This leads us to the final issue, namely the question of how brain evolution has occurred. There has been considerable debate in the recent literature as to whether developmental constraints have forced a significant degree of uniformity on brain structure, i.e. species differences in the volume of particular brain units merely reflect species differences in total brain volume (Finlay & Darlington 1995
; Finlay et al. 2001
; de Winter & Oxnard 2001
), or whether there has been mosaic evolution whereby some brain units have enlarged more rapidly than others (Barton & Harvey 2000
). There can be no doubt about the fact that there must be both developmental (Martin 1981
) and energetic (Aiello & Wheeler 1995
) constraints on final brain size; indeed, we have demonstrated above that such constraints do exist. However, the real issue here is whether brain units enlarge proportionally as total brain volume enlarges (Finlay et al. 2001
), or do so disproportionately as a function of specific selection pressures (Barton & Harvey 2000
). There is currently no real agreement on this.
One reason why there may be proportional convergence in brain component volumes is that higher order representations of sensory systems within the brain seem to be organized on a direct functional basis: upstream systems seem to be volumetrically correlated with their input systems (Stevens 2001
). Thus, increasing convergence in proportional volumes may reflect increasing integration of units from different functional groupings as a result of increased sharing of information. In support of this it is known that, in the primate brain, there are direct axonal links from subcortical areas like the amygdala and the cerebellum to the frontal lobe of the neocortex, whereas this is much less extensively the case in carnivores (Fuster 1988
). Using a different approach, we were here able to confirm that the cerebellum, at least, is unrelated to social group size when total brain and neocortex volumes are partialled out. Interestingly, cerebellum volume correlates negatively with those life-history variables that correlate positively with neocortex volume, suggesting that not all brain units are under the same linked selection regime (see also Barton & Harvey 2000
A more general issue of some importance concerns the overall pattern of brain evolution. Finlay & Darlington (1995)
have pointed out that, although brain units scale very tightly with each other, the scaling coefficient is not always unity. Of particular significance in the present context is the fact that, across mammals, the scaling coefficient for neocortex volume relative to the brain as a whole is significantly higher than unity: in fact, the scaling relationship against the whole brain ranges from 1.103 for neocortex as a whole, to 1.115 for the frontal lobe (Semendeferi et al. 1997
), indicating that the neocortex in general, and the frontal lobe in particular, have increased disproportionately during the course of primate brain evolution. Large-brained primates like apes and humans have disproportionately large frontal lobes—even though, as Semendeferi et al. (1997)
pointed out, they do not deviate from the general primate allometric scaling relationship. This is significant because the frontal lobe is widely understood to be primarily responsible both for integration across sensory and association units and for those cognitive processes generally referred to as ‘executive functions’ (Kolb & Wishaw 1996
One reason for the steep positive allometric scaling of the frontal lobe is the fact that the brain evolves (and, indeed, develops and myelinates; Gogtay et al. 2004
) from back (the visual areas) to front (the executive areas). Thus, when brain evolution occurs, it mainly involves adding more frontal cortex rather than increasing all brain units proportionately. Given that visual acuity is limited only by retinal area and not by body size or total brain size, there is limited value in adding more visual cortex (located mainly in the occipital lobe at the back of the brain) than is minimally necessary to map the inputs from the retina. This effectively means that there is increasing frontal lobe volume available for executive-type functions. Dunbar (2003)
showed that, in primates, the area of the primary visual cortex (commonly known as V1) is linearly (and tightly) related to the both volume of the visual pathway (lateral geniculate nucleus and the visual tract) and the volume of the orbit (the main factor determining retinal area). shows the consequences of this; the volume of the primary visual cortex (V1) quickly reaches an asymptotic value as a function of total brain volume, but the volume of the rest of the neocortex (non-V1 cortex) increases dramatically. Unfortunately, with Stephan's database, we are unable to partition the neocortex down into smaller units, but the volumetric analyses provided by Semendeferi et al. (1997)
for frontal lobe and by Fuster (1988)
for prefrontal cortex imply even steeper relationships for these more frontal units that are specifically involved in cognitive executive functions. Since it is these rather than the visual areas per se
that are likely to be responsible for the social brain effect, it may be no accident that increasing brain size correlates with increasing social skills (and hence group size).
Figure 4 Volumes of primary visual cortex (V1) and rest of neocortex (non-V1) plotted against total brain volume for primates. Source: data from Stephan et al. (1981).