Olfactory lateralization in non-human mammals: a mini-review

Authors

  • Ekaterina Berezina Department of Vertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-1792-6876
  • Andrey Giljov Department of Vertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-7533-1600
  • Karina Karenina Department of Vertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0001-8200-6876

DOI:

https://doi.org/10.21638/spbu03.2022.105

Abstract

The asymmetric use of nostrils and few contralateral projections in olfactory neural pathways allow us to suppose the dominance of one hemisphere in the processing of various odours in non-human mammals. Although olfaction is the most important sensory domain for many mammals, lateralization of this sense is poorly studied in this group of animals, and the existing limited knowledge is based on experiments on laboratory and domestic mammals. Here we review the most important studies in this developing field, with an emphasis on the methods used. Most of the recent studies indicate the dominance of the right hemisphere in the processing of social and aversive odours and analysis of familiarity of the olfactory stimuli. Dominance of the left hemisphere was found only in a form of a slight trend in the perception of food odour. Almost all existing results on olfactory lateralization are in line with the well-studied patterns of visual lateralization. However, further focused investigations are needed to confirm this consistency. Studies on a wider range of species and stimuli will help to get a better understanding of the relative hemispheric roles in olfactory perception.

Keywords:

olfactory lateralization, nostril use, sensory lateralization, brain asymmetry, mammals

Downloads

Download data is not yet available.
 

References

Anfora, G., Frasnelli, E., Maccagnani, B., Rogers, L. J., and Vallortigara, G. 2010. Behavioural and electrophysiological lateralization in a social (Apis mellifera) but not in a nonsocial (Osmia cornuta) species of bee. Behavioural Brain Research 206(2):236–239. https://doi.org/10.1016/j.bbr.2009.09.023

Anisman, H., Hayley, S., Kelly, O., Borowski, T., and Merali, Z. 2001. Psychogenic, neurogenic, and systemic stressor effects on plasma corticosterone and behavior: Mouse strain-dependent outcomes. Behavioral Neuroscience 115(2):443–454. https://doi.org/10.1037/0735-7044.115.2.443

Austin, N. P. and Rogers, L. J. 2012. Limb preferences and lateralization of aggression, reactivity and vigilance in feral horses, Equus caballus. Animal Behaviour 83(1):239–247. https://doi.org/10.1016/j.anbehav.2011.10.033

Berezina, E., Gilev, A., and Karenina, K. 2021. Approaches to studying sensory laterality in saigas: experiments in the wild. Saiga News 26:28–30.

Bonati, B., Csermely, D., and Sovrano, V. A. 2013. Looking at a predator with the left or right eye: Asymmetry of response in lizards. Laterality 18(3):329–339. https://doi.org/10.1080/1357650X.2012.673623

Braccini, S. N., Lambeth, S. P., Schapiro, S. J., and Fitch, W. T. 2012. Eye preferences in captive chimpanzees. Animal Cognition 15(5):971–978. https://doi.org/10.1007/s10071-012-0523-9

Brancucci, A., Lucci, G., Mazzatenta, A., and Tommasi, L. 2008. Asymmetries of the human social brain in the visual, auditory and chemical modalities. Philosophical Transactions of the Royal Society B: Biological Sciences 364(1519):895–914. https://doi.org/10.1098/RSTB.2008.0279

Brown, N. J. and Reimchen, T. E. 2019. Right nostril biases to experimental scents in Canis familiaris. Laterality 25(1):43–52. https://doi.org/10.1080/1357650X.2019.1614942

Burne, T. H. J. and Rogers, L. J. 2002. Chemosensory input and lateralization of brain function in the domestic chick. Behavioural Brain Research 133(2):293–300. https://doi.org/10.1016/S0166-4328(02)00009-8

Carlson, J. N., Fitzgerald, L. W., Keller, R. W., and Glick, S. D. 1991. Side and region dependent changes in dopamine activation with various durations of restraint stress. Brain Research 550(2):313–318. https://doi.org/10.1016/0006-8993(91)91333-V

Cohen, Y., Putrino, D., and Wilson, D. A. 2015. Dynamic cortical lateralization during olfactory discrimination learning. Journal of Physiology 593(7):1701–1714. https://doi.org/10.1113/jphysiol.2014.288381

Cohen, Y. and Wilson, D. A. 2017. Task-correlated cortical asymmetry and intra- and inter-hemispheric separation. Scientific Reports 7(1):1–9. https://doi.org/10.1038/s41598-017-15109-x

Craig, A. D. 2005. Forebrain emotional asymmetry: a neuroanatomical basis? Trends in Cognitive Sciences 9(12):566–571. https://doi.org/10.1016/J.TICS.2005.10.005

