Biomedical Engineering Reference
In-Depth Information
Appendix A Column: History of a Classical Conditioning
of PER in Honeybees
Long before research on PER conditioning started, it was well known that the PER
could be elicited by stimulating gustatory organs like the antennae, tarsi, or mouth-
parts with sugar solution. The PER had thus been detected in bees (Frings
1944
;
Frings and Frings
1949
), fl ies (Minnich
1926
), and butterfl ies (Minnich
1921
),
among others. Later, a Japanese researcher who had worked with Karl von Frisch,
Masutaro Kuwabara, realized that this appetitive refl ex could be conditioned using
visual stimuli as CS and sucrose solution delivered to the tarsi as US (Kuwabara
1957
). However, Kuwabara's work did not receive broad attention as shown by the
fact that almost 50 years had to pass before other researchers published results on
honeybee visual conditioning using Kuwabara's method (Hori et al.
2006
; Hori
et al.
2007
). For this conditioning to work, Kuwabara and Hori et al. had to cut the
bees' antennae. The low acquisition rates observed in antennae-deprived bees
despite long conditioning procedures (Hori et al.
2006
; Hori et al.
2007
) may be
related to this fact. It has been recently shown that antennae deprivation reduces
sucrose responsiveness when measured through tarsal stimulation (de Brito Sanchez
et al.
2008
), probably leading to a reduction of US value and of acquisition and
retention performances.
The olfactory conditioning of PER was afterwards established by a student of
Kuwabara, Kimihisa Takeda, who reported on this procedure in 1961 (Takeda
1961
)
using odors as CS and sucrose solution as US. As was common use 50 years ago,
Takeda did not report any acquisition, retention, or extinction curves, nor did he
provide any statistical analysis of PER responses. He only presented tables with the
raw data of single bees, with very low sample sizes. Despite data paucity, lack of
statistics, absence of controls, and representative sample sizes, Takeda's work laid
down the experimental principles and the scientifi c questions that would serve as a
basis for future, more controlled research on honeybee learning and memory. He
showed for the fi rst time extinction learning (including spontaneous recovery),
stimulus generalization and discrimination, conditioned inhibition, and second-
order conditioning in the olfactory domain in honeybees. In this way he established
olfactory PER conditioning as a useful tool for the study of invertebrate learning
and memory.
References
Abel R, Rybak J, Menzel R (2001) Structure and response patterns of olfactory interneurons in the
honeybee,
Apis mellifera
. J Comp Neurol 437:363-383
Avarguès-Weber A, Deisig N, Giurfa M (2011) Visual cognition in social insects. Annu Rev
Entomol 56:423-443
Ayestaran A, Giurfa M, de Bitro Sanchez MG (2010) Toxic but drank: gustatory aversive com-
pounds induce post-ingestional malaise in harnessed honeybees. PLoS One 5:e15000.
doi:
10.1371/journal.pone.0015000
