. Error bars indicate the standard error of the mean.
Figure 2 with 2 supplements
Color discrimination in the neuronal response (information, percent explained variance [PEV]) generally decreases with load, but some neurons show the opposite effect.
Shown are the three ipsilateral load conditions (i.e., load increases on the same side as the neuron’s favorite location). Ipsilateral loads are one (blue), two (yellow), and three (red). The labels ‘color A’ and ‘color B’ always refer to the same pair of colors at the neuron’s favorite location, irrespective of the load condition. (A) Example of a sample neuron with color information decline at load 1 (blue), load 2 (yellow), and load 3 (red). Top: raster plot, where every dot represents a single spike during the individual trials (rows of dots); middle: peri-stimulus-time histogram (PSTH) of average firing rate (solid line for color ID 1, dashed line for color ID 2) with the standard error of the mean (shaded areas); bottom: percent explained variance of color identity (a measure of information about color) along the trial, the line at the top of the y-axis indicates significant bins. (B) Same as in (A) for an example of a delay neuron with information gain at a higher load.
Figure 2—figure supplement 1
Color discrimination in the neuronal response (information, percent explained variance [PEV]) decreases with load.
Example of a delay neuron with color information decline, at load 1 (blue), load 2 (green), and load 3 (red). Top: raster plot, where every dot represents a single spike during the individual trials (rows of dots); middle: peri-stimulus-time histogram (PSTH) of average firing rate (solid line for color ID 1, dashed line for color ID 2) with the standard error of the mean (shaded areas); bottom: percent explained variance of color identity (a measure of information about color) along the trial, the line at the top of the y-axis indicates significant bins.
Figure 2—figure supplement 2
Color discrimination in the neuronal response (information, percent explained variance [PEV]) increases with load.
Example of a sample neuron with color information gain; at load 1 (blue), at load 2 (green), and load 3 (red). Top: raster plot, where every dot represents a single spike during the individual trials (rows of dots); middle: peri-stimulus-time histogram (PSTH) of average firing rate (solid line for color ID 1, dashed line for color ID 2) with the standard error of the mean (shaded areas); bottom: percent explained variance of color identity (a measure of information about color) along the trial, the line at the top of the y-axis indicates significant bins.
Figure 3 with 2 supplements
Overview of recorded neurons.
(A) The neuronal population can be best described by seven individual clusters. (B) Percentages of neurons (total n = 362) with significant color information at load 1, during the sample and the delay. (C) Percentages (rounded) of significant neurons in individual load conditions for sample (n = 249), delay (n = 94), and sample and delay (n = 133). The pieces of the pies depicting significance at a specific load relate to the number of significant neurons in the respective phase (e.g., 36% of the 94 delay neurons (i.e., 34 neurons) are significant at load 1 (all pieces contain blue), these are the same neurons that make up the 9.36% of the total 362 neurons depicted in B).
Figure 3—figure supplement 1
Overview of analyses for bird 1.
(A) The neuronal population can be best described by seven individual clusters. (B) Percentages (rounded) of significant neurons in individual load conditions for sample (n = 68), delay (n = 19), and sample and delay (n = 37). (C) On correct trials (left) color is represented during the early and late phase of the sample and, to a lesser degree, during the early and late delay. On error trials (right), color information can be found in the early sample phase at load 2, and in the late sample phase at loads 2 and 3 (asterisks). Analysis of load 1 error trials was omitted due to their very low abundance. Statistical comparisons of correct vs. error trial information were performed on sub-sampled correct trials. Early and late sample each 400 ms, early and late delay each 500 ms, error bars indicate the standard error of the mean. (D) Divisive normalization-like regularization was observable for neuronal responses of neurons losing information (top) but not for neurons gaining color information at load 2 (bottom). Selectivity (SE) indicates how much the neuronal response is influenced by a color, relative to a second color when either is presented alone. Sensory interaction (SI) indicates how much the neuronal response is influenced by either color when both were displayed simultaneously. Slopes close to 0.5 indicate an equal influence of both colors. Slopes <0.5, or >0.5 indicate a weighted influence of a color. (Top) Information-carrying neurons in the sample (n = 35; left) and delay (n = 15; right) population. (Bottom) Information gaining neurons in the sample (n = 10; left) and delay (n = 3; right) population. The red line indicates the regression fit.