Dantzer, R., Tazi, A., and Bluthé, R. M. 1990. Cerebral lateralization of olfactory-mediated affective processes in rats. Behavioural Brain Research 40(1):53–60. https://doi.org/10.1016/0166-4328(90)90042-D

de Boyer Des Roches, A., Richard-Yris, M.-A., Henry, S., Ezzaouïa, M., and Hausberger, M. 2008. Laterality and emotions: visual laterality in the domestic horse (Equus caballus) differs with objects’ emotional value. Physiology and Behavior 94(3):487–490. https://doi.org/10.1016/j.physbeh.2008.03.002

de Castro, F. 2009. Wiring olfaction: the cellular and molecular mechanisms that guide the development of synaptic connections from the nose to the cortex. Frontiers in Neuroscience 3:52. https://doi.org/10.3389/neuro.22.004.2009

Frasnelli, E., Anfora, G., Trona, F., Tessarolo, F., and Vallortigara, G. 2010. Morpho-functional asymmetry of the olfactory receptors of the honeybee (Apis mellifera). Behavioural Brain Research 209(2):221–225. https://doi.org/10.1016/j.bbr.2010.01.046

Gagliardo, A., Filannino, C., Ioalè, P., Pecchia, T., Wikelski, M., and Vallortigara, G. 2011. Olfactory lateralization in homing pigeons: a GPS study on birds released with unilateral olfactory inputs. Journal of Experimental Biology 214(4):593–598. https://doi.org/10.1242/JEB.049510

Giljov, A., de Silva, S., and Karenina, K. 2017. Context-dependent lateralization of trunk movements in wild Asian elephants. Biological Communications 62(2):82–92. https://doi.org/10.21638/11701/spbu03.2017.204

Güntürkün, O., Ströckens, F., and Ocklenburg, S. 2020. Brain lateralization: a comparative perspective. Physiological Reviews 100(3):1019–1063. https://doi.org/10.1152/PHYSREV.00006.2019

Hardee, J. E., Thompson, J. C., and Puce, A. 2008. The left amygdala knows fear: laterality in the amygdala response to fearful eyes. Social Cognitive and Affective Neuroscience 3(1):47–54. https://doi.org/10.1093/SCAN/NSN001

Hausberger, M., Henry, L., Rethoré, B., Pougnault, L., Kremers, D., Rössler, C., Aubry, C., Cousillas, H., Boye, M., and Lemasson, A. 2021. When perceptual laterality vanishes with curiosity: A study in dolphins and starlings. Laterality 26(1–2):238–259. https://doi.org/10.1080/1357650X.2021.1890758

Hook-Costigan, M. A. and Rogers, L. J. 1998. Eye preferences in common marmosets (Callithrix jacchus): influence of age, stimulus, and hand preference. Laterality: Asymmetries of Body, Brain and Cognition 3(2):109–130. https://doi.org/10.1080/713754297

Jozet-Alves, C., Percelay, S., and Bouet, V. 2019. Olfactory laterality is valence-dependent in mice. Symmetry 11(9):1129. https://doi.org/10.3390/sym11091129

Kappel, S., Mendl, M. T., Barrett, D. C., Murrell, J. C., and Whay, H. R. 2017. Lateralized behaviour as indicator of affective state in dairy cows. PloS ONE 12(9):e0184933. https://doi.org/10.1371/journal.pone.0184933

Karenina, K., Giljov, A., Ingram, J., Rowntree, V. J., and Malashichev, Y. 2017. Lateralization of mother-infant interactions in a diverse range of mammal species. Nature Ecology and Evolution 1:0030. https://doi.org/10.1038/s41559-016-0030

Knaden, M. and Hansson, B. S. 2014. Mapping odor valence in the brain of flies and mice. Current Opinion in Neurobiology 24(1):34–38. https://doi.org/10.1016/J.CONB.2013.08.010

Kruper, D. C., Boyle, B. E., and Patton, R. A. 1966. Eye and hand preference in rhesus monkeys Macaca mulatta. Psychonomic Science 5(7):277–278. https://doi.org/10.3758/BF03328393

Larose, C., Richard-Yris, M.-A., Hausberger, M., and Rogers, L. J. 2006. Laterality of horses associated with emotionality in novel situations. Laterality: Asymmetries of Body, Brain and Cognition 11(4):355–367. https://doi.org/10.1080/13576500600624221

Litaudon, P., Bouillot, C., Zimmer, L., Costes, N., and Ravel, N. 2017. Activity in the rat olfactory cortex is correlated with behavioral response to odor: a microPET study. Brain Structure and Function 222(1):577–586. https://doi.org/10.1007/s00429-016-1235-8

Martín, J., López, P., Bonati, B., and Csermely, D. 2010. Lateralization when monitoring predators in the wild: a left eye control in the common wall lizard (Podarcis muralis). Ethology 116(12):1226–1233. https://doi.org/10.1111/j.1439-0310.2010.01836.x

McGreevy, P. D. and Rogers, L. J. 2005. Motor and sensory laterality in thoroughbred horses. Applied Animal Behaviour Science 92(4):337–352. https://doi.org/10.1016/j.applanim.2004.11.012

