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HOME > PAST ISSUE > May-June 2012 > Article Detail

FEATURE ARTICLE

Plenty of Room at the Bottom?

Tiny animals solve problems of housing and maintaining oversized brains, shedding new light on nervous-system evolution

William G. Eberhard, William T. Wcislo

The Price of Brain Upkeep

Energetically, the brain is a gas-guzzler, as neural tissue is more expensive to run than most other tissues. Humans, for example, have brains that account for slightly more than 2 percent of our biomass, but they burn up more than 15 percent of our basal metabolic energy. In addition, the density of information processing is greater in a smaller brain when it is performing the same operations as a larger brain and is thus more costly on a unit basis. These differences imply that the strength of natural selection for energetic efficiency may be more intense in small than in large species, especially within a given grade. They also raise the question of how tiny animals pay these high energetic costs.

2012-05EberhardF5.jpgClick to Enlarge ImageWith respect to information processing, animals might adopt several non-exclusive strategies to reduce costs. One, the size limitation option, is to reduce behavioral capacities and thus reduce the amount of neural tissue needed to sustain behavior. Another is the oversized brain option, which involves maintaining behavioral capacities and bearing the high metabolic costs of an enlarged central nervous system. And then there is the economy-of-design option, or modifying the properties of neurons and neural networks to increase behavioral capability per unit of nervous tissue. The last option could allow smaller animals to produce comparable behavior without investing in large nervous systems.

There are several ways that animals might achieve economy of design and thus economize on the energy budgets of their brains. All animals have sensory receptors that are tuned to specific inputs to improve their efficiency. Matched filters take advantage of mechanical properties of sensors and stimuli to filter sensory input without expending energy to do so, which reduces processing expenses at the receptor and at higher central nervous system levels. Many insects, for example, are highly sensitive to polarized light, a trait associated with the physical alignment of rhodopsin molecules in the microvillar membranes of photoreceptors. There are numerous other possible opportunities to reduce central nervous system costs, such as a heavier reliance on analog transmission and graded depolarizations, which work at small distances and are energetically more efficient than the action potentials that many other animals use for communication among neurons. Another example includes the use of the same neurons for multiple tasks, such as both sensory and motor functions, as is common in nematodes. Neuromodulation may be used more frequently by small animals. That involves altering the effects of a neuronal circuit by exposing it to different chemical environments, producing different behaviors. Nematodes frequently use muscle plates that allow a single synaptic process to stimulate multiple muscles. Still other strategies include the indirect control of cilia through muscles; a reduction in the relative numbers of interneurons, which transmit signals from one neuron to another as opposed to sensory and motor neurons; and the rearrangement of neuron positions and connections in order to minimize the total length of axons and dendrites. That last design is analogous to an architect holding down building costs by minimizing the length of wire needed to provide electricity throughout a house. The nervous system of the nematode Caenorhabditis elegans has been analyzed with respect to an optimal design in this save-wire aspect. The trend toward greater fusion of different ganglia in the central nervous system of minute insects may also be related to this type of efficiency. The relative frequencies of such design features in large versus small animals are not known.

2012-05EberhardF6.jpgClick to Enlarge ImageOther possibly important differences in small nervous systems involve the neurons themselves. In at least some groups, the dendrites of smaller neurons are themselves smaller and said to be less complex. Nearly 100 years ago, insect neuroanatomist Santiago Ramón y Cajal produced pioneering—and beautiful—studies of the nervous systems of insects. He found insect neurons to be more elaborate than those of vertebrates, and likened the neuroanatomy of an insect to a “fine pocket watch,” as opposed to the “rough grandfather clock” neuroanatomy of a vertebrate. In general, the functional significance of these neuroanatomical differences is not well understood, but we expect that they represent promising starting points for future research.

Design economies could also occur at the behavioral level but are even less studied. Robotic engineers incorporate behavioral design features to minimize the input needed to generate information about the external world in order to achieve desired outcomes. A rigid hierarchy of relatively simple behavioral subroutines can facilitate goal-directed behavior if subroutines are serially ordered to maximize desired motor output per bit of sensory input. For instance, grasping a randomly positioned object is a difficult task that requires a series of visual-to-motor transformations. In robots this task is rendered easier computationally if a robot executes a subroutine to turn and face the object, triggering a second subroutine to move to a specified distance from it. Grasping it from a standard distance and direction simplifies the task. The possibility that small animals are more likely to use such behavioral designs has, to our knowledge, never been checked.








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