Decreasing sleep requirement with increasing numbers of neurons as a driver for bigger brains and bodies in mammalian evolution
Suzana Herculano-Houzel (2015), Proc Royal Society B 282, 20151853
Mammals sleep between 3 and 19 hours per day, but what regulates daily sleep requirement is unknown. While mammalian evolution has been characterized by a tendency towards larger bodies and brains, sustaining larger bodies and brains requires increasing hours of feeding per day, which is incompatible with a large sleep requirement. Mammalian evolution, therefore, must involve mechanisms that tie increasing body and brain size to decreasing sleep requirements. Here I show that daily sleep requirement decreases across mammalian species and in rat postnatal development with a decreasing ratio between cortical neuronal density and surface area, which presumably causes sleep-inducing metabolites to accumulate more slowly in the parenchyma. Because addition of neurons to the non-primate cortex in mammalian evolution decreases this ratio, I propose that increasing numbers of cortical neurons led to decreased sleep requirement in evolution that allowed for more hours of feeding and increased body mass, which would then facilitate further increases in numbers of brain neurons through a larger caloric intake per hour. Coupling of increasing numbers of neurons to decreasing sleep requirement and increasing hours of feeding thus may have not only allowed but also driven the trend of increasing brain and body mass in mammalian evolution.
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Here are the data used in this study:
Species |
Brain mass, g or cm3 |
Daily sleep, h |
D/A, N/mg.mm2 |
NCX |
DNCX, N/mg |
ACX, mm2 |
O/N |
T |
MCX, g or cm3 |
Primates |
|
|
|
|
|
|
|
|
|
Aotus trivirgatus |
15.750 (19) |
16.97 |
10.831 |
441.90 x 106 (20) |
47,960 (20) |
4,428 (20) |
1.340 (20) |
1.670 |
7.396 (20) |
Callithrix sp. |
7.780 (19) |
10.22 |
17.679 |
244.72 x 106 (20) |
54,240 (20) |
3,068 (20) |
1.114 (20) |
1.331 |
4.084 (20) |
Cebus apella |
52.508 (19) |
5.95 |
3.337 |
1.14 x 109 (20) |
51,080 (20) |
15,306 (20) |
1.106 (20) |
2.067 |
31.640 (20) |
Saimiri sciureus |
30.216 (19) |
9.11 |
7.707 |
1.34 x 109 (19) |
80,920 (20) |
10,500 (20) |
0.768 (20) |
1.333 |
13.992 (20) |
Macaca mulatta |
87.346 (19) |
8.74 |
1.284 |
1.71 x 109 (19) |
32,110 (20) |
25,000 (15) |
2.011 (20) |
1.714 |
42.860 (19) |
Macaca radiata |
61.470 (25) |
9.02 |
2.595 |
1.66 x 109 (20) |
43,810 (20) |
16,882 (20) |
1.278 (20) |
1.835 |
30.986 (20) |
Papio cynocephalus |
151.190 (25) |
6.19 |
1.011 |
2.88 x 109 (20) |
33,730 (20) |
33,378 (20) |
1.317 (20) |
2.177 |
72.668 (20) |
Homo sapiens |
1,509 (24) |
8.47 |
0.114 |
16.34 x 109 (24) |
21,450 (24) |
188,100 (29) |
1.480 (29) |
2.938 |
552.7 (29) |
Eulipotyphla |
|
|
|
|
|
|
|
|
|
Blarina brevicauda |
0.340 (23) |
14.90 |
271.927 |
11.88 x 106 (23) |
59,280* (23) |
218 (c) |
1.000* (23) |
0.821 |
0.179* (23) |
Condylura cristata |
0.802 (23) |
10.32 |
106.832 |
17.25 x 106 (23) |
38,780* (23) |
363 (c) |
1.924* (23) |
1.072 |
0.389* (23) |
Erinaceus europaeus |
3.230 (15) |
13.96 |
29.221 |
33.53 x 106 (b) |