Morris, J. S., Frith, C. D., Perrett, D. I., Rowland, D., Young, A. W., Calder, A. J., and Dolan, R. J. 1996. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383(6603):812–815. https://doi.org/10.1038/383812A0

Najt, P., Bayer, U., and Hausmann, M. 2013. Models of hemispheric specialization in facial emotion perception — a reevaluation. Emotion 13(1):159–167. https://doi.org/10.1037/a0029723

Nielsen, B. L., Jezierski, T., Bolhuis, J. E., Amo, L., Rosell, F., Oostindjer, M., Christensen, J. W., McKeegan, D., Wells, D. L., and Hepper, P. 2015. Olfaction: an overlooked sensory modality in applied ethology and animal welfare. Frontiers in Veterinary Science 2:69. https://doi.org/10.3389/FVETS.2015.00069

Olds, J. L., Bhalla, U. S., McPhie, D. L., Lester, D. S., Bower, J. M., and Alkon, D. L. 1994. Lateralization of membraneassociated protein kinase C in rat piriform cortex: specific to operant training cues in the olfactory modality. Behavioural Brain Research 61(1):37–46. https://doi.org/10.1016/0166-4328(94)90006-X

Robins, A. and Rogers, L. J. 2006. Complementary and lateralized forms of processing in Bufo marinus for novel and familiar prey. Neurobiology of Learning and Memory 86(2):214–227. https://doi.org/10.1016/j.nlm.2006.03.002

Rogers, L. and Andrew, R. 2002. Comparative vertebrate lateralization. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511546372

Rogers, L. J. and Anson, J. M. 1979. Lateralisation of function in the chicken fore-brain. Pharmacology Biochemistry and Behavior 10(5):679–686. https://doi.org/10.1016/0091-3057(79)90320-4

Rogers, L., Vallortigara, G., and Andrew, R. 2013. Divided brains: the biology and behaviour of brain asymmetries. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511793899

Rogers, L. J., Ward, J. P., and Stanford, D. 1994. Eye dominance in the small-eared bushbaby, Otolemur garnettii. Neuropsychologia 32(2):257–264. https://doi.org/10.1016/0028-3932(94)90011-6

Rogers, L. J., Zappia, J. V., and Bullock, S. P. 1985. Testosterone and eye-brain asymmetry for copulation in chickens. Experientia 41(11):1447–1449. https://doi.org/10.1007/BF01950028

Royet, J.-P. and Plailly, J. 2004. Lateralization of olfactory processes. Chemical Senses 29(8):731–745. https://doi.org/10.1093/CHEMSE/BJH067

Shipley, M. T. and Ennis, M. 1996. Functional organization of olfactory system. Journal of Neurobiology 30(1):123–176. https://doi.org/10.1002/(SICI)1097-4695(199605)30:1<123::AID-NEU11>3.0.CO;2-N

Siniscalchi, M. 2017. Olfactory lateralization; pp. 103–120 in Rogers, L. J. and Vallortigara, G. (eds), Lateralized Brain Functions: Methods in Human and Non-Human Species. Springer Science + Business Media LLC. https://doi.org/10.1007/978-1-4939-6725-4_4

Siniscalchi, M., d’Ingeo, S., and Quaranta, A. 2016. The dog nose “KNOWS” fear: Asymmetric nostril use during sniffing at canine and human emotional stimuli. Behavioural Brain Research 304:34–41. https://doi.org/10.1016/J.BBR.2016.02.011

Siniscalchi, M., Padalino, B., Aubé, L., and Quaranta, A. 2015. Right-nostril use during sniffing at arousing stimuli produces higher cardiac activity in jumper horses. Laterality 20(4):483–500. https://doi.org/10.1080/1357650X.2015.1005629

Siniscalchi, M., Sasso, R., Pepe, A. M., Dimatteo, S., Vallortigara, G., and Quaranta, A. 2011. Sniffing with the right nostril: lateralization of response to odour stimuli by dogs. Animal Behaviour 82(2):399–404. https://doi.org/10.1016/j.anbehav.2011.05.020

Vallortigara, G. and Andrew, R. J. 1994. Olfactory lateralization in the chick. Neuropsychologia 32(4):417–423. https://doi.org/10.1016/0028-3932(94)90087-6

Vallortigara, G., Chiandetti, C., and Sovrano, V. A. 2011. Brain asymmetry (animal). Wiley Interdisciplinary Reviews: Cognitive Science 2(2):146–157. https://doi.org/10.1002/wcs.100

Vallortigara, G., Rogers, L. J., Bisazza, A., Lippolis, G., and Robins, A. 1998. Complementary right and left hemifield use for predatory and agonistic behaviour in toads. NeuroReport 9(14):3341–3344. https://doi.org/10.1097/00001756-199810050-00035

Downloads

Published

2022-05-04

How to Cite

Berezina, E., Giljov, A., & Karenina, K. (2022). Olfactory lateralization in non-human mammals: a mini-review. Biological Communications, 67(1), 49–56. https://doi.org/10.21638/spbu03.2022.105

Issue

Section

Review communications

Categories