Figure 3—figure supplement 2
Overview of analyses for bird 2.
(A) The neuronal population can be best described by seven individual clusters. (B) Percentages (rounded) of significant neurons in individual load conditions for sample (n = 181), delay (n = 75), and sample and delay (n = 96). (C) On correct trials (left) color is represented during the early and late phase of the sample and, to a lesser degree, during the early and late delay. On error trials (right), color information can be found in the late sample phase at loads 2 and 3 (asterisks). Analysis of load 1 error trials was omitted due to their very low abundance. Statistical comparisons of correct vs. error trial information were performed on sub-sampled correct trials. Early and late sample each 400 ms, early and late delay each 500 ms, error bars indicate the standard error of the mean. (D) Divisive normalization-like regularization was observable for neuronal responses of neurons losing information (top) but not for neurons gaining color information at load 2 (bottom). Selectivity (SE) indicates how much the neuronal response is influenced by a color, relative to a second color when either is presented alone. Sensory interaction (SI) indicates how much the neuronal response is influenced by either color when both were displayed simultaneously. Slopes close to 0.5 indicate an equal influence of both colors. Slopes <0.5 or >0.5 indicate a weighted influence of a color. (Top) Information-carrying neurons in the sample (n = 70; left) and delay (n = 28; right) population. (Bottom) Information gaining neurons in the sample (n = 46; left) and delay (n = 5; right) population. The red line indicates the regression fit.
Figure 4 with 2 supplements
Information encoding at the population level.
(A) Color information (percent explained variance [PEV]) decreases with an increasing ipsilateral load (i.e., on the same side as the neuron’s favorite location) but not with an increasing contralateral load (i.e., on the opposite side to the neuron’s favorite location). (B) On correct trials (left) color is represented during the early and late phase of the sample and, to a lesser degree, during the early and late delay. On error trials (right), color information can be found in the early sample phase at load 2, and in the late sample phase at loads 2 and 3 (asterisks). Analysis of load 1 error trials was omitted due to their very low abundance. Statistical comparisons of correct vs. error trial information were performed on sub-sampled correct trials. Early and late sample each 400 ms, early and late delay each 500 ms, shaded areas, and error bars indicate the standard error of the mean.
Figure 4—figure supplement 1
Sample population (A) and delay population (B), same as Figure 4A with full time axis.
Notably, the ‘delay populations’ (B) also showed an elevated level of information during the sample, whereas the ‘sample populations’ (A) did not show an elevated level of information during the delay.
Figure 4—figure supplement 2
Same as Figure 4B, after applying a more stringent criterion on neuronal significance (see text).
On correct trials (left) color is represented during the early and late phase of the sample and, to a lesser degree, during the early and late delay. On error trials (right), color information can be found in the early sample phase at load 2, and in the late sample phase at loads 2 and 3 (asterisks). Analysis of load 1 error trials was omitted due to their very low abundance. Statistical comparisons of correct vs. error trial information were performed on sub-sampled correct trials. Early and late sample each 400 ms, early and late delay each 500 ms, error bars indicate the standard error of the mean.
Figure 5 with 2 supplements
Divisive normalization-like regularization was observable for neuronal responses of neurons losing information (A) but not for neurons gaining color information at load 2 (B).
Selectivity (SE) indicates how much the neuronal response is influenced by a color, relative to a second color when either is presented alone. Sensory interaction (SI) indicates how much the neuronal response is influenced by either color when both were displayed simultaneously. Slopes close to 0.5 indicate an equal influence of both colors. Slopes <0.5, or >0.5 indicate a weighted influence of a color. (A) Information-carrying neurons in the sample phase (as one bin; n = 105; left) and delay phase (as one bin; n = 43; right) population. (B) Information gaining neurons in the sample phase (as one bin; n = 56; left) and delay phase (as one bin; n = 8; right) population. The red line indicates the regression fit.
Figure 5—figure supplement 1
Divisive normalization-like regularization was observable for neuronal responses of neurons without significant information.