27,000 (49) |
924 (15) |
2.214 (49) |
1.047 |
0.967 (15) |
Scalopus aquaticus |
0.999 (23) |
8.45 |
168.291 |
28.68 x 106 (23) |
60,252* (23) |
357 (c) |
1.296* (23) |
1.070 |
0.382* (23) |
Glires |
|
|
|
|
|
|
|
|
|
Cavia porcellus |
3.656 (26) |
9.37 |
20.729 |
43.51 x 106 (26) |
22,222 (26) |
1,072 (26) |
2.606 (26) |
1.827 |
1.959 (26) |
Mesocricetus auratus |
0.965 (18) |
14.98 |
98.985 |
17.14 x 106 (18) |
39,099* (18) |
395 (c) |
2.507 (18) |
1.129 |
0.446* (18) |
Mus musculus |
0.402 (26) |
11.60 |
46.316 |
13.69 x 106 (18) |
122,232 (26) |
296 (4) |
0.870 (26) |
0.724 |
0.214 (26) |
Oryctolagus cuniculus |
7.100 (15) |
9.55 |
31.739 |
71.45 x 106 (21) |
43,800 (48) |
1,380 (15) |
3.566 |
n.a. |
n.a. |
Rattus norvegicus |
1.724 (26) |
12.27 |
49.685 |
31.02 x 106 (18) |
35,330 (26) |
711 (4) |
1.497 (26) |
1.212 |
0.862 (26) |
Afrotheria |
|
|
|
|
|
|
|
|
|
Dendrohyrax sp. |
3.328 (27) |
5.40 |
6.308 |
98.97 x 106 (27) |
12,709 (27) |
3,791 (27) |
1.426 (27) |
1.598 |
6.058 (27) |
Loxodonta Africana |
4,618 (22) |
3.30 |
0.007 |
5.59 x 109 (22) |
3,661 (22) |
514,134 (22) |
10.628 (22) |
2.633 |
1,353.9 (22) |
Procavia sp. |
4.317 (27) |
5.45 |
4.920 |
197.92 x 106 (27) |
20,794 (27) |
4,226 (27) |
1.241 (27) |
1.482 |
6.263 (27) |
Artiodactyla |
|
|
|
|
|
|
|
|
|
Bos taurus |
486 (15) |
3.19 |
0.123 |
1.34 x 109 (a) |
13,000 (48) |
105,500 (15) |
4.085 (48) |
2.142 |
226.0 (15) |
Giraffa camelopardalis |
537 (28) |
3.44 |
0.073 |
1.73 x 109 (28) |
5,882 (28) |
80,256 (28) |
7.763 (28) |
2.394 |
192.1 (28) |
Sus scrofa |
64.180 (28) |
8.20 |
0.559 |
307.08 x 106 (28) |
7,375 (28) |
13,188 (28) |
8.543 (28) |
1.336 (28) |
17.614 (28) |
Scandentia |
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Tupaia sp. |
3.040 (15) |
15.84 |
29.457 |
60.39 x 106 (19) |
38,000 (49) |
1,290 (15) |
1.511 (20) |
0.798 |
1.030 (20) |
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Values refer to both hemispheres together. Daily sleep hours from (7). When more than one estimate was available, the value presented here is the average for the species. For the other columns, numbers in parentheses refer to references in the main text. a, value estimated from brain mass according to (28). b, value estimated from cortical mass according to (30). C, values estimated as 7.34118 x VCX0.654, according to (15). DNCX, neuronal density in the cerebral cortical grey matter, except where indicated with * (density includes the white matter), in neurons/mg (our own data) or neurons/mm3 (data taken from other authors). ACX, total surface area of the cerebral cortex, in mm2. D/A, ratio between neuronal density in the cerebral cortex (in neurons/mg) and total cortical surface area (in mm2). NCX, number of neurons in the cerebral cortex. O/N, ratio between numbers of other cells (non-neuronal cells, presumed to be mostly glial cells) and neurons in the cortical grey matter, except where indicated with * (ratio includes the white matter). T, thickness of the cortical grey matter, in mm (from VCX/ACX). MCX, mass (in g, our data) or volume (in cm3) of the cortical grey matter, except where indicated with * (mass includes white matter). n.a., not available.