Evolutionary Changes in the Olfactory
Projection Neuron Pathways of
Eumalacostracan Crustaceans
JEREMY M. SULLIVAN
*
AND BARBARA S. BELTZ
Department of Biological Sciences, Wellesley College, Wellesley, Massachusetts 02481
ABSTRACT
Output from the olfactory lobe (primary olfactory center) of eumalacostracan crustaceans
is transmitted to the medulla terminalis (MT) and hemiellipsoid body (HB) in the lateral
protocerebrum (higher order center) by a large population of projection neurons. In eureptan-
tian crustaceans (lobsters, crayfish, and crabs), these projection neurons also form the output
pathway from an additional neuropil, the accessory lobe (higher order center), which appears
to have arisen de novo in these animals. In a previous study of lobsters and crayfish we
showed that whereas projection neurons innervating the olfactory lobe project primarily to
the MT, those innervating the accessory lobe project exclusively to the HB (Sullivan and Beltz
[2001a] J. Comp. Neurol. 441:9 –22). In the present study, we used focal dye injections to
examine the olfactory projection neuron pathways of representatives of four eumalacostracan
taxa (Stomatopoda, Dendrobranchiata, Caridea, and Stenopodidea) that diverged from the
eureptantian line prior to the appearance of the accessory lobe. These experiments were
undertaken both to examine the evolution of the olfactory pathway in the Eumalacostraca
and to provide insights into the changes in this pathway that accompanied the appearance of
the accessory lobe. The innervation patterns of the olfactory projection neurons of the species
examined were found to differ markedly, varying from that observed in the most basal taxon
examined (Stomatopoda), in which the neurons primarily project to the MT, to those observed
in the two highest taxa examined (Caridea and Stenopodidea), in which they primarily target
the HB. These results suggest that substantial changes in the relative importance of the MT
and HB within the olfactory pathway have occurred during the evolution of the Eumalaco-
straca. J. Comp. Neurol. 470:25–38, 2004. © 2004 Wiley-Liss, Inc.
Indexing terms: accessory lobe; olfactory pathway; olfactory projection neuron
Olfactory cues serve important functions in the biology
of eumalacostracan crustaceans, playing central roles in
feeding, mating, and territorial behaviors. Correspond-
ingly, the primary olfactory neuropil, the olfactory lobe, is
one of the most prominent neuropils in the brains of these
animals. The lateral protocerebrum of eumalacostracan
crustaceans has long been recognized as another impor-
tant brain center in the olfactory pathway, as it is the
target of the output tract from the olfactory lobe (Fig. 1;
Hanstro ¨m, 1924, 1925, 1931, 1947; Blaustein et al., 1988;
Sandeman et al., 1993; Sullivan and Beltz 2001a, b). The
importance of the lateral protocerebrum in the olfactory
pathway has also been underlined by ablation experi-
ments suggesting that this region is involved in discrimi-
nating food from nonfood items and in the control of feed-
ing behaviors (Maynard and Dingle, 1963; Maynard and
Yager, 1968; Maynard and Sallee, 1970; Hazlett, 1971). In
addition to having strong connections with the olfactory
lobe, the lateral protocerebrum also has connections with
the optic neuropils (Hanstro ¨m, 1925; Mellon, 2000; Sulli-
van and Beltz, 2001b) and is therefore thought to be an
associative brain center.
The lateral protocerebrum is located proximal to the
optic neuropils (lamina ganglionaris, medulla externa,
and medulla interna) and is comprised of two main re-
gions: the medulla terminalis and the hemiellipsoid body
Grant sponsor: National Science Foundation; Grant number: IBN
0091092.
*Correspondence to: Jeremy Sullivan, Department of Biological Sci-
ences, Wellesley College, Wellesley, MA 02481.
E-mail: jsulliv2@wellesley.edu
Received 8 September 2003; Revised 21 October 2003; 24 October 2003
DOI 10.1002/cne.11026
Published online the week of January 19, 2004 in Wiley InterScience
(www.interscience.wiley.com).
THE JOURNAL OF COMPARATIVE NEUROLOGY 470:25–38 (2004)
© 2004 WILEY-LISS, INC.