ScienceWeek

NEUROBIOLOGY: INVERTEBRATES AND SYSTEMS NEUROBIOLOGY

The following points are made by Ralph J. Greenspan (Current Biology 2004 14:R177):

1) Various members of the invertebrate subkingdom played a pivotal role in the history of neurobiology. A short list of some of the most notable discoveries and advances that have become part of the canon would have to include: the first recording from a photoreceptor cell (horseshoe crab); the first voltage clamp of an axon (squid); the first report of presynaptic inhibition (crab); and the first report of an electrical synapse (crayfish). All of these "firsts" solved problems or identified properties that had immediate and lasting relevance to all brains, whether attached to a backbone or not.

2) Then came the "identified cell" approach, which became the mantra of invertebrate neurobiology for the next few decades [2]. The name refers to the ability to record isolated responses from individual cells and to know where to find those cells in any individual. As a means of understanding the parameters governing an individual cell's physiology or the delineation of particular circuits -- by "circuit-breaking" -- it was unequaled by anything in the vertebrate world (with the possible exception of Mauthner cell recordings in fish). And as long as the contribution of an individual neuron to a specific circuit was considered to be stable and predictable, it held sway. But as the stability and predictability of a given cell's role in its network came into question, the identified cell approach lost some of its luster. Moreover, as a strategy for understanding the large-scale interactions among many hundreds or thousands of cells -- a principal goal of mammalian neurobiology -- it was not even in the running.

3) Invertebrates have also been touted for their exotic specializations: their odd adaptations of sensory and motor systems to particular ecological niches. The courtship song of the cricket, motion detection by the fly visual system, swimming in the leech and aggressive displays in the lobster exemplify some of the most informative of these specializations. Invertebrates have not, however, been suggested as a means to unraveling mechanisms of complex function that are relevant to human cognition. Those issues have traditionally been the province of "systems neurobiology".

4) Systems neurobiology connotes a class of studies of the mammalian brain in which recordings are made during complex physiological events occurring in many hundreds or thousands of cells in the brain. Its principal aim is to crack the complexity that underlies perception, cognition and sophisticated motor output. Invertebrate brains are not part of the picture. Yet, despite this apparent incompatibility, there is an incipient discipline emerging that may well deserve the name "invertebrate systems neurobiology". Where has this nascent field come from and what are its prospects? As with all emergent fields, this one had a lone pioneer -- in this case T.H. Bullock, who has recorded EEGs from a more diverse array of species than most of us have ever eaten.(1,2,)

5) Invertebrate systems have a number of features that have provided an impetus for this new systems neurobiology. These include: surprisingly complex neural and cognitive functions in relatively small brains; the feasibility of performing single cell electrode recordings, regional optical recordings, and local field potential recordings; the coupling with a rich variety of behavioral outputs; and the advantages of smallness for defining circuitry and large-scale interactions. To the extent that such approaches can be carried out in the fruit fly Drosophila, the potential also arises for genetic manipulation to be coupled with physiology and behavior.

References:

1. Bullock, T.H. and Horridge, G.A. (1965). Structure and Function in the Nervous Systems of Invertebrates. (San Francisco: W.H. Freeman and Co.)

2. Bullock, T.H. (2003). Have brain dynamics evolved?. Neural Comput. 15, 2013-2027

Current Biology http://www.current-biology.com

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ON LEARNING AND MEMORY IN INVERTEBRATES

The following points are made by Gordon M. Shepherd (citation below):

1) The capacity to store and recall information, is a necessary component of learning. Animals as low on the evolutionary scale as the flatworms (Planaria can show classical conditioning, which implies that there is a memory mechanism present. Whether this is distributed throughout the peripheral nerves or body cells of this animal, as some of the more sensational experiments imply, is still a controversial question. In higher invertebrates and vertebrates, it is clear that memory mechanisms related to behavioral experiences depend on the brain.

2) The octopus has the largest brain among the invertebrates. It also has highly developed eyes and a highly developed tactile system in its tentacles. J.Z. Young (1907-1997) and his colleagues in London showed that the octopus can readily learn visual discrimination tasks, such as distinguishing between vertical and horizontal lines. By making ablations of different parts of the brain, they showed that visual memory is stored in the vertical lobe. Octopuses can also learn tactile discriminations with their tentacles (though they cannot learn proprioceptive discriminations). It was found that tactile memories are stored in the octopus inferior frontal and subfrontal lobes. Thus, the visual and tactile memory systems are mostly separate, though there is some overlap in the vertical lobe.

3) This separation of memory systems is more distinct than is the case in vertebrates, at least as far as is known at present. The vertical lobe of the octopus is packed with millions of very small neurons; many of these lack axons, and thus appear to form microcircuits by means of dendrodendritic interactions. Young (1978) hypothesized that these "microneurons" are crucial for memory, and that during learning they inhibit unwanted pathways, leaving others open to be used selectively in the learned task.

Adapted from: Gordon M. Shepherd: Neurobiology. 2nd Ed. Oxford University Press 1988, p.604.

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EXPERIMENTAL EVOLUTION OF LEARNING ABILITY IN FRUIT FLIES

The following points are made by F. Mery and T.J. Kawecki (Proc. Nat. Acad. Sci. 2002 99:14:274):

1) Learning ability is known to respond readily to direct artificial selection on a particular conditioned behavior (1-5). In such experiments the conditionability of the focal behavior is the sole criterion that determines whether an individual is allowed to breed. However, in natural populations learning and memory may entail fitness costs, if only because of the energy needed to maintain neuronal information and underlying structures. It remains unclear how readily learning evolves under natural selection, when its contribution to reproductive success is indirect and has to be set against its potential costs.

2) To address this issue, the authors kept populations of Drosophila melanogaster under ecological conditions expected to favor the evolution of learning ability in the context of oviposition substrate choice. The choice of a suitable oviposition substrate is an ecologically important decision with a direct impact on fitness. It may be modified by experience because in nature Drosophila females lay eggs over extended time, potentially on many different substrates, which are also fed on by the adults. They can thus assess the quality of the oviposition medium, which, together with relatively well developed associative memory, opens an opportunity for learning to contribute to Darwinian fitness.

3) In summary: The presence of genetic variation for learning ability in animals opens the way for experiments asking how and under what ecological circumstances improved learning ability should evolve. The authors report experimental evolution of learning ability in Drosophila melanogaster. The authors exposed experimental populations for 51 generations to conditions expected to favor associative learning with regard to oviposition substrate choice. Flies that learned to associate a chemical cue (quinine) with a particular substrate, and still avoided this substrate several hours after the cue had been removed, were expected to contribute more alleles to the next generation. From about generation 15 on, the experimental populations showed marked ability to avoid oviposition substrates that several hours earlier had contained the chemical cue. The improved response to conditioning was also expressed when the flies were faced with a choice of novel media. The authors demonstrate that these behavioral changes are caused by the evolution of both a higher learning rate and a better memory.

References (abridged):

1. Tryon, R. C. (1940) Yk. Natl. Soc. Stud. Educ. 39, 111-119.

2. McGuire, T. R. & Hirsch, J. (1977) Proc. Natl. Acad. Sci. USA 74, 5193-5197.

3. Brandes, C. , Frisch, B. & Menzel, R. (1988) Anim. Behav. 36, 981-985.

4. Lofdahl, K. L. , Holliday, M. & Hirsch, J. (1992) J. Comp. Psychol. 106, 172-183.

5. Reif, M. , Linsenmair, K. E. & Heisenberg, M. (2002) Anim. Behav. 63, 143-155.

Proc. Nat. Acad. Sci. http://www.pnas.org

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