Acquisition of innate odor preference depends on spontaneous and experiential activities during critical period

Animals possess an inborn ability to recognize certain odors to avoid predators, seek food, and find mates. Innate odor preference is thought to be genetically hardwired. Here we report that acquisition of innate odor recognition requires spontaneous neural activity and is influenced by sensory experience during early postnatal development. Genetic silencing of mouse olfactory sensory neurons during the critical period has little impact on odor sensitivity, discrimination, and recognition later in life. However, it abolishes innate odor preference and alters the patterns of activation in brain centers. Exposure to innately recognized odors during the critical period abolishes the associated valence in adulthood in an odor-specific manner. The changes are associated with broadened projection of olfactory sensory neurons and expression of axon guidance molecules. Thus, a delicate balance of neural activity is needed during the critical period in establishing innate odor preference and convergent axon input is required to encode innate odor valence.

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Acquisition of Innate Odor Preference Depends on Spontaneous and Experiential Activities During Critical Period

10.1101/2020.01.28.923722 ◽

2020 ◽

Cited By ~ 1

Author(s):

Qiang Qiu ◽

Yunming Wu ◽

Limei Ma ◽

Vivekanandan Ramalingam ◽

C. Ron Yu

Keyword(s):

Sensory Neurons ◽

Neural Activity ◽

Critical Period ◽

Odor Preference ◽

Early Postnatal Development ◽

Odor Recognition ◽

Cognate Receptor ◽

Spontaneous Neural Activity ◽

Specific Manner ◽

Prior Experiences

AbstractAnimals possess inborn ability to recognize certain odors, which enables them to seek food, avoid predators and find mates even in the absence of prior experiences. The establishment of innate odor preference has been thought to be genetically hardwired. Here we report that the acquisition of innate odor recognition requires spontaneous neural activity and is influenced by sensory experience during early postnatal development. Genetic silencing of mouse olfactory sensory neurons during the developmental critical period has little impact on odor sensitivity, odor discrimination and recognition later in life. However, it abolishes innate odor preference and alters the patterns of activation in brain centers. Moreover, exposure to an innately aversive odor during the critical period abolishes aversion in adulthood in an odor specific manner. The loss of innate aversion is associated with broadened projection of OSNs expressing the cognate receptor such that they innervate ectopic glomeruli in the olfactory bulb. These results indicate that a delicate balance of neural activity is required during critical period in establishing innate odor preference and that ectopic projection is a convergent mechanism to alter innate odor valence.

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Odorant Receptors in the Formation of the Olfactory Bulb Circuitry

Physiology ◽

10.1152/physiol.00015.2012 ◽

2012 ◽

Vol 27 (4) ◽

pp. 200-212 ◽

Cited By ~ 14

Author(s):

Claudia Lodovichi ◽

Leonardo Belluscio

Keyword(s):

Olfactory Bulb ◽

Axon Guidance ◽

Sensory Neurons ◽

Odorant Receptors ◽

Olfactory Sensory Neurons ◽

Neural Connectivity ◽

Axon Terminals ◽

Primary Function

In mammals, smell is mediated by odorant receptors expressed by sensory neurons in the nose. These specialized receptors are found both on olfactory sensory neurons' cilia and axon terminals. Although the primary function of ciliary odorant receptors is to detect odorants, their axonal role remains unclear but is thought to involve axon guidance. This review discusses findings that show axonal odorant receptors are indeed functional and capable of modulating neural connectivity.

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The olfactory critical period is determined by activity-dependent Sema7A/PlxnC1 signaling within glomeruli

eLife ◽

10.7554/elife.65078 ◽

2021 ◽

Vol 10 ◽

Author(s):

Nobuko Inoue ◽

Hirofumi Nishizumi ◽

Rumi Ooyama ◽

Kazutaka Mogi ◽

Katsuhiko Nishimori ◽

...

Keyword(s):

Sensory Neurons ◽

Knockout Mice ◽

Critical Period ◽

Olfactory Sensory Neurons ◽

Early Exposure ◽

Signaling Molecule ◽

Tufted Cells ◽

Olfactory Imprinting ◽

Activity Dependent ◽

Positive Quality

In mice, early exposure to environmental odors affects social behaviors later in life. A signaling molecule, Semaphorin 7A (Sema7A), is induced in the odor-responding olfactory sensory neurons. Plexin C1 (PlxnC1), a receptor for Sema7A, is expressed in mitral/tufted cells, whose dendrite-localization is restricted to the first week after birth. Sema7A/PlxnC1 signaling promotes post-synaptic events and dendrite selection in mitral/tufted cells, resulting in glomerular enlargement that causes an increase in sensitivity to the experienced odor. Neonatal odor experience also induces positive responses to the imprinted odor. Knockout and rescue experiments indicate that oxytocin in neonates is responsible for imposing positive quality on imprinted memory. In the oxytocin knockout mice, the sensitivity to the imprinted odor increases, but positive responses cannot be promoted, indicating that Sema7A/PlxnC1 signaling and oxytocin separately function. These results give new insights into our understanding of olfactory imprinting during the neonatal critical period.

