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Try out PMC Labs and tell us what you think. Learn More. Author contributions: R. A major component of perception is hedonic valence: perceiving stimuli as pleasant or unpleasant. Here, we used early olfactory experiences that shape odor preferences and aversions to explore developmental plasticity in circuits mediating odor hedonics.
We used 2-deoxyglucose autoradiographic mapping of neural activity to identify circuits differentially activated by biologically relevant preferred and avoided odors across rat development. We then further probed this system by increasing or decreasing hedonic value. Hedonic responses to these biologically important odors were modified through diet suppression of the maternal odor and co-rearing with a male. Early experience ificantly modified odor-evoked circuitry in an age-dependent manner.
For example, co-rearing with a male, which induced pup attraction to male odor, reduced activity in amygdala regions normally activated by the unfamiliar avoided male odor, making this region more consistent with maternal odor. Understanding the development of odor hedonics, particularly within the context of altered early life experience, provides insight into the development of sensory processes, food preferences, and the formation of social affiliations, among other behaviors.
Experiences can shape hedonic valence. Understanding the role of changing brain circuitry during development and its impact on behavioral function is critical for understanding sensory processing across development. These data converge with exciting literature on the brain's hedonic network and highlight the ificant role of early life experience in shaping the neural networks of highly biologically relevant stimuli. This may be particularly true in the olfactory system, which is heavily and reciprocally connected to limbic structures such as the amygdala, orbitofrontal cortex OFCand hippocampus in humans and other mammals.
In fact, activity of second-order neurons in the Ladies want hot sex Orangeburg NewYork 10962 bulb OB convey information about learned Wilson et al. Furthermore, learned aversive and appetitive odors differentially activate rat anterior aPCX and posterior pPCX piriform cortex Moriceau and Sullivan, b ; Moriceau et al. For example, in addition to primary sensory areas, odors varying in hedonic valence are differentially encoded by activity within the amygdala, OFC, and other regions Schoenbaum et al.
Convergence of olfactory pathway and limbic circuits could therefore help tag odor hedonics to the representation of the odor itself. Odor hedonics are a major factor in varied functions such as food preferences and social affiliations Doty, Life-long odor preferences and aversions are often shaped by early developmental experience Mennella and Beauchamp, ; Doty, ; Herz et al.
The olfactory system has an early functional development, playing an important role in mammalian infant approach to the mother in humans and nonhumans Sullivan and Toubas, ; Raineki et al. Odor learning during the perinatal period can induce odor preferences and aversions that shape odor-guided behavior throughout Ladies want hot sex Orangeburg NewYork 10962 Fillion and Blass, ; Mennella et al.
However, the olfactory system does not function in isolation of other brain regions and has extensive reciprocal connections with circuits involved in emotion and memory Gottfried, ; Martinez-Marcos, This larger network within which the olfactory system functions can show a much more extended developmental emergence Cunningham et al. Here, we explored the ontogeny of behavioral and neural network responses to biologically relevant odors maternal odor and male odor from birth to weaning in rats.
Maternal odor induces attraction at all of these ages, although the attraction weakens in some aspects as pups approach weaning. In contrast, male odor in pups raised exclusively with the mother is highly aversive to pups. We used 2-deoyxglucose 2-DG metabolic mapping to identify neural circuit components and their functional connectivity activated in response to these hedonically different odors at different ages.
We found that, although network membership changed with development, core circuits differentially active during preferred and avoided odors were present across early development. In addition, we modified the hedonic valence of these same odors through early experience e. This allowed us to identify circuits selective for preferred or aversive odors in isolation of the actual identity of the odor.
Our demonstrate how odor hedonic-valence-specific neural circuits emerge and elaborate during early development to allow appropriate odor-guided behavior during a time of dramatic changes in an animal's ecological niche. Day of birth was considered PN, and litters were culled to 12 pups 6 males, 6 females on PN1. Food and water were available ad libitum. All subjects were used only one time and all procedures were approved by the Institutional Animal Care and Use Committee in accordance with guidelines from the National Institutes of Health.
A total of males and females were used, with equal s of males and females ased to each group. Mothers were fed normal rat chow Purina LabDiet Maternal odor was suppressed via administration of a sucrose-based, fat-sufficient diet Harlan Teklad TD. Because maternal odor is learned by pups, this procedure provides us with the ability to test the hedonics of maternal odor in pups that have not learned the natural maternal odor Teicher and Blass, ; Sullivan et al. This procedure blocks the emergence of threat to male odor at PN10 and provides a method with which to assess the neural basis of the hedonics of male odor without activation of the threat system Mennella and Moltz, For biological odors maternal and male odorthe experimental odor was delivered via a flow dilution olfactometer and the control odor was a familiar odor of clean wood shavings 20 ml in a Petri dish.
These odorants were chosen based on odor preference data published by Khan et al. For each trial, the pup was given 1 min to make a choice. It was considered a choice when the pup's entire body entered the alleyway of an arm Sullivan and Wilson, ; Moriceau et al.
The two biological odors used were maternal odor and male odor. For maternal odor, two anesthetized mothers were placed in an airtight chamber connected to a flow dilution olfactometer Raineki et al. Maternal odor is diet-dependent, so Ladies want hot sex Orangeburg NewYork 10962 will approach any lactating mother on the same diet as their own mother Leon,; Sullivan et al.
