Working memory capacity of crows and monkeys arises from similar neuronal computations

  1. Lukas Alexander Hahn  Is a corresponding author
  2. Dmitry Balakhonov  Is a corresponding author
  3. Erica Fongaro
  4. Andreas Nieder
  5. Jonas Rose
  1. Neural Basis of Learning, Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum, Germany
  2. Animal Physiology, Institute of Neurobiology, University of Tübingen, Germany
6 figures, 2 tables and 2 additional files

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 …

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 …

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 …

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 …

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 …

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 …

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), …

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), …

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 …

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 …

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 …

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 …

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 …

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 …

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 …

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 …

Load 1Load 2Load 3Group name
+--Load 1 neuronsGroup I
-+-Load 2 neuronsGroup II
--+Load 3 neuronsGroup III
++-Load 1 and 2 neuronsGroup IV
+-+Load 1 and 3 neuronsGroup V
-++Load 2 and 3 neuronsGroup VI
+++Load 1, 2, and neuronsGroup VII
Pooled group 1Pooled group 2Pooled 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.
PhaseLoad 1Load 2Load 3
Sample55 % (137 neurons)55 % (137 neurons)43 % (107 neurons)
Delay36 % (34 neurons)37 % (35 neurons)39 % (37 neurons)

Additional files

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