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O1-02-06: The Alzheimer's beta-secretase enzyme BACE1 is required for accurate axon guidance of olfactory sensory neurons and normal glomerulus formation in the olfactory bulb

Alzheimer s & Dementia ◽

10.1016/j.jalz.2012.05.213 ◽

2012 ◽

Vol 8 (4S_Part_2) ◽

pp. P87-P88 ◽

Cited By ~ 1

Author(s):

Tharu Rajapaksha ◽

Robert Vassar

Keyword(s):

Olfactory Bulb ◽

Axon Guidance ◽

Sensory Neurons ◽

Olfactory Sensory Neurons ◽

Beta Secretase

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The Alzheimer's β-secretase enzyme BACE1 is required for accurate axon guidance of olfactory sensory neurons and normal glomerulus formation in the olfactory bulb

Molecular Neurodegeneration ◽

10.1186/1750-1326-6-88 ◽

2011 ◽

Vol 6 (1) ◽

pp. 88 ◽

Cited By ~ 69

Author(s):

Tharinda W Rajapaksha ◽

William A Eimer ◽

Thomas C Bozza ◽

Robert Vassar

Keyword(s):

Olfactory Bulb ◽

Axon Guidance ◽

Sensory Neurons ◽

Olfactory Sensory Neurons

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Axon Guidance of Olfactory Sensory Neurons in Zebrafish

Chemical Senses ◽

10.1093/chemse/bjh129 ◽

2005 ◽

Vol 30 (Supplement 1) ◽

pp. i92-i93 ◽

Cited By ~ 1

Author(s):

N. Miyasaka

Keyword(s):

Axon Guidance ◽

Sensory Neurons ◽

Olfactory Sensory Neurons

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Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1518329113 ◽

2016 ◽

Vol 113 (7) ◽

pp. E902-E911 ◽

Cited By ~ 27

Author(s):

Li-Hui Cao ◽

Bi-Yang Jing ◽

Dong Yang ◽

Xiankun Zeng ◽

Ying Shen ◽

...

Keyword(s):

Sensory Neurons ◽

Neural Activity ◽

Odorant Receptors ◽

Olfactory Sensory Neurons ◽

Intracellular Recordings ◽

Patch Clamp Technique ◽

Current Voltage ◽

Opposing Effects ◽

Induced Changes ◽

Odor Sensitivity

In Drosophila, olfactory sensory neurons (OSNs) rely primarily on two types of chemoreceptors, odorant receptors (Ors) and ionotropic receptors (Irs), to convert odor stimuli into neural activity. The cellular signaling of these receptors in their native OSNs remains unclear because of the difficulty of obtaining intracellular recordings from Drosophila OSNs. Here, we developed an antennal preparation that enabled the first recordings (to our knowledge) from targeted Drosophila OSNs through a patch-clamp technique. We found that brief odor pulses triggered graded inward receptor currents with distinct response kinetics and current–voltage relationships between Or- and Ir-driven responses. When stimulated with long-step odors, the receptor current of Ir-expressing OSNs did not adapt. In contrast, Or-expressing OSNs showed a strong Ca2+-dependent adaptation. The adaptation-induced changes in odor sensitivity obeyed the Weber–Fechner relation; however, surprisingly, the incremental sensitivity was reduced at low odor backgrounds but increased at high odor backgrounds. Our model for odor adaptation revealed two opposing effects of adaptation, desensitization and prevention of saturation, in dynamically adjusting odor sensitivity and extending the sensory operating range.

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A critical period terminates the differentiation of olfactory sensory neurons

10.1101/2020.02.12.945428 ◽

2020 ◽

Author(s):

Shadi Jafari ◽

Mattias Alenius

Keyword(s):

Gene Regulation ◽

Sensory Neurons ◽

Critical Period ◽

Odorant Receptor ◽

Terminal Differentiation ◽

Olfactory Sensory Neurons ◽

Genetic Studies ◽

Vast Number ◽

Gene Regulatory ◽

Or Gene

AbstractDevelopment generates a vast number of neuron types and classes. When and how neuronal differentiation end is poorly understood. Here, we show that Drosophila olfactory sensory neurons (OSNs) matures during a critical period and reveal that the differentiation termination mechanism is similar to the mammalian odorant receptor (OR) choice mechanism. We first showed that initiation of Drosophila OR expression required heterochromatin opening and a H3K9me3 demethylase, Kdm4b. Further genetic studies demonstrated that Lsd1 and su(var)3-9, similar to mouse, were required to balance heterochromatin in order to stabilize OR expression. Expression analysis showed that Lsd1, su(var)3-9 increased and Kdm4b decreased during the first two days after eclosion. We further showed that environment changes during the period, but not after, caused permanent transformed Lsd1, su(var)3-9 and Kdm4b expression and altered OR gene regulation. These results together suggest the last step in OSN terminal differentiation to be a gene regulatory critical period.

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