For male odor, an awake male was placed in an airtight chamber connected to a flow dilution olfactometer. In the case of familiar male odor, a father housed in the same colony on same diet as the test litters' fathers was placed into the olfactometer. Individual activity levels during odor presentations were scored using automated-tracking with Ethovision software Noldus. Before testing, a mother was anesthetized with urethane to prevent milk letdown. The natural maternal odor was eliminated from the mother's ventrum for this test and reintroduced via an airstream infused throughout the testing environment from underneath a screen mesh floor supporting the mother and pup.
This procedure induces nipple attachment onto a mother with maternal odor removed and indicates that the odor does not have to be on the mother's ventrum to induce pup nipple attachment Raineki et al. The ventrum of the mother was washed with acetone, alcohol, and then water, to remove the maternal odor Hofer et al.
The pup was then placed on the opposite side of the chamber. Latency to nipple attach was recorded throughout the 3 min test. We have used this procedure in studies Raineki et al. The rationale for this test is that pups require maternal odor to nipple attach; without maternal odor, nipple attachment does not occur Hofer et al.
Maternal odor is learned and raising pups without exposure to the natural maternal odor removes Ladies want hot sex Orangeburg NewYork 10962 odor's ability to support nipple attachment the suppressed maternal odor group. These pups do nipple attach, but now rely on their mother's new maternal odor, which is not dependent upon gut bacteria and is sufficient to produce the OB changes induced by natural maternal odor in typically reared pups Sullivan et al.
Therefore, in this test, pups raised with a mother fed a diet that suppressed the natural maternal odor would be expected to fail to nipple attach to a naturally odorized mother or a washed mother with natural maternal odor infused in the air surrounding the pup Sullivan et al. Regions of interest ROIs were analyzed using ImageJ software, a computer-based system for quantitative optical densitometry.
For computing 2-DG uptake, autoradiographic density was measured in both hemispheres of the brain for each ROI described below and then averaged across both hemispheres. Four brain slices per ROI were analyzed per animal and the reported reflect an average of relative 2-DG uptake across all four slices.
An increase in autoradiographic density indicates increased neural activation, but does not differentiate between inhibitory and excitatory activity. All analyses were conducted by investigators blinded to the experimental conditions. We have used this procedure frequently in studies Sullivan and Wilson, ; Landers and Sullivan, ; Sullivan et al. No staining was required for the analysis of the OB because anatomical landmarks are visible with 2-DG Fig.
Specific nuclei and anatomical landmarks were identified by staining sections with cresyl violet after exposure and used to make template overlays for the autoradiographs Fig. With the aid of a stereotaxic atlas Paxinos and Watson,brain areas were outlined Fig. Behavioral and 2-DG uptake data were analyzed by ANOVA followed by post hoc Fisher's tests between individual groups or Student's t tests in cases with two experimental groups. Bivariate correlation matrices were created by computing ratios of mean 2-DG uptake Ladies want hot sex Orangeburg NewYork 10962 all pairwise combinations of brain regions analyzed for maternal, male, and no odor at each age.
For quantitative analyses of functional connectivity, the difference between each odor's correlation matrix and the no odor correlation matrix was computed at each age and group differences were analyzed by ANOVA followed by post hoc Fisher's tests. In Experiment 1, we assessed distributed brain regions both within and outside the primary olfactory pathway for their modulation of activity in concert with the hedonic valence of an odorant stimulus across ontogeny. All Y-maze choices were made between the experimental odor and a familiar odor clean beddingthus showing whether odors were of increasing or decreasing hedonic value relative to Ladies want hot sex Orangeburg NewYork 10962 familiar odor.
Approach and avoidance responses to odorants remained relatively stable throughout development. Male odor consistently elicited the most avoidance and maternal odor consistently elicited the most approach across development. The response to maternal and male odor is plotted in both saturated and 10 PPM odorant graphs to allow comparison.
For diluted 10 PPM odors, no ificant interaction between age and odor was found Fig. When 2-DG responses to odors were analyzed with sex as a variable, no sex differences were found. Bivariate correlation matrices representing the ratios of mean 14 C 2-DG uptake calculated between all pairwise brain regions analyzed in response to maternal, male, or no odor presentations at PN Core olfactory areas are shown in purple and red, amygdala areas in blue, hippocampus subareas in black, and orbitofrontal and PCX areas in green. Changes in functional connectivity across odors and ages can be observed in specific neural network modules.
Mean difference in z -score-converted correlations of mean 14 C 2-DG uptake between biological odors male odor, maternal odor and the no odor control condition in three different network modules across age.
BPFC-olfactory cortex module. CAmygdala-hippocampus module. A ificant main effect of age was found Fig. Therefore, within the primary olfactory regions, biological-odor-evoked pPCX activity emerged later than the other regions and the pPCX was the only region to differentiate between maternal and male odor. However, a ificant main effect of odor was found Fig. Post hoc tests indicated that male and maternal odor consistently activated the CA1 across early development relative to no odor.
For example, a single data point represents the correlation between 2-DG uptake in a given brain region across all animals at that age with uptake in a different region in the same animals.Ladies want hot sex Orangeburg NewYork 10962
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