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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.

This article is unfortunately not freely available, but email the author for a PDF here

 

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

 

 

 

 

 

 

 

 

 

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)

 

 

 

 

 

 

 

 

 

 

 

 

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.