Both phases contain the same neurons (n = 171). Selectivity (SE) indicates how much the neuronal response is influenced by a color, relative to a second color when either is presented alone. Sensory interaction (SI) indicates how much the neuronal response is influenced by either color when both were displayed simultaneously. Slopes close to 0.5 indicate an equal influence of both colors. Slopes <0.5, or >0.5 indicate a weighted influence of a color. The red line indicates the regression fit. Non-informative sample neurons had a fitted slope of 0.38 (R2adj = 0.16, F(1,1366) = 258.08, p < 0.001), significantly smaller than 0.5 (CI = [0.33 0.42]). Delay neurons had a slope of 0.40, also significantly smaller than 0.5 (R2adj = 0.13, F(1,1366) = 197.51, p < .001, CI = [0.35 0.46]). This indicates that for these neurons the reference color influenced firing rate more than the probe color. This smaller slope is not related to the amount of information encoded for the individual colors (which determined the favorite location). It does however indicate that those non-informative neurons were influenced by any color at their favorite location and thereby might have been informative about if the favorite location had a color but not about what color.
Figure 5—figure supplement 2
Example for information gain due to unequal interaction at load 2.
Notice how a lack of fire rate differentiation at load 1 (blue curves, left plot) turns into a differential firing rate at load 2 (purple curves, right plot). Depicted is one typical neuron. Black box insets depict the color and load condition during the sample (there were no colors present during the delay), and indicate which firing rate curve (mean ± SEM) the neuron had. Source Data File 1: This file contains all details of the reported statistics. The file consists of one MATLAB struct. The struct contains three major fields, corresponding to the different statistical analyses conducted in the Results section. ‘Behavior’ contains statistical results reported in the section ‘The WM capacity of crows is similar to that of monkeys’. ‘smpDlyEarlyLate’ contains statistical results reported in the section ‘The neuronal population has gradually less information with increasing load’. Divisive-normalization-like regularization (‘DNR’) contains statistical results reported in the sections ‘Gain of information at load 2 can be explained by neuronal normalization’ and ‘Higher loads produce divisive normalization-like neuronal responses’.
Author response image 1
Example neuron (same as in Figure 2A of the manuscript), smoothed with 100 ms bins.
Top: raster plot, where every dot represents a single spike during the individual trials (rows of dots); middle: peri-stimulus-time histogram (PSTH) of average firing rate (solid line for color ID 1, dashed line for color ID 2) with the standard error of the mean (shaded areas); bottom: percent explained variance of color identity (a measure of information about color) along the trial, the line at the top of the y-axis indicates significant bins.
Tables
Table 1
Overview of significant groups.
The ‘+’ denotes that a neuron of the respective group had a significant percent explained variance (PEV) in the respective load condition. The ‘-’ denotes that a neuron of the respective group did not have a significant PEV in the load respective condition. The pooled groups contained only neurons with a ‘+’ for the respective load condition.
| Load 1 | Load 2 | Load 3 | Group name | |
|---|---|---|---|---|
| + | - | - | Load 1 neurons | Group I |
| - | + | - | Load 2 neurons | Group II |
| - | - | + | Load 3 neurons | Group III |
| + | + | - | Load 1 and 2 neurons | Group IV |
| + | - | + | Load 1 and 3 neurons | Group V |
| - | + | + | Load 2 and 3 neurons | Group VI |
| + | + | + | Load 1, 2, and neurons | Group VII |
| Pooled group 1 | Pooled group 2 | Pooled group 3 |
Author response table 1
Proportion of neurons with significant color information (number of neurons) at the different load conditions in the sample and the delay phase.
| Phase | Load 1 | Load 2 | Load 3 |
|---|---|---|---|
| Sample | 55 % (137 neurons) | 55 % (137 neurons) | 43 % (107 neurons) |
| Delay | 36 % (34 neurons) | 37 % (35 neurons) | 39 % (37 neurons) |
Additional files
-
Transparent reporting form
- https://cdn.elifesciences.org/articles/72783/elife-72783-transrepform1-v2.pdf
-
Source data 1
Reported statistical results and numerical values.
- https://cdn.elifesciences.org/articles/72783/elife-72783-supp1-v2.zip
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Working memory capacity of crows and monkeys arises from similar neuronal computations
eLife 10:e72783.
https://doi.org/10.7554/eLife.72783
