Gray mouse lemurs showed individual hand preferences as well as
sex-specific orientation asymmetries related to emotional valence of
conspecific communication calls. Thus, males, but not females, exhibit
a right ear-left hemispheric advantage toward conspecific communication
calls of negative emotional valence. Hand preference of subjects was
not related to orientation asymmetries.
Gray mouse lemurs, like humans and non-human animals (e.g. [8,65]),
showed individual hand preferences. However, we did not find hand
preferences at population level that coincided with results of Dodson
et al [54] based on a lower sample size. Various studies of hand usage revealed task specific differences [25,30,66].
They hypothesized that low-level tasks such as food reaching in
contrast to more complex high-level tasks such as bimanual manipulation
are too simple to show handedness at population level. During insect
capturing, mouse lemurs have to catch moving insects that are too large
to handle with only one hand. Therefore they capture insects using
their mouth and one or both hands (unpublished results), which suggest
that they lack fine motor control. In our task, we forced subjects to
use one hand instead of the mouth, which made our task difficult for
them. We assume therefore that the forced food-grasping paradigm is not
a task that is too simple for these animals. Altogether, our results
suggest that brain asymmetries for the control of hand usage are
already present in an early primate. Handedness at population level
evolved later within the primate order. Further, the occurrence of
handedness at population level in some rodents, birds and amphibians
(e.g. [20,21,27,28]) suggests a convergent evolution in different taxonomic lineages.
The results for the hemispheric advantage in communication sound
perception are consistent and cannot be explained by a small sample
size, individual head turn preference or position of nest box and tail.
In comparison with other captive settings studying lateralization of
auditory perception (e.g. [36,48])
we used a large sample. We can rule out that subjects showed a general
orientation asymmetry. Analysing the head turn direction of each
subject across all stimuli revealed that only 6 of the 38 subjects
showed a significant individual side preference over all stimuli (two
male and four females; binomial test: p ≤ 0.039; all other subjects p ≥
0.065). We can further exclude that subjects' head turns were
influenced by the position of the tail, which is important for balance
in arboreal species, or the nest box. We found no differences in head
turn direction when the tail was bent to the right or left side of the
subject, or the nest box was attached on the right or the left side of
the cage.
In humans, non-human primates and non-primate animals, a left
hemispheric advantage for perception of communication sounds was
described (humans [1], raptor [34], starlings [35], sea lions [36], mice [37-39], Japanese macaques [40-43], rhesus monkeys [44-47]). Mouse lemurs showed a different pattern of hemispheric advantage as revealed for anthropoid primates (Japanese monkeys [40-42], rhesus monkeys [44-46], vervet monkey [48]).
However, in anthropoid primates the direction of hemispheric
asymmetries is plastic. Thus, Japanese monkeys and rhesus monkeys
showed a left hemispheric advantage and vervet monkeys a right
hemispheric advantage for communication sound perception. Altogether,
results in non-human primates revealed three patterns of hemispheric
asymmetries, a left hemispheric advantage for the perception of
communication sounds of negative emotional valence in males of an early
primate, a left hemispheric advantage in rhesus monkeys [44-46] and a right hemispheric advantage in vervet monkeys for communication sound processing of varying emotional valence [48].
Furthermore, non-primate animals demonstrated a right ear – left
hemispheric advantage for conspecific communication sounds (raptors [34], starlings [35], mice [37-39], sea lions [36]).
Altogether, it seems that lateralization of auditory perception at
population level evolved gradually in primates. Furthermore, findings
in sea lions, mice and birds favor the view of a convergent evolution
of hemispheric asymmetries in primate and non-primate animals. This
suggests a more complex evolutionary scenario of hemispheric
specializations in language processing than previously assumed.
Focussing on males, we found that conspecific communication calls of
negative valence cause a right head turn bias whereas the communication
calls of positive valence did not cause any bias. This suggests that
lateralisation in communication sound perception is linked to emotional
valence as shown for humans (e.g. [67]).
However, recent studies in humans and rhesus monkeys hypothesized that
hemispheric advantages for communication sound processing are more
affected by specific changes in spectral and temporal cues of the
acoustic stream [1,68,69].
Thus, in humans, the left hemisphere seems to be specialized to the
analyses of rapid temporal changes that speech perception requires
whereas the right hemisphere is specialized to the analyses of
fine-grained spectral changes that music perception requires [1,69].
According to the calls of the mouse lemurs whistles and tsaks are very
short calls with a rapid repetition rate whereas the trills are long
calls with a complex frequency structure. Further studies will explore
to what extent these cues can explain orientation asymmetries in mouse
lemurs.
In humans, men are more lateralized than women [2].
In mouse lemurs we found a right ear-left hemispheric advantage toward
conspecific communication sounds of negative valence for males, but not
for females or the whole population. This may suggest that as in
humans, mouse lemur males are more lateralized than females. In humans,
men and women differ in the performance of various linguistic and
emotional tasks [7,70].
Thus, females perform better than males. Thereby, imaging studies
revealed that during phonological processing, in men the left
hemisphere is activated whereas in women both hemispheres are activated
[71,72].
Further, sex differences occurred in the anatomy of language processing
areas as well as in the interhemispheric connection, the corpus
callosum [73]. The corpus callosum is larger in women than in men, suggesting more fibres that connect the two hemispheres. Kimura [7]
suggested that either the functions of the two hemispheres are not
sharply separated in women or that the larger commissural connections
reduce the hemispheric differences. Such sex-specific anatomical
differences in the corpus callosum were also found in prosimians, rats,
dogs and apes, but not in New and Old World monkeys [74-77].
As in humans the corpus callosum is larger in females than in males of
prosimians. Sex hormones are suggested to trigger these sex specific
differences [2].
Based on this, we suggest that mouse lemur females did not exhibit an
orientation bias because the strong commissural connections reduce
lateralization by analysing communication sounds in both hemispheres.
It is suggested that human language evolved from manual and facial gestures rather than from animal vocal communication [4]. This is supported by the fact that right-handedness is related to left hemispheric dominance of speech processing [4].
However, in mouse lemurs we did not find a relation between individual
hand preference and ear-hemispheric advantages toward conspecific
communication sounds. Such a relationship is also lacking in non-human
primates, who do show handedness at population level [29,44]. Thus, rhesus monkeys demonstrated a right-hand preference at population level in a coordinated bimanual task [29], but they did not show a relation between individual handedness and head turn direction [44].
Altogether, these data render support for the hypothesis that hand
preference and lateralization of communication sound perception evolved
independently from each other in primates [33].
Answers to all your Biology Questions
